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THE HUMAN FRONTAL LOBES
 THE SCIENCE AND PRACTICE OF NEUROPSYCHOLOGY
A Guilford Series
Robert A. Bornstein, Series Editor

The Human Frontal Lobes: Functions and Disorders, Second Edition

Bruce L. Miller and Jeffrey L. Cummings, Editors

Developmental Motor Disorders: A Neuropsychological Perspective

Deborah Dewey and David E. Tupper, Editors

Cognitive and Behavioral Rehabilitation: From Neurobiology to Clinical Practice

Jennie Ponsford, Editor

Aphasia and Language: Theory to Practice

Stephen E. Nadeau, Leslie J. Gonzalez Rothi, and Bruce A. Crosson, Editors

Pediatric Neuropsychology: Research, Theory, and Practice

Keith Owen Yeates, M. Douglas Ris, and H. Gerry Taylor, Editors
 THE HUMAN
FRONTAL LOBES
Functions and Disorders
SECOND EDITION

Edited by

BRUCE L. MILLER
JEFFREY L. CUMMINGS

Series Editor’s Note by Robert A. Bornstein

THE GUILFORD PRESS

New York London
© 2007 The Guilford Press
A Division of Guilford Publications, Inc.
72 Spring Street, New York, NY 10012
www.guilford.com

All rights reserved

No part of this book may be reproduced, translated, stored in a retrieval system, or

transmitted, in any form or by any means, electronic, mechanical, photocopying,
microfilming, recording, or otherwise, without written permission from the Publisher.

Printed in the United States of America

This book is printed on acid-free paper.

Last digit is print number: 9 8 7 6 5 4 3 2 1

Library of Congress Cataloging-in-Publication Data

The human frontal lobes : functions and disorders / edited by Bruce L.
Miller, Jeffrey L. Cummings.—2nd ed.
p. cm.—(The science and practice of neuropsychology)
Includes bibliographical references and index.
ISBN-10: 1-59385-329-7 ISBN-13: 978-1-59385-329-7 (hardcover)
1. Frontal lobes—Physiology. 2. Frontal lobes—Pathophysiology.
3. Frontal lobes—Physiology. 4. Frontal lobes—Pathophysiology.
I. Miller, Bruce L., 1949– . II. Cummings, Jeffrey L., 1948– .
III. Series.
[DNLM: 1. Frontal Lobe—physiology. 2. Brain Diseases. 3. Mental
Disorders. WL 307 H918 2007]
QP382.F7H85 2007
612.8′25—dc22
2006002478
 About the Editors

Bruce L. Miller, MD, is Professor of Neurology at the University of California at San

Francisco (UCSF), where he holds the A.W. & Mary Margaret Clausen Distin-
guished Chair. He is also the clinical director of the aging and dementia program at
UCSF, where he heads the State of California Research and Clinical Center and a
new National Alzheimer’s Disease Research Center. For nearly two decades, Dr.
Miller has been the scientific director of the John Douglas French Foundation for
Alzheimer’s Disease, for which he has organized conferences, scientific consortiums,
and grant programs. He has been listed in The Best Doctors in America since 1996.
Dr. Miller directs a National Institutes of Health–funded program on fronto-
temporal dementia (FTD) called “FTD: Genes, Images, and Emotions.” He has pub-
lished more than 250 articles.

Jeffrey L. Cummings, MD, is Director of the Alzheimer’s Disease Research Center

and the Deane F. Johnson Center for Neurotherapeutics at the University of Califor-
nia at Los Angeles (UCLA). He is the Augustus S. Rose Professor of Neurology and
Professor of Psychiatry and Biobehavioral Sciences in the David Geffen School of
Medicine at UCLA. Dr. Cummings is past president of the American Neuropsychiat-
ric Society and the Behavioral Neurology Society. He is the recipient of several pres-
tigious awards, including the Henderson Lectureship of the American Neurological
Society. Dr. Cummings has lectured, pursued research, and produced a body of
research-related publications on the topics of neuropsychiatry, behavioral neurology,
neurotherapeutics, and drug development. He has contributed to the understanding
of the role of the frontal–subcortical circuits in the behavior of normal individuals
and of persons with brain disorders and is the author of the Neuropsychiatric Inven-
tory, a tool used to assess behavioral changes in patients with neurological diseases.

v
 Contributors

Judith Aharon-Peretz, MD, Cognitive Neurology Unit, Rambam Health Care

Campus, Haifa, Israel
Serena Amici, MD, Memory and Aging Center, Department of Neurology, University
of California, San Francisco, California
Michel Benoit, MD, PhD, Centre Mémoire de Ressources et de Recherche, Centre
Hospitalier Universitaire de Nice, Nice, France
Antonello Bonci, MD, PhD, Memory and Aging Center, Department of Neurology,
University of California, San Francisco, California
Adam L. Boxer, MD, PhD, Memory and Aging Center, Department of Neurology,
University of California, San Francisco, California
Arne Brun, MD, PhD, Department of Pathology, Lund University Hospital, Lund,
Sweden
Hervé Caci, MD, PhD, Pédopsychiatre, Centre Hospitalier Universitaire de Nice,
Nice, France
Nigel J. Cairns, PhD, Department of Neurology, Washington University in St. Louis,
St. Louis, Missouri
Danielle Andrea Carlin, BA, Memory and Aging Center, Department of Neurology,
University of California, San Francisco, California
Tiffany W. Chow, MD, Departments of Medicine (Neurology Division) and
Psychiatry (Geriatric Psychiatry Division), University of Toronto, and Rotman
Research Institute, Baycrest, Toronto, Ontario, Canada
Helena Chui, MD, Department of Neurology, Keck School of Medicine, University
of Southern California, Los Angeles, California
Julia A. Chung, MD, Department of Psychiatry and Biobehavioral Science, Harbor–
UCLA Medical Center, Torrance, California
Jeffrey L. Cummings, MD, Department of Neurology and Alzheimer’s Disease
Research Center, University of California, Los Angeles, California
David Dean, BA, Memory and Aging Center, Department of Neurology, University
of California, San Francisco, California

vii
viii Contributors

Mary G. DeMay, MD, Memory and Aging Center, Department of Neurology,

University of California, San Francisco, California
Mark D’Esposito, MD, Department of Psychology, University of California, Berkeley,
California
Bruno Dubois, MD, Fédération de Neurologie, Hôpital de la Salpêtrière,
Paris, France
Laura B. Dunn, MD, Department of Psychiatry, University of California, San Diego,
La Jolla, California
Denys Fontaine, MD, Neurochirurgie, Centre Hospitalier Universitaire de Nice, Nice,
France
Adam Gazzaley, MD, PhD, Departments of Neurology and Physiology, University of
California, San Francisco, California, and Department of Neuroscience, University of
California, Berkeley, California
Daniel H. Geschwind, MD, PhD, Departments of Neurology and Psychiatry and
Biobehavioral Sciences, University of California, Los Angeles, California
Michael D. Geschwind, MD, PhD, Memory and Aging Center, Department of
Neurology, University of California, San Francisco, California
Jill Goldman, MA, MPhil, Memory and Aging Center, Department of Neurology,
University of California, San Francisco, California
Maria Luisa Gorno-Tempini, MD, PhD, Memory and Aging Center, Department of
Neurology, University of California, San Francisco, California
Cheryl L. Grady, PhD, Department of Psychiatry, University of Toronto, and Rotman
Research Institute, Baycrest, Toronto, Ontario, Canada
Jordan Grafman, PhD, Cognitive Neuroscience Section, National Institute of
Neurological Disorders and Stroke, National Institutes of Health, Bethesda,
Maryland
Murray Grossman, MD, Department of Neurology, University of Pennsylvania,
Philadelphia, Pennsylvania
Elizabeth Head, PhD, Department of Neurology, University of California, Irvine,
California
Argye E. Hillis, MD, Department of Neurology, Johns Hopkins School of Medicine,
Baltimore, Maryland
Marco Iacoboni, MD, PhD, Departments of Neurology, Psychiatry and Biobehavioral
Sciences, and Psychology, University of California, Los Angeles, California
Harry J. Jerison, PhD, Department of Psychiatry and Biobehavioral Sciences,
University of California, Los Angeles, California
Julene K. Johnson, PhD, Memory and Aging Center, Department of Neurology,
University of California, San Francisco, California
Susan Jones, PhD, Department of Physiology, Development and Neuroscience,
University of Cambridge, Cambridge, United Kingdom
 Contributors ix

Jason H. T. Karlawish, MD, Division of Geriatric Medicine, Department of

Medicine, University of Pennsylvania, Philadelphia, Pennsylvania
Daniel I. Kaufer, MD, Department of Neurology, University of North Carolina
School of Medicine, Chapel Hill, North Carolina
Joel H. Kramer, PsyD, Memory and Aging Center, Department of Neurology,
University of California, San Francisco, California
Ae Young Lee, MD, Department of Neurology, Chungnam National University
School of Medicine, Taejon, Korea
Virginia M.-Y. Lee, PhD, Department of Pathology and Laboratory Medicine,
University of Pennsylvania School of Medicine, Philadelphia, Pennsylvania
Ira M. Lesser, MD, Department of Psychiatry and Biobehavioral Science, Harbor-
UCLA Medical Center, Torrance, California
Brian Levine, PhD, Department of Psychology, University of Toronto, and Rotman
Research Institute, Baycrest, Toronto, Ontario, Canada
Irene Litvan, MD, Department of Neurology, University of Louisville School of
Medicine, Louisville, Kentucky
Vianney Mattei, MD, Psychiatrie, Centre Hospitalier Universitaire de Nice, Nice,
France
Ian G. McKeith, MD, School of Neurology, Neurobiology, and Psychiatry, University
of Newcastle upon Tyne, and Wolfson Research Centre, Newcastle General Hospital,
Newcastle upon Tyne, United Kingdom
Margaret C. McKinnon, PhD, Department of Psychology, University of Toronto,
and Rotman Research Institute, Baycrest, Toronto, Ontario, Canada
Bruce L. Miller, MD, Memory and Aging Center, Department of Neurology,
University of California, San Francisco, California
Jennifer Ogar, MS, Center for Aphasia and Related Disorders, VA Northern
California Health Care System, Martinez, California
Barton W. Palmer, PhD, Department of Psychiatry, University of California, San
Diego, La Jolla, California
Danijela Pavlic, BS, Memory and Aging Center, Department of Neurology, University
of California, San Francisco, California
William Perry, PhD, Department of Psychiatry, University of California, San Diego,
La Jolla, California
Bernard Pillon, PhD, Centre de Neuropsychologie, Fédération de Neurologie, Hôpital
de la Salpêtrière, Paris, France
Bruce H. Price, MD, Department of Neurology, McLean Hospital, Harvard Medical
School, Belmont, Massachusetts
Lovingly Quitania, BA, Memory and Aging Center, Department of Neurology,
University of California, San Francisco, California
x Contributors

Katherine P. Rankin, PhD, Memory and Aging Center, Department of Neurology,

University of California, San Francisco, California
Scott L. Rauch, MD, Department of Psychiatry, Massachusetts General Hospital,
Harvard Medical School, Charlestown, Massachusetts
Philippe H. Robert, MD, Centre Mémoire de Ressources et de Recherche, Centre
Hospitalier Universitaire de Nice, Nice, France
Susan A. Legendre Ropacki, PhD, Department of Psychology, Loma Linda University,
Loma Linda, California
Howard Rosen, MD, Memory and Aging Center, Department of Neurology,
University of California, San Francisco, California
Carole Samango-Sprouse, EdD, Department of Pediatrics, George Washington
University, Washington, DC
Douglas W. Scharre, MD, Department of Neurology, Ohio State University,
Columbus, Ohio
William W. Seeley, MD, Memory and Aging Center, Department of Neurology,
University of California, San Francisco, California
W. Dale Stevens, MSc, Department of Psychology, Harvard University, Cambridge,
Massachusetts
Virginia E. Sturm, MD, Department of Psychology, University of California, Berkeley,
California
Donald T. Stuss, PhD, Departments of Medicine and Psychology, University
of Toronto, and Rotman Research Institute, Baycrest, Toronto, Ontario, Canada
Eva Svoboda, PhD, Department of Psychology, University of Toronto, and Rotman
Research Institute, Baycrest, Toronto, Ontario, Canada
Rachel Tomer, PhD, Department of Psychology, University of Haifa, Haifa, Israel
John Q. Trojanowski, PhD, Department of Pathology and Laboratory Medicine,
University of Pennsylvania School of Medicine, Philadelphia, Pennsylvania
Irene van Balkan, MD, Department of Neurology, University of Louisville School of
Medicine, Louisville, Kentucky
Pei-Ning Wang, MD, Neurological Institute, Taipei Veterans General Hospital,
and Department of Neurology, National Yang-Ming University School of Medicine,
Taipei, Taiwan
Anthony P. Weiss, MD, Department of Psychiatry, Massachusetts General Hospital,
Harvard Medical School, Charlestown, Massachusetts
Grace Yoon, MD, Memory and Aging Center, Department of Neurology, University
of California, San Francisco, California
 Series Editor’s Note

The second edition of The Human Frontal Lobes represents a window into the rapid
growth of our knowledge on the functions of the frontal lobe. In the few years since
the first edition was released, the sophistication of our understanding, and the tech-
nologies and techniques that have been developed, continue to expand the horizons
of our appreciation of frontal lobe functions and their centrality in human behavior.
This edition reflects the vast increase in knowledge that has been accrued over the
past 8 years. Drs. Miller and Cummings have assembled an all-star team of basic and
clinical scientists who provide a comprehensive review of the frontal lobes, including
cytoarchitectonics, neurotransmitter systems, and neuroimaging. In keeping with
the rapid growth in knowledge and evolving technologies, the section on imaging
techniques has been significantly expanded. Similarly, the sections on neurological
and psychiatric diseases reflect the increasing awareness of the frontal lobes in
a broad range of disorders, as well as our enhanced understanding of the
pathophysiological mechanisms underlying these diseases.
The first edition of this book was the inaugural volume of the Guilford series The
Science and Practice of Neuropsychology. The goal of this series is to integrate the
scientific foundations and clinical applications of knowledge of brain–behavior rela-
tionships. The study of the frontal lobes is in many regards at the leading edge of the
neuroscience knowledge explosion that has fundamentally revised many traditional
concepts and constructs. This second edition demonstrates how rapidly the field is
advancing.

ROBERT A. BORNSTEIN, PhD

xi
 Preface

Since the publication of the first edition of The Human Frontal Lobes in 1999, scien-
tific understanding of the frontal lobes has greatly advanced, with the fields of neu-
ropsychology, neuroimaging, and neuroscience all contributing to a rapidly chang-
ing perspective on the role of the frontal lobes in behavior and cognition. Not only
are these advances important for understanding the neuroanatomy, neurophysi-
ology, and neurochemistry of frontal lobe function, but they have also altered clini-
cal approaches to the evaluation of patients with frontal lobe disorders. This chang-
ing landscape is reflected in this book’s new edition. This second edition of The
Human Frontal Lobes brings an international perspective to the organization, func-
tion, and role in disease of the frontal lobes, and the chapter authors come from a
wide variety of specialties.
The neuroanatomical section of this book is reorganized and expanded to reflect
the evolving understanding of frontal lobe divisions. Increasingly, frontal lobe divi-
sions are influenced by a better understanding of the circuits and connections associ-
ated with specific frontal areas. Harry J. Jerison contributes a fascinating chapter on
evolution that challenges existing paradigms regarding selective growth of pre-
frontal regions. Daniel H. Geschwind and Marco Iacoboni, leaders in our under-
standing of brain asymmetries, further pursue novel aspects of prefrontal anatomy
by describing differences in left versus right prefrontal structure, changes that reflect
these unique aspects of human anatomy. Other chapters in this section explore the
anatomy of prefrontal cortex from the histological to the gross morphological level.
These contributions are lively and accessible to a broad audience ranging from clini-
cians to basic scientists. Similarly, the neurochemistry section of this book reflects
new concepts regarding the roles of serotonin, acetylcholine, and dopamine in the
cognitive and emotional functions of the frontal lobe. The role of dopamine in
reward and learning is emphasized in a new chapter from Antonello Bonci and
Susan Jones.
Over the past 7 years the field of functional imaging has expanded, leading to a
comprehensive picture of the circuitry that contributes to the cognitive and emo-
tional underpinnings of frontal lobe function. The sections on functional and struc-
tural imaging and on neuropsychological functions reflect this evolving story.
Howard Rosen and David Dean offer a new chapter on structural imaging and
Adam L. Boxer describes the role that the frontal lobes play in the planning of move-

xiii
xiv Preface

ment. A new chapter from Margaret McKinnon and colleagues discusses the key
role of frontal cortex in autobiographical memory, and Adam Gazzaley and Mark
D’Esposito outline the anatomy and testing of working memory.
The neuropsychology section has chapters that range from practical to theoretical.
Joel H. Kramer and Lovingly Quitania offer a practical approach to bedside neuro-
psychological testing, while Donald T. Stuss explores more experimental approaches
to frontal testing. The critical roles of the frontal lobes in personality and emotion
are described in a new chapter from Katherine P. Rankin.
The clinical chapters reflect an explosion of new findings regarding the critical
functions of the frontal lobes in the major degenerative disorders. A new series of
chapters explore the clinical (Pei-Ning Wang and Bruce L. Miller), imaging (Murray
Grossman), and neuropathological (Nigel J. Cairns and colleagues) features of
frontotemporal dementia and related disorders. Finally, the wide range of neurologi-
cal and psychiatric syndromes that are driven by loss of function in prefrontal cortex
are described.
The Human Frontal Lobes is recommended for readers who enjoyed the first edi-
tion of this book and for new readers interested in the rapidly evolving story regard-
ing the role of the prefrontal cortex in human disease.
 Dedication and Acknowledgments

We dedicate this book to Milton Miller (Bruce L. Miller’s father), who succumbed to
a brain tumor in 2005 during the preparation phase of this book. As a physician and
psychiatrist, Milton was enormously influential, modeling interactions with patients
that would affect generations of students. As a chair of psychiatry at Harbor–UCLA
Medical Center in Los Angeles, he was a leader in the psychiatric community and
improved the care of thousands of indigent patients with mental illnesses. As a
thinker and philosopher, he was able to see his way through complex ideas and
develop a vision that others could follow. As a father, he was remarkable and his
wonderful wit and wisdom will live on in his sons.
We both were highly influenced by D. Frank Benson, MD. Frank was a leader in
behavioral neurology in Boston before becoming the Augustus S. Rose Professor of
Neurology at UCLA. Dr. Cummings worked with Dr. Benson as a resident and fel-
low in Boston and as a colleague throughout the time Frank lived in Los Angeles. Dr.
Miller was one of the first fellows to be trained in Los Angeles after Frank’s move to
UCLA. As an insightful clinician and enthusiastic teacher, he inspired all who had
the privilege of studying with him. He was particularly fascinated by the frontal lobe
disorders, and our interest in the clinical phenomenology of frontal lobe dysfunction
can be traced largely to his influence.
We have the good fortune of being in departments that have outstanding leaders
who promote and encourage our investigation into the clinical neurobiology of
human behavior. We gratefully acknowledge the support of Dr. Stephen Hauser at
UCSF and Dr. John Mazziotta at UCLA.
Our work on the frontal lobes and particularly the frontotemporal dementias has
been greatly facilitated by center and program project grants from the National
Institute on Aging. Neil Buckholtz, Tony Phelps, and Elizabeth Koss were instru-
mental in facilitating these studies.
Academic productivity and scholarship can exist only where there is support from
one’s family and loved ones. I (B. L. M.) have the great joy of Debbie’s unstinting
love and encouragement. And I (J. L. C.) found new light in life with Kate (Xue)
Zhong.

xv
 Contents

PART I. OVERVIEW OF THE FRONTAL LOBES

1. The Human Frontal Lobes: An Introduction 3

Bruce L. Miller
2. Conceptual and Clinical Aspects of the Frontal Lobes 12
Jeffrey L. Cummings and Bruce L. Miller

PART II. ANATOMY

3. Frontal-Subcortical Circuits 25
Tiffany W. Chow and Jeffrey L. Cummings
4. The Dorsolateral and Cingulate Cortex 44
Daniel I. Kaufer
5. The Orbitofrontal Cortex and the Insula 59
Jennifer Ogar and Maria Luisa Gorno-Tempini
6. Structural and Functional Asymmetries of the Human 68
Frontal Lobes
Daniel H. Geschwind and Marco Iacoboni
7. Gross Morphology and Architectonics 92
Danielle Andrea Carlin
8. Evolution of the Frontal Lobes 107
Harry J. Jerison

xvii
xviii Contents

PART III. NEUROCHEMISTRY

9. Serotonin and the Frontal Lobes 121

Philippe H. Robert, Michel Benoit, and Hervé Caci

10. Oiling the Gears of the Mind: Roles for Acetylcholine 135
in the Modulation of Attention
Serena Amici and Adam L. Boxer

11. The Mesocortical Dopaminergic System 145

Antonello Bonci and Susan Jones

PART IV. FUNCTIONAL AND STRUCTURAL IMAGING APPROACHES

12. Structural Imaging of the Frontal Lobes 165

Howard Rosen and David Dean

13. Unifying Prefrontal Cortex Function: Executive Control, 187

Neural Networks, and Top-Down Modulation
Adam Gazzaley and Mark D’Esposito

14. Insight into Frontal Lobe Function from Functional Neuroimaging 207
Studies of Episodic Memory
W. Dale Stevens and Cheryl L. Grady

15. The Frontal Lobes and Autobiographical Memory 227

Margaret C. McKinnon, Eva Svoboda, and Brian Levine

16. Planning and the Brain 249

Jordan Grafman

17. Principles of Motor Control by the Frontal Lobes as Revealed 262

by the Study of Voluntary Eye Movements
Adam L. Boxer

PART V. NEUROPSYCHOLOGICAL FUNCTIONS

18. Bedside Frontal Lobe Testing 279

Joel H. Kramer and Lovingly Quitania

19. New Approaches to Prefrontal Lobe Testing 292

Donald T. Stuss

20. Language and Frontal Cortex 306

Argye E. Hillis
 Contents xix

21. Self-Representation and the Frontal Lobes 317

William W. Seeley and Virginia E. Sturm
22. Frontal Dysfunction and Capacity to Consent to Treatment 335
or Research: Conceptual Considerations and Empirical Evidence
Laura B. Dunn, Barton W. Palmer, and Jason H. T. Karlawish
23. Social Cognition in Frontal Injury 345
Katherine P. Rankin

PART VI. NEUROLOGICAL DISEASES

A. Frontotemporal Dementia and Related Disorders
24. Clinical Aspects of Frontotemporal Dementia 365
Pei-Ning Wang and Bruce L. Miller
25. Genetics and Neuropathology of Frontotemporal Dementia 382
Nigel J. Cairns, Virginia M.-Y. Lee, and John Q. Trojanowski
26. Imaging in Frontotemporal Dementia 408
Murray Grossman
27. Progressive Supranuclear Palsy, Corticobasal Degeneration, 422
and the Frontal Cortex
Irene van Balken and Irene Litvan
28. Frontal Variant of Alzheimer’s Disease 429
Julene K. Johnson, Arne Brun, and Elizabeth Head

B. Other Neurological Disorders

29. Vascular Disease of the Frontal Lobes 447
Ae Young Lee and Helena Chui
30. Parkinson’s Disease with and without Dementia 472
and Lewy Body Dementia
Bruno Dubois, Bernard Pillon, and Ian G. McKeith
31. Neurosurgical Intervention for Psychiatric Illness: 505
Past, Present, and Future
Anthony P. Weiss, Scott L. Rauch, and Bruce H. Price
32. Infectious, Inflammatory, and Demyelinating Disorders 518
Douglas W. Scharre
33. Traumatic Brain Injury 540
Judith Aharon-Peretz and Rachel Tomer
xx Contents

34. Adult-Onset Genetic Disorders Involving the Frontal Lobes 552

Michael D. Geschwind, Grace Yoon, and Jill Goldman
35. Frontal Lobe Development in Childhood 576
Carole Samango-Sprouse

PART VII. PSYCHIATRIC DISEASES

36. Frontal Lobe Functioning in Schizophrenia: 597

Evidence from Neuropsychology, Cognitive Neuroscience,
and Psychophysiology
Susan A. Legendre Ropacki and William Perry
37. Bipolar Disorder and the Frontal Lobes 614
Mary G. DeMay, Danijela Pavlic, and Bruce L. Miller
38. Obsessive-Compulsive Disorder and the Frontal Lobes 621
Denys Fontaine, Vianney Mattei, and Philippe H. Robert
39. Depression and the Frontal Lobes 636
Ira M. Lesser and Julia A. Chung

Index 649
 PART I
OVERVIEW OF THE FRONTAL LOBES
 CHAPTER 1
The Human Frontal Lobes
AN INTRODUCTION

Bruce L. Miller

Recent research into the functions of the fron- frontal cortex (Berker, Berker, & Smith, 1986)
tal lobes is transforming our understanding of forever changed the way that brain–behavior
this important brain region. This chapter offers relationships would be perceived. With the
an overview of the frontal lobes and introduces emergence of new histological and anatomical
the major topics discussed in greater detail techniques by von Economo and Broadmann,
throughout this book. A historical review em- and the growth of experimental psychology,
phasizes the key developments in frontal lobe Tilney suggested in 1928 that the 20th century
research generated over the past two centuries. would become “the century of the frontal
Also, it describes the important new imaging lobes.” Yet for the first 60 years of the 20th
techniques that play an increasingly central century, biologically oriented studies of frontal
role in the study of the frontal lobes; new cog- cortex were exceedingly uncommon, and op-
nitive, social, and pharmacological approaches portunities to understand the sequelae of fron-
to frontal lobe functions; and human neurolog- tal lesions associated with stroke, tumor, trau-
ical and psychiatric diseases in which fron- ma, seizures, infections, and neurodegenerative
tal lobes or frontal–subcortical connections to or psychiatric disorders were routinely ignored.
the frontal lobes are particularly vulnerable. Even when procedures such as the frontal
Frontotemporal dementia, traumatic brain in- leukotomy emerged as a routine practice for
jury, anterior cerebral artery stroke, schiz- patients with disabling psychiatric conditions,
ophrenia, and depression are introduced as there was never a systematic attempt to under-
model systems for understanding frontal func- stand the effects of this procedure on cognition
tion. Links between subcortical and frontal or behavior.
structures are noted, and future approaches to In retrospect, this lack of scientific progress
frontal lobe research are outlined. had many causes. Undoubtedly, the formal sep-
aration of the fields of psychiatry and neurol-
ogy at the end of the 19th century had a nega-
HISTORICAL OVERVIEW OF CLINICAL ADVANCES tive influence, leaving higher cortical functions
neglected by both fields. For nearly a century,
During the 19th century, Dr. John Harlow’s de- the dominant focus of psychiatry was no longer
scription of the social changes in Phineas Gage brain–behavior relationships, whereas neurol-
following traumatic injury to the orbitofrontal ogy became the study of motor and sensory,
cortex (Macmillan, 2001) and Broca’s delinea- but not higher cortical functions. Also, the
tion of the language functions of dominant frontal lobes did not prove easily tractable to

3
4 O V E R V I E W O F T H E F R O N TA L LO B E S

clinicians; the cognitive and behavioral deficits experiences with patients who had focal le-
associated with frontal injury were not readily sions.
apparent or easily characterized. The concepts The advent of behavioral neurology under
of executive control and behavioral disorders the leadership of Norman Geschwind and D.
due to frontal lobe pathology were foreign to Frank Benson stimulated a whole generation of
the field. Similarly, imaging and the technolo- neurologists and psychologists to explore the
gies needed to measure frontal lobe function anatomical basis for cognition and behavior.
or structures were lacking. By midcentury, Benson, a student and colleague of Geschwind,
Tilney’s predictions appeared premature. was particularly intrigued by functions of the
However, by the 1960s, a few investigators frontal lobes and even traveled to Russia to ob-
began seriously to tackle questions regarding serve Luria’s patient-based approach to frontal
the function of the frontal lobes. In the area of lobe function (Benson, 1996). Benson liked to
motor systems, Penfield’s intraoperative stimu- tell how Luria’s patients and their families ap-
lation work facilitated understanding of the proached him with profound formality, re-
functional organization of motor and premotor specting his place in Russia’s rigid hierarchy.
cortex. Penfield’s work helped to elucidate the Patients with frontal lobe injury were different,
concept that the frontal lobes has three major often greeting Luria like an old friend, entering
anatomical divisions: the motor strip involved inappropriately into his personal space.
with fine coordination of movement; the pre- Benson realized that the frontal lobes had a
motor area, a region involved with the overall strong connection to social cognition, and he
organization of movement; and the prefrontal was one of the first investigators to include the
region. Stimulation of the motor strip resulted study of behavior in the evaluation of frontal
in simple movements of the affected muscles lobe function. The importance of his studies
and muscle groups, whereas with premotor and their influence on his students cannot be
stimulation, complex organized movements underemphasized. Benson stressed the impor-
were seen (Penfield, 1954). Yet Penfield seemed tance of bedside observation. He believed that
to run into a brick wall when he electrically capturing phenomenology was the first step,
stimulated prefrontal cortex. These prefrontal with theories coming later. Theories were
areas were “silent,” and Penfield was unable to greatly bolstered if they were based upon care-
explain the functions of these regions based ful clinical observations. Among the behavioral
upon these stimulation studies. neurologists of his generation, Benson was
Paul Yakovlev’s anatomical studies of the most willing to explore the interface between
frontal lobes and their connections strongly in- neurology and psychiatry, and he realized that
fluenced neurologists and pathologists, includ- the frontal lobes played an important role in
ing Norman Geschwind, D. Frank Benson, and the genesis of behaviors that were considered
Arne Brun, who went on to do important psychiatric in origin.
research into frontal lobe function. Yakovlev Some of his most original work came from
focused these emerging investigators on the his study of the role of the frontal cortex in
phylogenetic and developmental origins of disorders that were considered psychiatric
frontal cortex and the subcortical–limbic con- in origin: syndromes such as reduplicative
nections to the frontal regions (Yakovlev, paramnesia and confabulation associated with
1968). This work eventually led to important amnesia. Benson hypothesized that one possi-
new studies that explored the clinical syn- ble mechanism for delusions was the patient’s
dromes associated with frontal injury from altered monitoring of distorted or incomplete
stroke, trauma, tumor, and neurodegeneration. information (Mercer, Wapner, Gardner, &
In the second half of the 20th century, Alexan- Benson, 1977). In the case of reduplica-
der Luria and D. Frank Benson began to focus tive paramnesia, the combination of dis-
their research on the vast space of the frontal torted visual information from a posterior
lobes. Luria (1970), the innovative Russian nondominant temporal–parietal lesion and ab-
psychologist, developed novel and, even by to- normal monitoring due to a frontal lesion led
day’s standards, remarkably modern theories to delusions about the identity of a place
about frontal lobe functions. His theories (Benson et al., 1976). With confabulation asso-
about frontal lobe organization were highly ciated with amnesia, frontal injury led a patient
theoretical, but many components of Luria’s to fill in the amnesia with false information,
ideas were shaped and sharpened by his clinical whereas without the frontal injury, the confab-
 Introduction 5

ulation would not occur (Benson et al., 1996; IMAGING

Stuss & Benson, 1986).
Benson and his colleague and friend Don Neuroimaging research continues as the pre-
Stuss evaluated the effects of leukotomy on eminent technique for evaluation of the frontal
frontal lobe function (Stuss et al., 1981). This lobes. Computed tomography (CT) became
work required finding patients in whom widely available in the late 1970s; prior to that,
leukotomy has had been performed. In many clinicians had few ways to visualize the struc-
instances, Stuss and Benson found patients in ture or function of frontal cortex. Older tools,
whom the procedure had been performed years pneumoencephalography and angiography,
or even decades earlier. It represented the be- were highly invasive, painful, and sometimes
ginning of a new era, and Stuss and Benson dangerous, and offered only crude outlines of
eventually modified Luria’s classification by frontal anatomy. With CT, suddenly clinical–
suggesting that the prefrontal cortex has three anatomical correlations could be made in vivo,
major anatomical divisions: orbitofrontal, and the presence and extent of structural le-
cingulate, and dorsolateral. Whereas the sions associated with stroke, demyelination, tu-
orbitofrontal cortex modulated social control mor, or trauma became visible prior to death.
and the cingulate cortex was responsible for CT allowed researchers to explore the relation-
the generation of goal-directed behavior, the ship between volume of frontal injury and clin-
neuropsychological functions of the frontal ical status with trauma, tumor, stroke, and
cortex were localized within dorsolateral neurodegeneration. Measurement of atrophy
prefrontal regions (Stuss & Benson, 1986). became a way to differentiate between normal
These concepts have proven remarkably dura- aging and dementia, and to separate the dis-
ble across many approaches, whether lesion- tinctive dementia syndromes from each other.
based or studied in healthy controls with func- Yet CT had constraints related to the frontal
tional magnetic resonance imaging (fMRI). lobes. In particular, artifacts generated from
Others continue to evaluate the frontal lobes adjacent bone diminished visualization of
from distinctive perspectives. The concept of orbitofrontal and anterior frontal structures.
working memory pioneered by Alan Baddeley Also, resolution between gray and white matter
(2003) began the parcellation of specific fron- was limited.
tal lobe neuropsychological functions localized Development of MRI in the early 1980s cir-
to different regions in the frontal cortex. Patri- cumvented some of the problems associated
cia Goldman-Rakic and colleagues (e.g., with CT. Better resolution of gray and white
Chafee & Goldman-Rakic, 1998) emphasized matter, and disappearance of artifacts associ-
the role of a frontoparietal system in visual at- ated with bone made MRI the technique of
tention/working memory tasks and showed the choice for the evaluation of the frontal lobes.
role and anatomy of the dopaminergic compo- MRI allowed quantitative measurement of
nents of this circuit. Mark D’Esposito and col- frontal volumes, facilitating studies on the role
leagues (e.g., Ranganath & D’Esposito, 2005), of frontal cortex, or subfrontal white matter le-
Cheryl Grady (2002), and others have success- sions in the pathogenesis of a wide variety of
fully used functional imaging techniques such cognitive and behavioral syndromes.
as fMRI to evaluate this working memory sys- Volumetric region-of-interest (ROI) mea-
tem in vivo. Marsel Mesulam’s (1998) histo- sures of normal or pathological tissue, corre-
logical and phylogenetic approaches to cortical lated with specific cognitive or behavioral pa-
organization have emphasized the functional rameters, remain a widely used approach to the
organization of cortex based on connections to study the sequelae from frontal injury. Hand-
primary sensory or motor areas. With his drawn measures (ROIs) in different frontal re-
single-cell recording in rodents, Edmund gions have facilitated the study of neurological
Rolls’s (2004) pioneering research has and psychiatric disorders. However, because
demonstrated the important function of this approach is slow and interrater reliability
orbitofrontal cortex in reward and eating- is a methodological concern, automatic ROI
related behaviors. Finally, Antonio Damasio’s methods are being developed for measuring the
(2003) “somatic marker” theory suggests that frontal lobes in their entirety and for selective
the orbitofrontal cortex is involved with the in- regional analyses.
terpretation of autonomic information in deci- Other MRI-based techniques have facilitated
sion making. study of brain–behavior relationships related
6 O V E R V I E W O F T H E F R O N TA L LO B E S

to the frontal lobes, including voxel-based- Increasingly, MRI is being explored as a way
morphometry (VBM) and deformation–tensor to supplement, or even replace, SPECT and
morphometry (DTM). With these techniques, PET techniques for measuring brain metabo-
the brains from two groups can be compared lism. Perfusion MRI (Callen, Black, Caldwell,
with regards to overall patterns of atrophy. & Grady, 2004) offers better resolution and is
Often a disease cohort is compared to age- less invasive than either SPECT or PET, but sys-
matched controls, and VBM and DTM also al- tematic comparisons between perfusion MRI,
low comparisons between an individual patient SPECT, and PET are still lacking. A newly
and a control group (Ashburner & Friston, funded National Institutes of Health (NIH) ini-
2001; Studholme et al., 2004). Or, a patient’s tiative on imaging in dementia will compare
results can be compared with use of images the relative value of perfusion MRI and PET,
obtained at different times. Unlike ROI ap- facilitating more scientific selection of imaging
proaches, VBM and DTM require no a priori techniques in the future.
hypotheses and allow comparisons of the fMRI is a new and powerful tool that has
whole brain (or specific frontal regions) be- dramatically changed research into the frontal
tween patient cohorts and controls. These tech- lobes by allowing noninvasive evaluation in
niques have proven particularly powerful for vivo. Relying upon changes in the MRI signal
delineating the most vulnerable brain regions that occur when the brain undergoes metabolic
in different conditions that cause dementia. activity (the BOLD signal), fMRI allows study
Structural MRI still holds great promise for of brain activity associated with specific cogni-
facilitating a better understanding of the fron- tive tasks (Frackowiak, 2000–2001). Frontal
tal lobes. VBM and ROI approaches are still brain regions that are active during working
relatively new, and studies combining these memory, self-reflection, word generation, tem-
techniques with newer cognitive approaches poral sequencing, set shifting, and many other
should offer many new insights into structural cognitive paradigms are being evaluated by
and functional relationships related to the fron- psychologists, psychiatrists, and neurologists
tal lobes. Movement from 0.5 to 1.5 T (tesla) with this technique (Baron-Cohen, 2004). An-
magnets has improved resolution of frontal re- other exciting development with fMRI has
gions and has facilitated better separation of been the mapping of networks activated with
gray matter from white matter. Furthermore, cognitive tasks or during rest (Greicius,
more powerful magnets (3, 4, and 7 T magnets) Krasnow, Reiss, & Menon, 2003). This eluci-
will offer even greater advantages for structural dates an understanding of what brain systems
resolution of the frontal lobes in the coming de- work together during specific activities. No
cade. technique has ever generated quite so much
Functional methods using radionuclides new data regarding the functional organization
such as single-photon emission computed to- of the frontal lobes, and it will be many years
mography (SPECT) and positron emission to- before this data can be fully understood.
mography (PET) have contributed to a better Magnetoencephalography, transcranial mag-
understanding of the frontal lobes. SPECT and netic stimulation, and nuclear magnetic reso-
PET have helped to show the frontal compo- nance spectroscopy represent other imaging
nent of a wide variety of disease states, includ- approaches that have been applied to the study
ing depression (Mayberg, 2002), obsessive– of frontal lobe function in healthy or disease
compulsive disorder (Saxena et al., 2004), states. Whatever the technique, it is clear that
schizophrenia (Hill et al., 2004), attention defi- neuroimaging will continue to influence of our
cit disorder (Schweitzer et al., 2003), Alzhei- understanding of the frontal lobes.
mer’s disease (Craig et al., 1996), and
frontotemporal dementia (Miller et al., 1991).
Similarly, frontal contributions to working NEUROANATOMICAL/FUNCTIONAL ORGANIZATION
memory, generation, executive function, apa-
thy, and disinhibition continue to be explored The frontal lobes are no longer considered a
with these functional techniques. Both SPECT single functional entity. Rather, there are a vari-
and PET still have great potential for imaging ety of ways to anatomically subdivide this
the brain receptor systems described in Chap- brain region, all based upon distinctive con-
ters 12–17, this volume. structs. Most researchers accept that the fron-
 Introduction 7

tal lobes have three major divisions: motor, mation, temporal sequencing, insight, interper-
premotor, and prefrontal regions. Motor and sonal perspective taking (theory of mind), and
premotor areas are considered distinctive func- social and real-world executive performance.
tional units, whereas prefrontal cortex is more Distinctive tasks that capture these different as-
complex, requiring further subdivision. One pects of executive control are in development.
system to subdivide the frontal cortex relies on Similarly, the anatomical components of these
the distinctive functions of different prefrontal tasks are under investigation. This topic is ex-
regions. Another approach considers regional plored by Kramer and Quitania in Chapter 18,
connections to and from specific subcortical re- this volume. Left versus right frontal lobe func-
gions. Additionally, the left and right frontal tions are now under careful scrutiny. Linguistic
lobes are increasingly differentiated: The left functions of Broca’s area in prefrontal cortex
frontal lobes are more specialized for language- has been understood for nearly 150 years, but
related functions, and the right frontal region is only recently have investigators begun to for-
dominant in social cognition and emotion. An- mally address the preeminence of the right
alyzing regional histology represents another prefrontal cortex for social and emotional
way to subdivide the frontal lobes. behavior. For example, in a recent imaging
A functional approach suggested by Stuss study of a large cohort of patients with demen-
and Benson (1986) divides prefrontal cortex tia, Rosen and colleagues (2004) found that re-
into orbital, dorsolateral, and cingulate re- petitive compulsive behaviors were strongly as-
gions. Increasingly, these gross divisions are be- sociated with right supplementary motor area
ing further parcellated into smaller functional atrophy, disinhibition with atrophy in the right
units. Baddeley (2003) and others have shown orbitofrontal cortex, and apathy with atrophy
a dorsal prefrontal (Brodmann’s area [BA] 46) in the right cingulate cortex. Right insular atro-
parietal system involved with working memory phy correlated with abnormalities in eating.
(left verbal working memory and right visual fMRI approaches to behavior suggest that self-
working memory). A more ventral frontal– reflection, reading the emotional expressions of
parietal system is involved with mirror move- others, and many other aspects of social cogni-
ments, (Rizzolatti, Fogassi, & Gallese, 2002), tion activate more right compared to left fron-
speech initiation (Dronkers, 1996), and affect tal regions. The specifics of behavioral special-
matching (Rosen et al., 2004). Orbitofrontal ization of right frontal cortex still remain
cortex has important medial–lateral and right– poorly understood, but the combination of
left divisions. Medial orbitofrontal cortex is fMRI and lesion studies should elucidate many
strongly connected with hypothalamic nuclei, of these details in the coming decades.
whereas lateral orbital cortex is more strongly Earlier, Yakovlev (1968), but more recently
connected with anterior temporal and insular Flaherty and Graybiel (1995), Tekin and
regions. In certain behavioral paradigms or- Cummings (2002), and others, have empha-
bitofrontal regions show antagonistic func- sized the intimate connections between sub-
tions. For example, the medial area activates cortical and frontal structures, and this connec-
when an individual is hungry, whereas the lat- tivity has helped to organize the frontal lobes
eral region activates when the same individual into distinctive units. The presence of these an-
is sated (Small, Zatorre, Dagher, Evans, & atomical circuits suggests one way to classify
Jones-Gotman, 2001). the organization of the frontal lobes. Tekin and
“Executive control,” a broad term used to Cummings suggest that there are five distinc-
describe the neuropsychological functions of tive frontal subcortical systems: (1) supplemen-
the frontal lobes, incorporates many distinctive tary motor area, (2) frontal eye fields, (3)
cognitive processes. Neuropsychologists are dorsolateral prefrontal, (4) orbitofrontal, and
now attempting to subdivide neuropsychologi- (5) anterior cingulate cortex. With each circuit,
cal functions into their anatomically driven specific neurochemical systems transmit their
subcomponents. Working memory is a core functional activity. Lesions in these different
constituent of executive function, and when frontal or subcortical circuits lead to distinctive
there are deficits in working memory, nearly all clinical syndromes. With supplementary motor
other tests of executive control are vulnerable. dysfunction, deficits in controlled movement
Other components of executive control include and repetitive motor behaviors emerge (Gorno-
generation, inhibition, set shifting, concept for- Tempini, Murray, Rankin, Weiner, & Miller,
8 O V E R V I E W O F T H E F R O N TA L LO B E S

2004); with eye movement injury, control of the right frontal area. These cells first appeared
gaze is diminished (Chou & Lisberger, 2004); in great apes but are only abundant in humans.
with dorsolateral dysfunction, there is loss of They first appeared in orangutans but are far
executive control and neuropsychological defi- more abundant in gorillas. Spindle cells show
cits in the area of working memory, and alter- still greater abundance in bonobo chimpanzees
nation and planning deficits emerge (Boone et and have 1,000-fold greater concentration in
al., 1999); orbitofrontal dysfunction causes humans than in chimps. Spindle cells are absent
social deficits, including disinhibition with in gibbons, New World monkeys, Old World
sparing of cognition (Damasio, 2003); and monkeys, and all other mammals studied
cingulate lesions lead to “amotivational” states (Allmann, Hakeem, & Watson, 2002; Nim-
(Tekin & Cummings, 2002). Psychiatric syn- chinsky et al., 1999). The role of these cells in
dromes are strongly linked to these frontal– social cognitive paradigms will be extensively
subcortical circuits, in particular, depression, studied in the coming decade.
mania, and obsessive–compulsive disorders.
The relationship of these psychiatric syn-
dromes to frontal lobe dysfunction is discussed NEUROLOGICAL DISORDERS
extensively in this book. Finally, movement dis- OF THE FRONTAL LOBES
orders are particularly prominent when the
basal ganglia component of frontal–subcortical One important approach to understanding
circuits is affected. frontal function is to examine neurological dis-
Mesulam (1998) considers anatomical con- orders that selectively attack the frontal re-
nectivity and histology in his approach to corti- gions. Neuroimaging has facilitated this ap-
cal organization of the frontal regions. His proach by allowing investigators to outline
system emphasizes limbic, paralimbic, and cor- brain areas affected by distinctive pathological
tical divisions. Cortical regions are divided into processes. Many neurological disorders involve
four subtypes—primary, unimodal, hetero- the frontal lobes either directly or through
modal, and supramodal cortex—based on the frontal–subcortical connections. Alzheimer’s
nature of these regions’ other cortical connec- disease (AD) is an example of a disease in
tions. With this system, the first-order regions which frontal cortex is not the primary site of
include primary motor (BA 4), sensory (BA 3), injury but is usually affected at some time in
visual (BA 17), auditory (BA 42), and gustatory the course of the illness (Johnson, Vogt, Kim,
cortex (BA 43). These regions are theoretically Cotman, & Head, 2004). With AD, the combi-
bound together by the fact that they are the nation of imaging, behavioral, and cognitive
first cortical regions that connect with sub- approaches has helped to clarify the role of the
cortical areas that translate information from cingulate cortex in a variety of psychological
or to the external milieu. Unimodal regions processes, including apathy and compulsions.
have efferent connections from the primary ar- There are also a few conditions in which fron-
eas and process only one type of sensory stim- tal cortex is the primary site of disease. Fronto-
uli (visual, auditory, or gustatory). Hetero- temporal lobar degeneration (FTLD) is one
modal regions are areas that connect with such example, and this disorder has become a
unimodal areas and are involved with multiple powerful model for the investigation of frontal
types of sensory processing. In the final, supra- function. Three subtypes of FTLD exist, all de-
modal division, many prefrontal regions are fined by distinctive clinical syndromes (Rosen
considered supramodal because they are re- et al., 2002). The core features of the major
mote from sensory processing, and involved subtype, frontotemporal dementia (FTD), in-
with higher order processing. clude loss of social and personal conduct, loss
Finally, in recent years, the role of a his- of insight, and emotional blunting. The most
tologically unique neuron, the spindle cell, is profound atrophy with FTD is in the anterior
being explored in relation to the distinctive cingulate, insular, and orbitofrontal cortex.
functions of the frontal lobes in humans. Ori- The right hemisphere is more severely affected
ginally described by von Economo, these large, than the left. In the second subtype, progressive
spindle-shaped cells found in layer 5b of the nonfluent aphasia, the atrophy involves these
ventral frontal anterior cingulate and anterior same frontal regions but is more severe on the
insular regions are more strongly localized to left than on the right side. With semantic de-
 Introduction 9

mentia, the third FTLD subtype, the insula and tom complex found in many patients with
orbitofrontal cortex, amygdala, and anterior schizophrenia is similar to the apathetic syn-
temporal lobes are bilaterally atrophic. These dromes caused by frontal injury (Boone, Miller,
distinctive anatomies facilitate exploration of Swartz, Lu, & Lee, 2003). Furthermore, pa-
the functions of the right versus left frontal cor- tients with schizophrenia who have the most
tex and different frontal regions. Each patient severe negative symptoms, such as apathy, tend
with FTLD shows slightly distinctive involve- to have the smallest frontal brain volumes, fur-
ment of dorsolateral, orbital, cingulate, or in- ther linking specific symptoms in schizophrenia
sular regions. This allows comparison of indi- to the frontal lobes (Roth, Flashman, Saykin,
viduals, or groups of patients, with unique McAllister, & Vidaver, 2004). Also, a wide-
anatomical patterns, with the goal of parceling variety of PET and fMRI studies show meta-
out the specific functions of these frontal re- bolic abnormalities at rest and during ac-
gions. tivation in prefrontal cortex (Davidson &
There are other neurological disease models Heinrichs, 2003). Finally, autopsies of many
for the evaluation of frontal lobe function. Be- patients with schizophrenia reveal neuropatho-
ginning with Harlow’s descriptions of Phineas logical abnormalities. Most of these changes
Gage, trauma has helped to delineate the func- are found in the hippocampus, but recent
tional anatomical divisions in the frontal lobes. work suggests that abnormalities in the frontal
Often, trauma selectively injures orbitofrontal regions (Webster, O’Grady, Kleinman, &
cortex while sparing dorsolateral regions (Al- Weickert, 2005).
exander & Stuss, 2000). In patients with these Schizophrenia represents just one of the
selective injuries, profound deficits in social many psychiatric illnesses in which behavioral
behavior and intelligence, with sparing of the disturbance is linked to the frontal lobes. Ma-
cognitive components of frontal lobe function, jor depression is associated with hypometabo-
led to the recognition that orbitofrontal and lism in the dorsal and orbitofrontal cortex
dorsolateral components of the frontal lobes (Mayberg, 2002). Metabolic changes have also
are distinctive. Similarly, from the clinical study been noted in the anterior cingulate and insular
of patients with selective injury to the cingulate regions. Similarly, disproportionate atrophy in
cortex associated with anterior cerebral artery the orbitofrontal cortex is seen in elderly pa-
stroke or psychosurgery (Brower & Price, 2001), tients with depression or bipolar disorder. Also,
researchers now suspect that this area is partic- injury to frontal cortex is often followed by de-
ularly important for initiation of behavior. pressive syndromes, and right orbitofrontal in-
jury can trigger secondary manic syndromes.
Frontal–subcortical circuits have also been
PSYCHIATRIC DISORDERS AND THE FRONTAL LOBE hypothesized to participate in obsessive–
compulsive disorder, and this hypothesis is sup-
An important paradigm shift in psychiatry has ported by both structural and functional imag-
been the recognition of dysfunction in the ing. Finally, attention deficit disorder is clearly
prefrontal cortex or within frontal–subcortical associated with dysfunction in the prefrontal
circuitry in many psychiatric disturbances. This cortical, attentional, and executive systems.
conceptual shift has been driven by converging
evidence generated through a wide variety of
approaches: cognitive, behavioral, neuroimag- SUMMARY
ing, and neuropathological. Schizophrenia rep-
resents one such disorder in which all of these The frontal lobes are a large brain region rep-
distinctive parameters suggest frontal dysfunc- resenting 30% of the cortical surface. The
tion. coming decade will see a more definitive explo-
Neuropsychological testing of many patients ration of the structural, functional, neuro-
with schizophrenia shows deficits in frontal/ex- chemical, and histological underpinnings of the
ecutive skills compared to controls (Kremen, frontal lobes. Understanding the frontal lobes
Seidman, Faraone, Toomey, & Tsuang, 2004). will lead to advances against a wide variety of
Similarly, the behavioral features of patients neurological and psychiatric conditions. These
with schizophrenia have many parallels to pa- new developments are outlined throughout this
tients with frontal injury. The negative symp- book.
10 O V E R V I E W O F T H E F R O N TA L LO B E S

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 CHAPTER 2
Conceptual and Clinical Aspects
of the Frontal Lobes

Jeffrey L. Cummings
Bruce L. Miller

The human frontal lobes mediate the behaviors FRONTAL LOBE FUNCTIONS
that most distinguish man from animals. Even
higher nonhuman primates lack the empathy, Several major categories of function are medi-
regret, sarcasm, social awareness, planning, and ated by the frontal lobes. Elemental neurologi-
judgment characteristic of human behavior. cal functions, speech and language abilities,
These frontally mediated behaviors define the volitional eye movements, motivational behav-
highest level of human culture and achievement. iors, social competency, and executive abilities
Frontal executive functions are also among the are mediated by discrete regions within the
most vulnerable of all human capabilities and frontal lobe.
are compromised by a variety of neurological
illnesses, including stroke, demyelinating disor-
Elemental Neurological Functions
ders, neurodegenerative diseases, traumatic
brain injury, and neoplasms. Developmental Basic neurological functions mediated by the
disorders frequently find their most severe ex- frontal lobes include pyramidal motor func-
pressions in frontal executive dysfunction. tions, control of continence, and olfaction.
Disorders of frontal lobe function and exec- Olfaction depends on the integrity of the olfac-
utive abilities are commonly encountered in tory bulb, olfactory nerve, and olfactory tract.
clinical circumstances. The assessment and in- The olfactory bulbs and nerves lie on the infe-
terpretation of frontal executive skills are com- rior surface of the orbitofrontal cortex, where
plex and require substantial clinical expertise. they are vulnerable to damage by orbitofrontal
Neuropsychological measures have evolved injury. Traumatic contusions and subfrontal
that capture aspects of frontal executive behav- neoplasms (e.g., meningiomas) are not infre-
ior, and advances are being made in developing quent causes of acquired olfactory dysfunction.
bedside tests that provide insight into frontal The medial olfactory track projects into the
executive abnormalities. In this brief chapter, septal region of the basal forebrain within the
an overview of frontal executive dysfunction is inferior medial frontal lobe.
provided, methods of assessment are described, The pyramidal motor tract begins in the mo-
and disorders commonly affecting these func- tor strip and projects through the internal cap-
tions are discussed. The anatomical underpin- sule and peduncle to the basis pontis and the
nings of distinct aspects of frontal executive medullary decussations before descending to
functions are correlated with clinical and func- the anterior horn cells. Pyramidal lesions cause
tional descriptions. a characteristic posture featuring extension of

12
 Conceptual and Clinical Aspects 13

the lower limb and flexion of the upper limb. The palmomental reflex can occur in normal
This posture is the typical hanging posture of individuals but may occur asymmetrically or be
the nonhuman primate and reflects the evolu- elicitable after multiple stimulations in individ-
tionary history of the nonpyramidal motor sys- uals with frontal dysfunction. It has been hy-
tem. There is concomitant spasticity of the in- pothesized that the palmomental reflex repre-
volved limbs, with a gradual crescendo of tone, sents a primitive growl response associated
culminating in sudden cessation of resistance as with upper limb simulation.
Golgi tendon organs release the spastic resis-
tance. The pyramidal motor system mediates
Sphincter Control
fine finger and lip movements, as well as upper
limb reach into the environment. This upper The urethral and anal sphincters are repre-
limb reach, and hand and lip dexterity allow sented anatomically in the medial inferior fron-
for fine motor control of writing and speech, tal cortex, inferior to the leg area of the medial
which contribute importantly to human enter- primary motor cortex. Involvement of this re-
prise and culture. gion through anterior cerebral artery stroke or
degeneration results in loss of sphincter control
and urinary or fecal incontinence.
Ocular Motor Functions
Volitional eye movements are mediated by the
Speech and Language Functions
frontal eye fields anterior to the motor strip.
Saccadic eye movements depend on the integ- Speech and language functions are mediated by
rity of this system. Supranuclear eye move- frontal lobe structures. A frontal dysarthria has
ment abnormalities reflecting an involvement been described with lesions anterior to the
of the frontal eye fields or disconnection of mouth area of the primary frontal cortex.
the fields from the ocular nuclei occur in Aphemia is a syndrome that begins with mu-
progressive supranuclear palsy, Huntington’s tism and evolves into a “foreign accent syn-
disease, and a variety of other neurological drome.” It is associated with small lesions con-
disorders. Seizures produce ocular deviation fined to Broca’s area of the left hemisphere.
away from the affected frontal eye field, and Larger Broca’s area lesions produce the syn-
ocular eye deviation toward the affected side drome of Broca’s aphasia, with nonfluent ver-
is characteristic of a postictal state or a focal bal output, largely intact comprehension, and
lesion. compromised repetition. Medial left frontal le-
sions produce a transcortical motor aphasia
characterized by nonfluent output, preserved
Frontal Release Signs
comprehension, and preserved repetition. An
Frontal release signs, more properly called executive aprosodia with impaired speech oc-
“primitive reflexes,” represent evolutionarily curs with lesions of the right hemisphere in the
derived motor programs that facilitate the exis- location equivalent to Broca’s area on the left.
tence of the infant but are normally lost as More anterior lesions of the right hemisphere
frontal cortex matures and frontal function contribute to a language output syndrome of
suppresses these more primitive motor pro- verbal dysdecorum, featuring lewd remarks,
grams. The suck reflex represents the innate sarcasm, or inappropriate humor (Alexander,
sucking response necessary for infant survival. Benson, & Stuss, 1989). Thus, frontal lobe le-
It reappears in advanced neurological disorders sions may produce a variety of speech and lan-
or diseases specifically affecting the frontal guage disorders. The syndromes tend to be spe-
lobes. Similarly, the grasp reflex enhances the cific for left or right hemisphere.
chance of survival in tree-dwelling primates,
whose survival from infancy depends on un-
Prefrontally Mediated Skills and Syndromes
learned reflexes to hang from parents or
branches. The grasp reflex reappears in pa- The prefrontal cortex is parcellated into orbito-
tients with diffuse neurological dysfunction or frontal, dorsolateral prefrontal, and medial
frontal lobe disorders. The extensor plantar frontal/anterior cingulate regions. Each of
represents a portion of the triple flexion with- these mediates a separate set of skills and
drawal reflex, a protective response to distal produces a distinct clinical syndrome when
limb stimulation. rendered dysfunctional (described below). Dis-
14 O V E R V I E W O F T H E F R O N TA L LO B E S

orders affecting the medial frontal cortex pro- interna before connecting to thalamic nuclei.
duce an apathetic amotivational syndrome; dis- The direct circuit projects from globus pallidus
orders of the orbitofrontal cortex produce interna to medial thalamic regions. The dy-
a disinhibited, impulse control disorder; and namic balance between direct and indirect cir-
lesions of the dorsolateral prefrontal cortex cuitry provides the basis for some types of
result in executive dysfunction (Cummings, motoric and behavioral disturbances eman-
1998; Sarazin et al., 1998). ating from disorders of one of the compo-
nent pathways (Litvan, Paulsen, Mega, &
Cummings, 1998).
FRONTAL–SUBCORTICAL CIRCUITS Each of the frontal–subcortical circuits is rel-
atively discrete, with communication between
Frontal–cortical regions are connected to a circuits occurring primarily at the level of the
complex circuitry of subcortical structures frontal cortex. This anatomical arrangement
(Figure 2.1). Frontal motor cortex and frontal emphasizes the unique function of the frontal
eye fields connect to subcortical motor and oc- cortex as an integrator across functional com-
ular control nuclei through descending path- plexes.
ways involving the basal ganglia and thalamus. The principal pathways outlined here share
The behaviorally relevant cortical regions of common transmitters, as well as an overall
medial frontal cortex, orbitofrontal cortex, and common anatomical structure (while remain-
dorsolateral prefrontal cortex each project to ing largely discrete within those structures).
distinct areas of the striatum. These striatal re- Glutamate is the principal cortical transmitter,
gions in turn project to subdivisions of the sub- both from cortex to striatum, and from
stantia nigra and globus pallidus. Nigral and thalamus to cortex. The main excitatory trans-
pallidal structures project to discrete nuclei of mitter within the circuits is also primarily glu-
the dorsomedial thalamic nuclei. The final limb tamate, whereas the common inhibitory trans-
of the circuit projects back to frontal cortex, as mitter is γ-aminobutyric acid (GABA). These
well as more widely to parietal and temporal pathways receive modulating input from sero-
regions (Cummings, 1998). Each frontal– tonergic and dopaminergic nuclei. In addition,
subcortical circuit has both a direct and an in- cholinergic interneurons comprise a population
direct pathway. The indirect pathway projects within the striatal structures. Differential
from globus pallidus externa to the sub- expression of receptor subtypes distinguishes
thalamic nucleus and back to globus pallidus among the frontal–subcortical circuits.

FIGURE 2.1. Principal anatomic structures of frontal–subcortical circuits.

 Conceptual and Clinical Aspects 15

MEDIAL FRONTAL CORTEX judgment, impulsive decision making, lack of

consideration for the impact of their behavior,
The medial frontal cortex comprises the sup- absence of an appreciation for the effect of
plementary motor area and the anterior their behavior or comments on others, and lack
cingulate cortex. The anterior cingulate is inti- of empathy for others. This orbitofrontal
mately involved in motivated behavior, and the syndrome has been labeled a “pseudopsycho-
principal behavioral product of anterior pathic” disorder, linking it to the sociopathic or
cingulate dysfunction is an amotivational apa- psychopathic behavior exhibited by individuals
thetic state. Apathy has several dimensions (Ta- with character disorders who manifest a disre-
ble 2.1). Motoric apathy is manifested by di- gard for accepted social conventions. Like indi-
minished motor activity, reduced gesturing, viduals with sociopathy, patients with orbito-
and diminished verbal output. Cognitive apa- frontal syndromes may commit minor crimes,
thy is manifested by decreased curiosity and al- such as shoplifting, and may come to clinical
tered interest in learning, deducing, and draw- attention through manifestations of criminal
ing logical conclusions. Affective apathy behavior (Miller, Darby, Benson, Cummings,
includes diminished vocal inflection and re- & Miller, 1997). Other behaviors that fre-
duced facial expression of internal emotional quently co-occur with the orbitofrontal disinhi-
states. Emotional apathy is evidenced by re- bition syndrome include apathy, restlessness,
duced social interest, diminished affection, and stereotypes, indifference, euphoria, disinterest-
compromised enthusiasm. Motivational apathy edness, cheerfulness, diminished attention, de-
includes reduced initiation and poor mainte- pendence or hyperdependence on stimuli in the
nance of implemented activities. The indepen- physical environment, planning disorders, and
dence and anatomical and neurobiological cor- impairment of emotional control (Sarazin et
relates of these different forms of apathy have al., 1998). When orbitofrontal injury is sus-
not been determined. tained in childhood, a similar behavioral com-
Apathy occurs with degenerative, ischemic, plex emerges but, in addition, the patients
neoplastic, and infectious conditions affecting exhibit defective social and moral reasoning
the anterior cingulate cortex, nucleus (Anderson, Bechara, Damasio, Tranel, &
accumbens, globus pallidus, thalamus, or con- Damasio, 1999). “Theory of mind” tests reveal
necting white matter tracts. Apathy is particu- that the ability to infer the mental state of oth-
larly striking in some patients with ers depends explicitly on right orbitofrontal
frontotemporal dementia, individuals with function (Stuss, Gallupp, & Alexander, 2001).
thalamic stroke, and persons with human Orbitofrontal dysfunction is frequently appar-
immunodeficiency virus (HIV) encephalopathy. ent in individuals exhibiting the environmental
dependence syndrome manifested by imitation
and utilization behavior (Lhermitte, 1986;
ORBITOFRONTAL CORTEX Lhermitte, Pillon, & Serdaru, 1986).

The orbitofrontal cortex, particularly the right-

hemispheric orbitofrontal regions, mediates the DORSOLATERAL PREFRONTAL CORTEX
rules of social convention. Patients with orbito- AND EXECUTIVE FUNCTION
frontal lesions are socially disabled, manifest-
ing interpersonal disinhibition, poor social The dorsolateral prefrontal cortex is responsi-
ble for organizing a volitional response to envi-
ronmental contingencies, recalling past events
and planning current actions in a temporally
TABLE 2.1. Components of the Apathetic Syndrome informed manner, programming motor acts to
follow volitional command, implementing pro-
Motoric grams to achieve the intended goal, monitoring
Cognitive the results of the action to determine the suc-
Affective cess of the intervention, and adjusting or stop-
Emotional ping the action depending on the outcome of
Motivational the assessment (Royall et al., 2002) (Figure
2.2). Each of these component processes is an
16 O V E R V I E W O F T H E F R O N TA L LO B E S

FIGURE 2.2. Components of frontal executive function abnormalities and relevant assessments.

executive process, and each may be impaired in the presence of a primary language deficit.
independently of the others. Thus, patients Likewise, the typical memory syndromes asso-
with executive dysfunction disorders may man- ciated with prefrontal dysfunction, such as a
ifest any of a diverse array of clinical phenom- retrieval deficit disorder, cannot be exhibited in
ena reflecting the complex organizational the presence of a frank amnesia associated with
framework mediating executive function. Not temporal lobe dysfunction. Strategies associ-
all patients with frontal lobe or frontal– ated with resolution of complex visuospatial
subcortical circuit disorders exhibit abnormali- challenges cannot be developed and applied in
ties in all executive function domains. the absence of elementary visual perceptual
Prefrontal functions are conceptualized as a and visuospatial functions. In the course of as-
nested series of hierarchical functions, with the sessment, relative functional capacity of instru-
first, lowest level involved in selecting motor mental functions must be ensured before con-
actions and motor programs, the second pro- clusions can be derived about the integrity of
viding contextual control and involved in se- executive functions.
lecting premotor representations contingent on Many executive function tasks assess multi-
external circumstances, and a third, episodic ple types of executive processes. For example,
control level placing the volitional act in a tem- the Wisconsin Card Sorting Test assesses both
porally relevant and situationally informed abstraction and preservation. The clock draw-
context (Koechlin, Ody, & Kouneiher, 2003). ing task tests both visual strategy and freedom
Executive function depends on the integrity from distraction. Failure of a specific execu-
of instrumental functions, such as language, tive function task rarely implicates a single,
memory, praxis, and visuospatial skills. One unique executive process. Rules that apply to
cannot abstract proverbs, a function that de- assessing frontal disorders are summarized in
pends on assigning two meanings to language, Table 2.2.
 Conceptual and Clinical Aspects 17

TABLE 2.2. Observations Guiding the Assessment of Frontal Lobe Functions

• Executive function has many dimensions, including choosing, planning, programming, implementing,
monitoring, and adjusting or ending a volitional act.
• Individual component processes of executive functions can be affected independently.
• Not all component processes are affected in patients with frontal lobe disorders simultaneously.
• Assessment of multiple component processes should be included in the evaluation of patients with a
suspected frontal lobe dysfunction.
• Executive function depends on intact instrumental functions such as language, memory, praxis,
perception, and visuospatial processing.
• Many tests of frontal lobe function simultaneously assess more than one component process.
• Executive function is synthetic, creative, and generative; the constrained and structured circumstances of
many testing situations minimize the effects of frontal dysfunction.
• Executive functions, motivation, and social behavior depend on frontal–subcortial circuitry in addition
to integrity of frontal cortex.
• “Frontal” disorders may occur with subcortical lesions (basal ganglia, thalamus) linked to frontal cortex
through fontal–subcortical circuits.
• Three relatively distinct frontal lobe syndromes are recognized: An amotivational syndrome reflects
dysfunction of the anterior cingulate and medial frontal cortex; disinhibition is associated with
disturbances of the inferior frontal cortex; and executive dysfunction is associated with dysfunction of
the dorsolateral prefrontal cortex.

Component Procedures of Executive Function tive function level include mental control tasks
and the ability to hold the task in mind, such as
Volition
reciting the months of the year in reverse order
There are few pure tests of volition. Assessment or spelling the word “world” backwards,
of this domain is best accomplished by investi- tower tests that require extensive planning,
gating the patient’s insight and determining his complex figure copy tasks that require a so-
or her understanding of the illness, disability, phisticated strategy to best accomplish the
and likelihood of regaining employment status. copy, maze tasks that require the patient to an-
Verbal fluency testing contains a generative in- ticipate and plan maze moves, and a clock-
tellectual component relevant to the assessment drawing task that requires the patient to ex-
of volition. Patients must volitionally search hibit spatial planning (Royall, Cordes, & Polk,
their lexicon to identify members of a specific 1998). Memory functions rendered abnormal
category, such as animals or words beginning by prefrontal cortex dysfunction include prob-
with the letter “a.” lems retrieving information from semantic
Volitional activity demands the ability to stores, impairments of temporal ordering, dec-
suppress habitual responses in favor of novel rements of source memory (where or when
activity, an ability tested by the Stroop Color– something was learned), increased susceptibil-
Word Test. This ability is critical to implement- ity to interference in the course of memory test-
ing programs in response to environmental ing, compromised strategies for encoding and
contingencies (Peterson et al., 1999). Volition retrieval, impaired metamemory or insight into
also requires abstraction of a pattern from the memory function, and increased rates of
background. Abstraction is assessed by the confabulatory and false memory responses
Wisconsin Card Sorting Test and tests of simi- (Wheeler, Stuss, & Tulving, 1995). Patients
larities, differences, and proverb interpretation have difficulty retrieving remote memories, just
(Goldstein, Obrzut, John, Ledakis, & Arm- as they do retrieving recent memories, and
strong, 2004; Rezai et al., 1993). there is less of a recent–remote dissociation in
frontally based retrieval deficit syndromes
compared to temporally based amnestic disor-
Planning and Recalling
ders (Mangels, Gershberg, Shimamura, &
This component of executive function medi- Knight, 1996). Procedural or motor learning is
ates development of a plan and puts it into a impaired in patients with prefrontal lesions
temporal context of previously accomplished (Gomez Beldarrain, Grafman, Pascual-Leone,
activities. Assessments relevant to this execu- & Garcia-Monco, 1999).
18 O V E R V I E W O F T H E F R O N TA L LO B E S

Motor Programs call search is assessed through tests of recent

and remote recall; strategy generation can be
Appropriate programming involves both se-
determined through complex figure copy
lecting and implementing a program and re-
tasks; mental control is assessed by asking the
sisting or inhibiting alternative responses.
patient to repeat the months of the year in re-
Commonly used motor program tests include
verse order, to spell the word “world” back-
alternating programs, reciprocal programs,
ward, or to execute serial subtractions. Ab-
and the go/no-go test.
straction is assessed through interpretation of
proverbs or derivation of the meaning of dif-
Implementation of Volitional Activity ferences or similarities. Motor tasks include
motor programming tasks such as go/no-go
The actual implementation phase of volitional tasks and serial hand sequences. Freedom
activity is mediated by frontal motor cortex or, from distraction can be assessed by asking
in the case of eye movements, by frontal eye the patient to draw the face of a clock and
fields. Relevant measures of motor activity in- set it for the time of 11:10. Vigilance and
clude the Trail Making A test, the grooved peg- concentration are examined with a continu-
board test, and the finger-tapping test. ous performance test, and the ability to shift
sets can be determined by asking the patient
Monitoring the Effects of Volitional Activity to perform oral trails (alternating between
counting and reciting the alphabet).
A variety of vigilance and abstraction tasks are In addition to these individual components
required to monitor the impact of a volitional of a bedside assessment of frontal lobe func-
effect. Cancellation tasks assess vigilance, as do tions, several relevant rating scales and ques-
digit span and continuous performance tasks. tionnaires have been developed and may as-
sist in identifying and characterizing frontal
Adjusting and Stopping Volitional Activity lobe disorder. The EXIT-25, which provides a
brief assessment of several component frontal
Adjusting and stopping volitional activity is as executive functions, may be used in conjunc-
critical as implementing it. Perseveration is a tion with the CLOX, a method of scor-
commonly observed clinical phenomenon that ing clock drawing that emphasizes executive
represents an inability to stop an action appro- function (Royall et al., 1998). The Frontal
priately. This is tested clinically with multiple Assessment Battery (FAB; Dubois, Slachevsky,
loops or motor programming tasks, such as Litvan, & Pillon, 2000) also assesses several
alternating programs. The Wisconsin Card processes relevant to frontal lobe function
Sorting Test and the Trail Making B Test also and has been shown to identify patients with
elicit perseverative behavior. frontal lobe syndromes. The Montreal Cogni-
tive Assessment (MoCA; Nasreddine et al.,
2005) is a 30-item cognitive assessment with
BEDSIDE ASSESSMENT an emphasis on evaluation of executive func-
OF FRONTAL LOBE FUNCTION tion.
Assessment of neuropsychiatric symptoms
Orbitofrontal, medial frontal, and some as- may assist in identifying patients with frontal
pects of dorsolateral prefrontal dysfunction are lobe dysfunction. The Neuropsychiatric Inven-
best assessed by careful observation during the tory (NPI; Cummings et al., 1994) had been
course of an interview. Is the patient disinhibit- used to assess patients with frontotemporal de-
ed, impulsive, and tactless? Is the patient apa- generation, where it reveals a characteristic
thetic, agestural, and without motivation? profile of disinhibition and euphoria (Levy,
Does the patient have poor judgment, failing to Miller, Cummings, Fairbanks, & Craig, 1996).
grasp the implications of his or her illness or The Frontal Systems Behavior Scale (Stout,
disability? Ready, Grace, Malloy, & Paulsen, 2003) in-
Bedsides mental status testing can assess a cludes ratings of apathy and disinhibition and
substantial number of component executive measures of executive dysfunction, and is use-
processes. Lexical search strategies are as- ful in assessment of patients with frontal lobe
sessed by verbal fluency; information and re- disorders.
 Conceptual and Clinical Aspects 19

FUNCTIONAL IMAGING AND THE EXPLORATION TABLE 2.3. Conditions Producing a Disproportionate
OF FRONTALLY MEDIATED ABILITIES Impact on Frontal and Frontal–Subcortical Function
Vascular disorders
Functional magnetic resonance imaging Anterior cerebral artery occlusion
(fMRI) has emerged as a tool uniquely suited Middle cerebral artery occlusion
to explore aspects of frontal lobe function. In Anterior communicating artery aneurysm rupture
these assessments, an individual is challenged Cerebrovascular disease affecting small vessels
with a unique situation or test. Activation of Degenerative disorders
a specific region of the frontal lobes in re- Frontotemporal dementia
Primary progressive aphasia
sponse to the challenge implies participation Frontal variant of Alzheimer’s disease
of that region in generating the response. Progressive supranuclear palsy
This methodology has been successfully ap- Corticobasal degeneration
plied to the exploration of higher-order hu- Parkinson’s disease
man cognitive functions. For example, regret Multiple sclerosis
has been shown to depend on the integrity of Infections
Syphilis
orbitofrontal cortex (Camille et al., 2004). HIV infection
Conflict monitoring has been ascribed by Traumatic brain injury
fMRI to the anterior cingulate, a concept Brain neoplasms
consistent with the idea that absence of con- Butterfly gliomas
flict monitoring would result in an apathetic Subfrontal meningiomas
syndrome (Kerns et al., 2004). Activation of Hydrocephalus
the presupplementary motor area, as well as
right dorsolateral prefrontal region was ob-
served when patients paid attention to their
volitional activity (Lau, Rogers, Haggard, & Frontotemporal dementia affecting primarily
Passingham, 2004). Participation of the ante- right anterior temporal or frontal structures
rior cingulate cortex has been demonstrated produces a disinhibition syndrome, whereas
in monitoring situations in which errors are asymmetric involvement of the left frontal
likely to occur (Carter et al., 1998), and the cortex produces primary progressive aphasia.
orbitofrontal cortex was found to participate A frontal variant of Alzheimer’s disease has
in reward-dependent activity in nonhuman been recognized, in which prominent frontal
primates (Roesch & Olson, 2004). This ap- features co-occur with a typical amnestic
proach has been unusually valuable in link- type of memory disorder (Johnson, Head,
ing regions of frontal cortex to specific be- Kim, Starr, & Cotman, 1999). Disorders of
haviors. frontal–subcortical circuits, such as progres-
sive supranuclear palsy and corticobasal de-
generation, also produce a frontal-type syn-
DIFFERENTIAL DIAGNOSIS OF CONDITIONS drome. Demyelinating disorders, particularly
PREDOMINANTLY AFFECTING multiple sclerosis, affecting frontal lobe white
FRONTAL CORTICAL FUNCTION matter tracks can produce a prominent
frontal-type syndrome. Traumatic brain injury
A variety of neurological disorders can have not infrequently has disproportionate effects
disproportionate impact on frontal function on the orbitofrontal cortex, resulting in an
(Table 2.3). Among vascular disorders, occlu- orbitofrontal disinhibition syndrome in the
sion of the anterior cerebral artery produces posttraumatic state. Syphilis and HIV are two
an anterior cingulate syndrome, whereas oc- examples of infectious disorders that can
clusion of the superior branch of the middle have disproportionate effects on frontal func-
cerebral artery affects dorsolateral prefrontal tion. Patients with brain tumors, particularly
cortex. Rupture of anterior communicating butterfly gliomas involving the frontal lobes
artery aneurysms may produce orbitofrontal bilaterally, or subfrontal meningiomas that
injury and a disinhibition syndrome. Frontal compress the orbitofrontal cortex from be-
cortical degenerations likewise produce a low, may present with prominent frontal lobe
prominent frontal disorder (Miller, Boone, dysfunction. Obstructive hydrocephalus may
Cummings, Read, & Mishkin, 2000). produce a frontal-type syndrome.
20 O V E R V I E W O F T H E F R O N TA L LO B E S

TREATMENT & Garcia-Monco, J. C. (1999). Procedural learning

is impaired in patients with prefrontal lesions. Neu-
Most disorders of the frontal lobe await dis- rology, 52, 1853–1860.
Johnson, J. K., Head, E., Kim, R., Starr, A., & Cotman,
covery of disease-modifying treatments to
C. W. (1999). Clinical and pathological evidence for
ameliorate their impact on frontal function.
a frontal variant of Alzheimer’s disease. Archives of
Disease-specific therapies may be useful in Neurology, 56, 1233–1239.
ameliorating progression of stroke or multiple Kerns, J. G., Cohen, J. D., MacDonald, A. W., III, Cho,
sclerosis affecting frontal lobe functions. Symp- R. Y., Stenger, V. A., & Carter, C. S. (2004). Anterior
tomatic treatments may sometimes provide cingulate conflict monitoring and adjustments in
useful relief of symptoms. Cholinesterase in- control. Science, 303, 1023–1026.
hibitors have modest effects on executive dys- Koechlin, E., Ody, C., & Kouneiher, F. (2003). The ar-
function in Parkinson’s disease dementia (Emre chitecture of cognitive control in the human pre-
et al., 2004), and selective serotonin reuptake frontal cortex. Science, 302, 1181–1185.
Lau, H. C., Rogers, R. D., Haggard, P., & Passingham,
inhibitors may improve behavior in frontal de-
R. E. (2004). Attention to intention. Science, 303,
generations (Swartz, Miller, Lesser, & Darby,
1208–1210.
1997). Levy, M. L., Miller, B. L., Cummings, J. L., Fairbanks,
L. A., & Craig, A. (1996). Alzheimer disease and
frontotemporal dementias: Behavioral distinctions.
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PART II
ANATOMY
 CHAPTER 3
Frontal–Subcortical Circuits

Tiffany W. Chow
Jeffrey L. Cummings

Frontal–subcortical circuits (FSCs) incorporate or more FSCs. After introducing the generic
complex input from the central nervous system neuroanatomy and connectivity of the circuits,
to modulate the expression of cognition and this chapter presents cognitive and behavioral
emotion through behavior and movement. Al- functions of the FSCs. The following section
exander, DeLong, and Strick (1986) used the describes the impact of clinical neuropsychiat-
concept of the motor thalamocortical circuit as ric syndromes on the cognitive, behavioral, and
an architectural template to build the concept motor FSCs. Subsequent chapters of this book
of other FSCs. Their description of five corti- detail further the assessment of FSC function.
cally anchored circuits provided a basis for
subsequent elucidation of how those circuits
influence behavior and movement. This chap- THE FSC PROTOTYPE
ter presents the clinical neuropsychiatric syn-
Shared Anatomy and Neurochemistry of the FSCs
dromes associated with disturbances of these
circuits. These FSCs include those behaviorally As illustrated in Figure 3.1, FSCs share a com-
relevant circuits originating in dorsolateral pre- mon template of topography and physiology.
frontal, superior medial frontal, and orbito- Each circuit enjoins the same member struc-
frontal cortices. In addition, there are impor- tures, but the circuits are arranged in parallel,
tant roles for inferotemporal and posterior largely segregated from each other. The relative
parietal cortical regions via open connections
to these circuits.
This chapter begins with an orientation to
features shared by all FSCs. We describe the
balanced inhibitory and excitatory influences
that modulate cortical activation within each
circuit. Each circuit has a direct pathway that
generally enhances cortical activity; there is
also a mechanism for inhibition within each
circuit via an indirect pathway. The manifesta-
tions of direct or indirect pathway dominance
allow a wide repertoire of adaptive responses
to shifting internal priorities or external envi-
ronmental stimuli. The manifestation of a par-
ticular neuropsychiatric symptom can reflect a
loss of the balancing mechanism within one FIGURE 3.1. Basic structural template for the FSCs.

25
26 A N ATO M Y

TABLE 3.1. Neurotransmitters and Neuropeptides

of the FSCs
Glutamate Enkephalin
GABA Neurotensin
Dopamine Substance P
Acetylcholine Dynorphin
Serotonin Adenosine
Norepinephrine Neuropeptide Y

anatomical positions of the circuits are pre-

served as they pass through striatum (caudate
and putamen), globus pallidus, substantia
nigra, and thalamus (Mega & Cummings,
1994). In addition to sharing anatomical com-
ponents, each circuit makes use of the same
neurotransmitters and neuropeptides, although
the distribution of neuroreceptor subtypes
might mediate different activations for each FIGURE 3.3. The superior medial FSC. Input travels
circuit (see Table 3.1). Figures 3.2 to 3.5 show from neurons of the anterior cingulate and other
the cortical areas involved in FSCs; although superior medial frontal (SMF) regions to the ven-
these figures illustrate one cerebral hemisphere, tral striatum, which includes the ventromedial
the FSCs are present bilaterally. caudate, ventral putamen, nucleus accumbens,
and the olfactory tubercle (Middleton & Strick,
2000; Selemon & Goldman-Rakic, 1985). Projec-
tions then innervate areas of the globus pallidus
and substantia nigra (not shown). This FSC con-
tinues to the ventroanterior and dorsomedial nu-
clei of the thalamus and closes with projections
back to cortex (Middleton & Strick, 2000).

Each FSC has a direct pathway that results in

sustained activation of the cortical component.
Cortical projections release glutamate (GLU)
to the corresponding regions of the striatum,
which usually includes the caudate nucleus;
some FSCs involve the putamen or ventral
striatum, which consists mainly of the nucleus
accumbens. Binding of GLU at N-methyl-D-
aspartate receptors in the striatum triggers re-
lease of γ-aminobutyric acid (GABA) at the in-
FIGURE 3.2. Dorsolateral prefrontal–subcortical cir- ternal segment of the globus pallidus interna
cuit. Brodmann’s areas 9 and 46 from DLPFC (GPi) and substantia nigra. This diminishes
serve as the origins. Each of these BAs has a dor- GABA release from the GPi to the thalamic
sal and ventral stream by which it relays to the component of the circuit. The disinhibited
dorsal aspect of the head of the caudate. These thalamus then enhances glutamatergic excita-
four subcircuits continue to specific regions with- tion of cortical regions.
in GPi and/or the substantia nigra (not shown). There is also an indirect pathway for each
From those destinations, the circuit proceeds to circuit to balance the direct pathway. The indi-
ventroanterior, ventrolateral, or dorsomedial rect pathway diverges from the direct pathway
thalamic nuclei before returning to the cortical or- when striatal efferents project to the globus
igins (Middleton & Strick, 2000). pallidus externa (GPe). GABA-ergic pallidal fi-
 Frontal–Subcortical Circuits 27

to the direct or the indirect pathway, respec-

tively.
The direct and indirect pathways diverge in
neuroanatomical connectivity at the cytoarchi-
tectural level. The division of striatal neurons
into striosomes and matrix allows for the bifur-
cation of circuits to direct and indirect path-
ways. Both striosomes and matrix produce
GABA, but striosomes project onward to GPi
(the direct pathway), and the matrix efferents
take the other route (indirect pathway), pro-
jecting to GPe. The pathways also differ in
neuroreceptors expressed: The striosomal di-
rect pathway features dopamine type 1 recep-
tors, whereas the matrix indirect pathway has
dopamine type 2 receptors.
Several neurotransmitters and neuropeptides
have impacts on the cortex, striatum, and glo-
bus pallidus within the FSCs. Neurotransmit-
FIGURE 3.4. Lateral and medial orbitofrontal–sub-
ters and neuropeptides with effects on the FSCs
cortical circuits. The lateral OFC (lateral and or-
are listed in Table 3.1. Neurotransmitter influ-
bital aspects of Brodmann’s area 12) connects as
ences on the circuits are complex. No single
two subcircuits with ventromedial caudate, then
neurotransmitter has one simple role in activat-
medial GPi and substantia nigra (not shown),
ing or inhibiting a given circuit. The heteroge-
then dorsomedial and ventroanterior thalamic
neity of receptors for each neurotransmitter
nuclei, before returning to lateral OFC. The
(e.g., at least five dopamine receptor families
medial OFC begins from Brodmann’s area 13 and
have been described) and different localization
insular transitional cortex, projecting to the ven-
of these receptors on components of the circuit
tromedial caudate, similar to the lateral orbito-
frontal circuit, but also with projections to the
ventral striatum similar to the superior medial
FSC. The next destination of the medial OFC
subcircuits is ventral pallidum and substantia
nigra (not shown). Thalamic nuclei for this circuit
include ventroanterior, dorsomedial, and ventro-
lateral.

bers extend to the subthalamic nucleus, which

then stimulates the GPi of the direct pathway
with GLU. This glutamatergic influence on the
GPi counterbalances the direct pathway’s
GABA-ergic input at the GPi, which would
otherwise lead to inhibition of cortical activa-
tion via the thalamus.
The direct pathway of the circuit disinhibits
the thalamus, whereas the indirect pathway in-
hibits it. The relative influences of the direct
and indirect pathways determine the control of
the thalamocortical connections and the motor, FIGURE 3.5. Lateral view of cortical contributions
cognitive, or behavioral output of the circuit. to DLPFC and inferotemporal subcortical circuit.
Both pathways begin with excitatory, gluta- The inferotemporal circuit echoes the FSC’s corti-
matergic projections from the frontal cortex to cal connectivity to basal ganglia with reflection
specific areas within the striatum. Striatal out- back to via thalamus for modulation of cortical
put neurons then project to either GPi or Gpe visuomotor processing (see Table 3.2).
28 A N ATO M Y

make it difficult to predict the outcome of acti- 3.6). Open elements of the circuits relate
vating a single neurotransmitter receptor. Cir- systematically to brain regions that mediate re-
cuit physiology also enjoys a reputation for lated functions and have similar phylogenetic
plasticity that reflects shifts in pre- and post- origins to the FSC. Neuroanatomical structures
synaptic neuroreceptor activation. Neurotrans- with which the circuits share open connections
mitters also affect one another; for example, are more easily understood in the context of
cholinergic agonism can enhance dopamine re- the clinical syndromes specific to each circuit
lease in the striatum. Pharmacological manipu- and are discussed below.
lations of the FSCs are therefore challenging,
because benefits in one axis of behavior, cogni-
tion, or motor function may bear undesirable BEHAVIORALLY RELEVANT FSCS
effects in another. A classic example is the pro-
duction of extrapyramidal rigidity when dopa- Lesion studies and functional neuroimaging re-
mine receptor blockade is used to treat psycho- veal the roles of the FSCs in cognition, motiva-
sis. tion, affect, and motor control. Classically,
three FSCs were linked to executive dysfunc-
tion, akinetic mutism, and disinhibition; more
FSC Connections
recent neuropsychological and neuroimaging
Each FSC has three orders of connectivity: (1) studies have confirmed major roles for the
connections within each circuit’s direct and in- dorsolateral prefrontal (DLPFC), superior
direct pathways, (2) corticocortical connec- medial frontal (formerly known as ante-
tions with the other circuits, and (3) open con- rior cingulate), and medial orbitofrontal–sub-
nections to areas outside the FSCs (see Figure cortical (OFC) circuits, as well as a contribut-

FIGURE 3.6. Connectivity of the FSCs, using symbols derived from Figure 3.1. Figure courtesy of Sajung
Yun.
 Frontal–Subcortical Circuits 29

ing role for the lateral OFC. We present the the examiner shifts the rules for matching the
associations among these four neurobehavioral cards (e.g., matching by color instead of
FSCs to cognition, motivation, affect, and so- shape). A third individual who has suffered a
cial behavior. hemorrhagic infarct in the left head of the
caudate nucleus, disrupting both the superior
medial frontal and DLPFC FSCs, would show
Executive Functions
marked impairment on the WCST in slow pro-
Examples of executive activities include the cessing time and perseverative errors.
ability to organize a behavioral response to Four of the FSCs and their open connections
solve a complex problem (e.g., learning new in- therefore contribute to executive function.
formation, copying complicated figures), sys- Brain lesions outside of the FSC proper may
tematically searching memory, activation of re- cause FSC dysfunction if they affect open con-
mote memories, appropriate prioritization of nections. Posterior parietal Brodmann’s area
external stimuli, attention, generation of motor (BA) 7a is richly interconnected to prefrontal
programs, and use of verbal skills to guide BA 46 of the DLPFC (Yeterian & Pandya,
behavior. As described in more detail by Stuss 1993). BA 7a participates in visual processing,
(Chapter 19, this volume), basic working attending to significant visual stimuli, visually
processes for these activities include (1) task guided reaching, and planning visuospatial
setting, (2) initiation of the task, (3) detecting strategies. This is distinct from the infero-
error, and (4) behavioral self-regulating func- temporal subcortical circuit, which contributes
tions. input to the motor FSC (see Table 3.2).
These processes are modulated by more than The number of FSCs disrupted will change
one FSC. Superior medial cortex includes the behavior. The exact location of a lesion along
anterior cingulate gyri. Task setting correlates the FSC may also determine the type of cogni-
with activity in the left DLPFC, whereas error tive impairment that results. Lesions of the
detection correlates with right DLPFC acti- dorsolateral cortex and caudate nucleus result
vation (Stuss, Binns, Murphy, & Alexander, in poor recall, with relative preservation of rec-
2002). The laterality of DLPFC FSC contribu- ognition abilities (Butters, Wolfe, Granholm, &
tions to cognition highlights the presence of Martone, 1986), whereas further along the cir-
FSC connectivity in both hemispheres, with the cuit, thalamic lesions produce impairment of
potential for differentiation between hemi- both recall and recognition (Stuss, Guberman,
spheres. Initiation of a new task involves both Nelson, & Larochelle, 1988). Lesions in the
left and right superior medial frontal FSCs thalamus usually combine the amnesia of me-
(Stuss, Floden, Alexander, Levine, & Katz, dial limbic dysfunction and executive im-
2001). Behavioral self-regulation can be defec- pairment (Deymeer, Smith, DeGirolami, &
tive after disruption of the medial OFC circuit. Drachman, 1989; Eslinger, Warner, Grattan, &
Impulsivity can cause difficulty with executive Easton, 1991; Stuss et al., 1988), because the
function by enhancing distractibility and im- thalamus is poised at the intersection of the
pairing prioritization of external stimuli. FSCs, with the limbic circuit comprised of the
The separation of executive function into ba- hippocampus, fornix, and hypothalamus.
sic processes helps to explain how lesions in We present the functional neuroimaging
different frontal areas can cause a patient to do findings that support these linkages in the con-
poorly on tests of executive function, such as text of circuit-related neuropsychiatric syn-
the Wisconsin Card Sorting Test (WCST), dromes later in this chapter.
while performing adequately on other tests. Er-
rors may be made to different degrees and for
Motivational Function
different reasons, based on the type and num-
ber of FSCs disrupted. For example, an individ- Akinetic mutism occurs with bilateral lesions
ual may show impairment on the WCST be- of the anterior cingulate cortex (Barris &
cause of slowed response time after resection of Schuman, 1953; Fesenmeier, Kuzniecky, &
a butterfly glioma that intruded upon superior Garcia, 1990; Nielsen & Jacobs, 1951). With
medial frontal cortex. Another individual with bilateral lesions, patients are profoundly apa-
a lesion to the left DLPFC may have no diffi- thetic or abulic; rarely moving, they are incon-
culty initiating a response but will make multi- tinent, eat and drink only when fed, and may
ple errors due to faulty task setting whenever have speech limited to monosyllabic responses
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 CHAPTER VI
VARIOUS INCIDENTS IN MURRAY ISLAND

I have previously mentioned that I had engaged two Murray

Island natives, Debe Wali and Jimmy Rice, to assist Ontong, our
Javanese cook. At first I offered them a shilling a day as wages. This
they refused after much consideration, but agreed that they would
take a pound a month. Later on, when they had practical experience
that one pound sterling a month was not so advantageous to them
as six shillings a week, they repented of their bargain, but as it was
not to our interest to be hard on them, we reverted to my original
offer. Our supply of silver was running short, so after a time we had
to pay in half-sovereigns; at first there was some difficulty in making
them understand the equity of their having to return four shillings in
silver in exchange for the gold coin.
One morning during my temporary absence from the island,
Jimmy Rice came up on the verandah, followed by an islander
named Gi, and said, “This man want to speak along you, fellow.” Gi
said, “Me want sell porslin along you.” My colleagues, not having at
that time an instinctive knowledge of pidjin English, and forgetting
that f and sh are often transmuted into p and s, awaited with some
interest Gi’s disclosure of the porcelain. Gi produced four shillings
(por s’lin’) and said, “Me want to buy ten s’lin’.” A light gradually
dawned on my colleagues as they recollected the Saturday night
transactions with Jimmy Rice and Debe Wali.
The more obvious part of this arrangement had evidently been
noised abroad, and Gi came prepared to test our readiness to give a
half-sovereign in exchange for four shillings.
After introducing Gi, Jimmy Rice retired below the verandah,
where he remained evidently appreciating the humour of the
situation. He said afterwards, “I laugh along myself inside. I laugh,
laugh, laugh. Gi he gammon.”
This was by no means the only occasion on which we were
humbugged, but we did not mind, for were we not studying the
psychology of the natives amongst other subjects, and it was most
interesting to watch the various idiosyncrasies of our friends and
acquaintances.
For example the grey-bearded Ari was somewhat slow and
perhaps a little stupid, but he was thoroughly conscientious and
always tried to do the right thing. We were never quite sure, by the
way, whether the old boy’s name, which was pronounced Ari, was
really a native name or merely their version of “Harry.” Pasi was a
man of stronger character and more intelligent; he had an alert
manner and an abrupt method of speech. Debe Wali was a highly
strung, nervous, voluble person, and not averse to thrusting himself
forward; Jimmy Rice was much quieter and slower in his speech and
thoughts; he was certainly more reliable than Debe Wali, but he had
a strong instinct of acquisitiveness, scarcely a day passed without his
asking for something. Myers tells me that once within twenty-four
hours he asked for a pair of boots, a belt, two empty rice bags, a
Jew’s harp, a hat, and of course some tobacco. Jimmy Dei was a
thorough gentleman, Gadodo a man of action, Alo a great, good-
natured fellow who kept and carefully tended a wheezy old sick
man. So I might go on, matching white men known to me with our
Papuan friends; few were really disagreeable, but I call to mind one
sleek, hypocritical man named Papi, who was always trying to get
the better of everyone else, and in this he generally succeeded.
Old Ulai was perhaps the greatest character of the lot, a regular
old heathen, who exhibited but scanty signs of grace. He gloated
over the past, especially the shady parts of it, and it was this lack of
reverence that made him so valuable to us. As he had but little of
that reticence that is so characteristic of the Melanesian, we were
able to get hints from him that we followed up with our other friends
to our great advantage. For, alas! I do not think our friend was very
truthful, nor did he know all about everything, and occasionally he
was inclined to gammon us even in serious matters; but that did not
matter, as we never trusted his word alone. Indeed, the cunning old
man was a great humbug, and he seemed to quite enjoy being
found out, and never resented the imputation of “gammoning.” He
had a craving for beer and grog, and often and often he would sidle
up and whisper, “You give me a little grog.” A demand, needless to
add, that was never satisfied.
 PLATE IX.

DEBE WALI AND HIS WIFE

JIMMY RICE AND HIS WIFE

 When I went to New Guinea I took Ontong, our Malay cook, with
me, and left Rivers, Myers, and McDougall with the two native
“boys.” My colleagues have described to me how amused they were
in watching the subsequent developments. Rivers did not consider it
expedient to definitely appoint one as cook and the other as helper,
knowing matters would right themselves.
Naturally, Debe Wali at once took the more important post, and to
Jimmy Rice fell the job of carrying water twice daily and getting
firewood. Debe’s active mind soon discovered that if he was doing
cook’s work he should have cook’s pay, so he wanted a rise in
wages. Then it dawned upon Jimmy Rice that he should not be left
out in the cold; he argued, “Debe, he now got one job—he cook; me
got two job—me cut ’im wood, me fetch ’im water. You give me
more wages.”
It did not take Debe Wali long to discover that Jimmy Rice had
practically the whole day to himself, while he, as cook, was more
occupied, though, to tell the truth, the cooking was of the most
rudimentary kind possible.
Eventually an arrangement was made between Debe and Jimmy
among themselves, by which they spent alternate weeks at cooking
and hewing wood and drawing water. There was always considerable
jealousy as to who was the better cook; once, when it was Jimmy’s
week to cook, and he had brought up some bread of his own
making, Debe came in, looked at it, and sticking his thumb well in,
blandly remarked, “I call that damper.”
On another occasion, when the mind of the entire island was
absorbed in the preparation of a big kaikai (feast), Jimmy Rice went
off into the bush to bring back his contribution of yams, bananas,
and coconuts, and there became so absorbed in his work that he did
not return until after my colleagues had cooked their own dinner.
Debe Wali was furious when he heard of his comrade’s
unpunctuality. “When I cook, by jingo, I give you proper kaikai
(food); breakfast, sun there; dinner, sun up here; supper, sun over
there.” That same evening and the following morning Debe forgot to
fill the jugs with water.
One nice thing about our helpers was that they never considered
themselves as servants. They treated us as equals, much to the
amusement and disgust of Ontong. They would come up from the
kitchen, loll on our deck chairs, and chatter away always in the most
amusing fashion.
Myers also told me the following:—“Debe astonished us one
evening by the calm announcement, ‘Milk he no good. Me suck
(chuck) ’im away. He full plenty big black pigeon.’ With no little
interest we prepared to make the acquaintance of the big black
‘pigeon,’ ignorant at that time that the word ‘pigeon’ is applied by
the Murray Islanders to any living thing that is not obviously a four-
footed animal. We found an open tin of condensed milk swarming
with large black ants.”
Ten years previously, when in Mabuiag, I sent Dick, the boy who
used to fetch and carry for me, to a fresh-water pool with a net and
bottle to see what he could catch. He returned in high glee crying,
“Doctor, I catch ’im pigeon belong water-hole.” The “pigeons”
happened to be some small water-beetles.
Very shortly before we left I invited the Mamoose, Pasi, who is the
Mamoose of Dauar, and Jimmy Dei, the Sergeant of Police, to dinner.
We gave them soup, curry and rice, rice and honey, and pancakes.
Judging from the quantities they ate they enjoyed themselves very
much. Afterwards we gave them songs and music on the
phonograph, and I obtained their autographs, for it is not often that
one has two kings to dinner.
Rivers had asked them twice before, when some of us were in
New Guinea; on one occasion when Pasi went home he saw his
eldest son nursing a very small infant, and he asked him, “What man
belong that boy?” “Why, poppa,” was the answer, “he belong you!”
His wife had presented Pasi with a baby when he was out to dinner.
According to the common practice of the island, Pasi had promised
the unborn babe to a native named Smoke, who, having no children
of his own, had expressed a wish to “look out for it,” or in other
words, to take care of it; a zogo is said to “look out garden.”
I was informed by Myers that at this supper Harry, the Mamoose,
and Pasi each asked for three helpings of curry, and three of rice
with jam and marmalade. Pickles and marmalade proved an
irresistible attraction. Even Pasi, who has travelled as far as
Thursday Island, had never met with marmalade before.
When Harry began his third helping Pasi spoke to him in the
Miriam tongue, “Only take a little.” The hosts knew enough of the
language to understand what was said, and, to the evident
amusement of the two guests, persuaded Pasi also to “take a little.”
Cigars were given them after dinner, which they were polite
enough to pretend to relish. Harry’s cigar remained almost
unsmoked; a New Guinea boy finished Pasi’s. Although smoking was
practised in these islands before the white men came, and they grew
their own tobacco, they never smoked much at a time.
The native pipe is made of a piece of bamboo from about a foot to
between two and three feet in length. The natural partition at the
one end, and the intermediate one, if such occurs, is perforated. At
one end of the pipe there is always a complete partition, and near
this a small hole is bored; into the latter a small wooden or bamboo
tube, a few inches in length, is inserted. The tobacco is put in this,
and the open end of the pipe applied to the mouth, and by suction
the pipe is filled with tobacco smoke. I have seen them put their
mouth to the bowl and blow down it. As soon as the pipe is filled
with smoke, the right hand is applied to the open end and the bowl
removed. This hole is applied to the mouth, and the smoke sucked
through it after the withdrawal of the hand from the open end. The
length of the pipe causes such a draught that the smoke is violently
inhaled.
When a man has had a suck he will put his hand to the open end
of the pipe to prevent the escape of the smoke and pass it on to
another, who receives it, and maybe transmits it to a third in the
same manner. The women usually prepare the pipes, and pass them
on to the men. This method of smoking occurs over a considerable
portion of New Guinea, but, so far as I am aware, it is confined to
the Papuans.
The effect of this kind of smoking appears to be very severe. The
men always seem quite dazed for a second or two, or even longer,
and their eyes water; but they enjoy it greatly, and value tobacco
very highly, they will usually sell almost anything they possess for
some. I have seen an old man reel and stagger from the effects of
one pull at a bamboo pipe, and I have heard of a man even
dropping down on the ground from its effects.
To return to this supper party. When the guests were trying to
enjoy the cigars, Jimmy Dei arrived in a very excited condition,
bringing to the chiefs news of apparently no small importance. It
transpired that he, in his capacity as Sergeant of the Police, had
reported the assault of an islander upon his wife, who had
thereupon summoned her husband to appear at the court-house on
the following day. Any excitement of this kind is always most
welcome to such an impressionable people as these are.
Myers has kindly given me an account of the following
circumstance that happened when I was in New Guinea:—“We were
awakened one morning by the sound of voices in the ‘kitchen’—that
is, the space below the verandah on which we slept. They were the
voices of Debe Wali and his wife, between whom short and quickly
answered sentences were passing. Louder and louder grew their
talk. Suddenly a blow was heard, followed by a metallic noise and
the sound of falling water. There was silence for a time, then softer
talking, and a woman’s low cry. Up came Debe Wali to us, labouring
to suppress the most intense excitement. ‘Woman belong me want
me go bush (i.e. to the garden). Me I no go. I cook here. I say to
woman, “You go.” She say, “No, you go.” I tell ’im, “You sh-sh.” He
no sh-sh. I tell ’im, “You be quiet: you wake ’im white man; he
sleep.” He talk on. I hit ’im with saucepan. Hold on. I fetch ’im.’ And
Debe vanished below to reappear with his weapon, which, as he put
it, he had ‘capsized’ on to his wife. A few minutes later the little
woman, one of the hardest-working on the island, came to us to be
treated for a terrible gash down to the bone on the back of her
head, which had to be sewn up. Debe was much alarmed on the
following day, for Kaige, the policeman, insisted on roaming about
the verandah and kitchen, mainly occupied in consuming our
tobacco. Had Debe not been our servant, he would undoubtedly
have been summoned by his wife, and, this being his fifth offence in
this direction, he would have been sent a prisoner to Thursday
Island. To show his penitence he wore all day a black kerchief round
his head; while, to smooth the ruffled feelings of his wife, he bought
from us (out of his next week’s wages) some yards of red twill which
he presented to her.”
Mr. Bruce has informed me by letter that early in 1899 Jimmy Rice
and Debe Wali had, for them, a serious quarrel. It happened in this
wise. Pedro, a Manila who had married Jimmy’s wife’s daughter by a
former husband, D. Pitt, had given Jimmy a small cutter. Jimmy’s
wife considered the boat was given to her as a present for her
daughter’s sake, so she began to “boss” the boat and crew. Debe
was captain, while Jimmy remained on shore to cook the bêche-de-
mer.
Jimmy’s troubles now began in earnest. First his wife thought that,
as she was owner of the boat, it was beneath her dignity to cook for
Jimmy, and told him when he asked for his breakfast or dinner to go
out and eat filth. Poor Jimmy asked Bruce for advice.
Shortly afterwards the “fish,” as bêche-de-mer is colloquially
termed, they obtained was demanded by Pedro, as owner of the
boat. This Jimmy gave him. Then the crew wanted their wages.
Jimmy said he had nothing to give them, that they were all his
friends, and had promised to work for nothing to clear the boat.
Debe Wali said no; he wanted wages. Jimmy and his wife had a bad
time of it, so the latter went to the Mamoose and summoned Jimmy
for wages.
 The police then told Jimmy he was summoned; and great was the
clatter of tongues and mutual abuse. Debe ran into his house and
brought out a big rowlock of a boat, and stabbed Jimmy in the chest
with it. Of course it did not do Jimmy the least harm, but he
commenced shouting “Police! police!” knowing well enough that the
police were standing by and witnessing the whole affair. Of course
the police had to arrest Debe. Next day there was a cross-summons
in the court—one for wages, the other for assault.
We have here an interesting example of the confusion that arises
in the transition between one economic condition and another.
Formerly communal labour was the rule. If a well had to be sunk or
a house built, all friends would lend a hand, a feast with the
concomitant excitement being a sufficient immediate reward, the
reciprocity being, of course, fully recognised. Pedro’s loan of a boat
on the hire system of purchase is well understood. Before the white
man came it was customary for the Torres Straits Islanders to
purchase their canoes on what was virtually the three years hire
system. The crew demanding wages belongs to the new economic
custom introduced by the Europeans.
Pedro, the owner of the boat, was drowned in the hurricane that
swept across Northern Australia in March, 1899, and Jimmy had to
pay D. Pitt the balance due on the boat.
The new Erub (Darnley Island) church was to be opened in
September; and when the Murray Island contingent was about to
start to take part in the festivities, Finau could not get a passage for
himself or family unless he went with the Murray Islanders; so he
asked Jimmy to lend him his boat. Jimmy said he could not lend it.
Two months afterwards Jimmy’s cutter went to Garboi sandbank
to fish, and the crew slept on shore the first night. When they awoke
next morning no cutter was to be seen; she had parted her chain in
the night and had drifted away. So poor Jimmy lost his boat and all
his labour, and the worst of it is, he has the haunting fear that it was
the direct act of God because he did not lend his boat to the South
Sea teacher when he asked for it. All the people assert this is the
true explanation of his loss.
Jimmy is a happier man since his wife has ceased to be a
boatowner, as she now condescends to roast yams and cook fish for
him. Debe and he are as good friends as ever, and are always
plotting how they can get as many shillings as they can for the least
amount of work, and on the whole they succeed very well.
Debe is now the proud father of a pretty little daughter, and
devotes a good deal of his time to nursing it. Occasionally he has a
row with Kaima, his wife, when he considers she is not doing the
nursing in a scientific manner. Then he generally takes the
management of the baby for a time, but the infant does not fail to
proclaim when it is Debe’s watch on deck.
On Friday, August 4th, 1899, there were two earth tremors on
Murray Island. I cannot do better than transcribe Mr. Bruce’s vivid
description of the occurrence. “I had just sat down to lunch when
the iron roof and the verandah floor made such a clatter that I could
not at all make out what was wrong; about five minutes later there
came another and stronger shock. I jumped up and went on the
verandah.
“There was a great crowd of men playing hockey on the sand
beach in front of the house, and at first I thought some of them had
been larking on the verandah, but when I went out everything was
quiet. They were sitting down; not a word broke the deathlike
stillness. I thought at first they were resting after their game, but
even then they never sit still. I asked, ‘What’s wrong’? Then some of
them came up and said, ‘Why, ground he jump up and down all the
same as sea’!
“Then it struck me at once what had happened. I asked them how
they felt when the shock came. They said the whole beach was
heaving like the sea so that they could not stand. Some said they
felt sick and wanted to vomit; others said everything looked blurred
and indistinct, and men’s faces were all distorted when they looked
at them.
“I was sorry I was in the house at the time, as I should have liked
to experience the sensation. I should think each shock must have
lasted about two minutes, with an interval of five minutes between
them.
“After evening school I saw some of those who had been to their
gardens on the top of the hill. From their description the earthquake
was felt worse up there. Pasi told me he was sitting down on the
ground nursing the baby when the first shock came, and he and the
baby commenced to bob up and down, and he felt as if he were
sitting on something that was giving way with him. When the second
shock came, the coconuts on the trees were bobbing up and down,
everything was trembling and swaying; a bucket on the ground
opposite him was jumping up and down. He thought it was the devil,
and that he was bewitched, so he got up and called his wife to come
away. Soon they met other frightened people running home. Pasi
said he was ‘very glad to hear all man feel him all the same as
myself.’
“No doubt the people received a great scare. They were going
about in quite a subdued manner for a few days. When Sunday
came they were told by Finau that God was angry with them. God
has been very angry with them here this year; they were told the
same after the hurricane took place. But then I remember the
Princess Alice disaster on the Thames was referred to in the same
manner by Mr. Spurgeon at the Tabernacle; so we cannot wonder at
the coloured teacher attributing all disasters to the wrath of an
offended Deity.
“I had rather an amusing reason given to me why the cyclone of
the 4th and 5th of March (1899) happened. There was a crowd of
boats anchored in the bay, and a South Sea man wanted to hold a
service on the beach, but very few went to hear him pray. Whilst he
was praying, some unregenerate nigger had the impiety to play on
his concertina. That day the hurricane came. The men who told me
this thoroughly believed, since the praying South Sea man had
asserted it, that God had sent the hurricane because of that man
playing the concertina.
“That is the kind of God they like to have described to them, and
no other. Really the South Sea teachers know the kind of God to
depict to the native far better than the white missionary does; his
God of Love is beyond their comprehension. They look as if they
believed in Him, but converse with them, and you find the God of
Wrath is their ideal of what God is. He takes the place of Bomai, etc.,
which they have lost.
“At the opening of the new church at Erub, in September, all the
South Sea teachers from the Torres Straits were gathered together.
Captain H⸺ had just come across an article in a newspaper,
written by some German scientist, that a comet was to appear in the
heavens some time in October, and that it would strike our planet on
the 5th of November. The Captain described the comet to the Erub
Mamoose, who in his turn told the assembled teachers, and they,
not unnaturally, went to Captain H⸺ for further information. The
Captain, nothing loth, gave them what they wanted, with a practical
illustration of how the comet would act when it came in collision with
the earth. He got a ball of paper and a stick, making the latter
violently strike the ball of paper, which flew some distance away.
‘That,’ said he, ‘is the way our world will go, and I know that Old
Nick is preparing his fires for a lot of you fellows now.’
“The teachers held a meeting, and arranged that when each
teacher went home to his station he was to appoint three weeks of
special prayer, and to beseech God not to allow the comet to destroy
the earth. Finau arrived here full of it, and the people with him
arrived equally full of influenza through living in over-crowded
houses in Darnley.
“On Sunday I went as usual to church. At the close of the service
Finau told all the people to remain, as a special service was to be
held; so I remained along with the rest.
 “After a short interval Finau told them about the comet, and that a
very wise man had written in the newspaper that the world was
shortly to come to an end. This was true. He then read from the
Gospel of Mark, chapter xiii., from which he proved that this was the
time all these things were to happen, because this wise man said so
in the newspaper.
“He kept on until he had all the people in a proper state of fear.
Then he directly referred to me that I knew it was all true, and
would happen. I said ‘No.’ He took no notice, but told them that in
three weeks’ time, on the 5th of November, if God did not hear their
prayers, they would all be destroyed.
“After praying he invited anyone to stand up and pray and speak
on the subject of the comet. Immediately all the Murray Herschels
and Sir Robert Balls were on their feet, one after another,
expounding on comets and their destructive powers, and they also
finished up by saying, ‘Oh, it’s true! That wise man said so in the
newspaper.’ The subject suited them immensely.
“After they had all had their say, which occupied nearly two hours,
Finau told them from that day until the 5th of November there were
to be special prayers, asking God to rebuke the comet and make it
go another road away from the earth. They would all know in three
weeks’ time whether God had heard their prayers. If He did not
destroy the world then, that would be a sign that He had heard
them, and was pleased with them; but if the comet destroyed the
earth on the 5th of November, then they would understand that God
was angry with them, and wished to destroy them as a punishment.
“He then again referred to me as knowing it to be true. I had to
get up and speak (it was the first time I ever did so on church
matters). I told the people that I had not heard anything about this
comet, and that they were not to be afraid; that even if there was a
comet, it was not likely to interfere with our world, and even if it did,
I thought no harm would arise from it. They would all find, on the
5th of November, Murray Island would be quite safe, and everyone
would be going about their work as usual. I might as well have said
nothing; but there was so much sickness about (mainly influenza)
that I thought this frightening of the people would have an injurious
effect on them.
“The 5th of November came round, and nothing extraordinary
happened. So Finau appointed the 6th to be a day of thanksgiving to
God, because He had heard and answered their prayers by turning
the comet away from the earth.
“Thanksgiving took the form of prayers in the morning, feasting
and games in the afternoon. So you may be sure I had a good time
of it in school that Monday afternoon with the noise of the
thanksgiving outside and the inattention of the children inside.
“You people in England ought to be truly thankful that we have
such effectual fervent prayers in this part of the world. I think this
answer to prayer is quite as good as any I read in Mr. Stead’s Review
of Reviews last year. All that was wanting to make the wise man in
the newspapers and Finau’s predictions perfect was to have had the
earth tremors introduced in November instead of August, and then
what a tableau!
“Captain H⸺ is delighted at the good work he considers he has
done in stirring up the people to such a time of prayer. In his last
letter he says he has been the means of leading these South Sea
teachers and the natives to more earnest prayer through fear than
has ever been done by any individual in the Straits before.
“The Mamoose and Pasi left for Erub to attend the memorable
opening of the church a fortnight earlier than the general public, but
before starting the Mamoose left strict orders with the sergeant if
anyone made a storm of wind while he was away to find him out
and have him punished. No sooner did he start than it blew ‘old
boots’; no boat could leave the island, and the Mamoose had a
terrible passage.
“Kadud, the new Sergeant of Police, came to me and told me he
was looking out for the person who had made the wind, as the
Mamoose had given him strict orders to have him punished by a
fine. One day he came, saying he had found a dry coconut leaf stuck
in the creek at Kiam, and thought he would find the party. Another
day he would find a similar leaf and a shell stuck in the sand on the
beach. Kadud was getting furious, and all the time it was blowing a
hurricane. The storm lasted four weeks, so that the majority of the
people from Murray Island were late for the opening ceremony.
“For months they tried to find out the miscreant; Wali, being a
church member now, is past suspicion. It would make you laugh to
hear how seriously the Mamoose and Kadud talk when I ask them if
they have found out who it was that made the ‘big wind.’ ‘Oh no,’
they reply; ‘by-and-by we shall catch him.’
“Mappa, a Murray Islander—one of the L.M.S. teachers—is here at
present on a six months’ leave of absence; he is a shrewd, sharp
fellow, but a thorough native. He brought with him a young fellow
named Wai from his station at New Guinea, another sharper, who
has already a great reputation on Murray Island of being able to
make, injure, and kill, and Mappa backs him up. Tuk is the form of
sorcery he is supposed to practise, and the Murray people are
terribly frightened of it; they tell me the New Guinea men are very
powerful in tuk, and from Kiwai they can kill a whole village full of
people on Murray Island, nearly a hundred miles away.
“Wai first began practising on William, the deacon, who lives at
Dio. He went with some others to Dio, and showed William two
sticks of tobacco, and said ‘Tuk.’ William began to shake when Wai
told him to go and look in his box and see if he had lost any
tobacco. William, still trembling, got his key, looked in the box, and
said, ‘Yes.’ Wai held up the tobacco, and said, ‘This is it.’ William
replied, ‘Yes, that’s it.’ Wai exclaimed ‘Tuk,’ and the two sticks of
tobacco disappeared, much to the astonishment of the crowd.
William pressed a present on Wai, to secure himself against tuk.
When William told me about the affair I nearly exploded, trying to
keep serious, and endeavouring to sympathise with him. Wai is a
smiling, comedian-faced young fellow; he comes along to see me
every other day, and to have a smoke. Ulai and Mappa, a good pair,
are always extolling Wai’s great powers.
“A fortnight ago Mappa, who is taking Finau’s place, the latter
having gone on a visit to Mabuiag, had a crowd round him after a
Friday morning’s service, and used some strong language about
some men who had not attended church and about Kadud, who
owns a well at Kiam, about which he and the South Sea teacher
have a dispute.
“A woman named Deau went and told these men that Mappa was
speaking ill of them. They hurried along to the church compound,
Deau along with them. She then asked Mappa to repeat what he had
said, and told him he was bad man, that he thumped the pulpit with
his hand when preaching to them, and then went home and
thumped his wife. Mappa then began to tell her she was a bad
woman, a Samaria kosker—that is, a woman of Samaria. Deau could
not stand that, so she went to the police and summoned Mappa for
swearing at her by calling her a Samaria kosker. Mappa then
threatened the whole of Deau’s friends that he and Wai would put
tuk on them all. They were in a great panic; the sergeant, Kadud,
was nearly white when he came to see me, with some of the
threatened people, and asked if they could not arrest Mappa. They
all declared that Mappa had learnt tuk in New Guinea, and could
destroy them all if he chose.
“Mappa was summoned for slandering Deau, and dismissed on
this count; next he was charged with threatening the people. The
witnesses all held that when Mappa went back to New Guinea he
would destroy anyone he chose by using the sorcery of tuk. It was
tuk, tuk, and nothing but tuk. I asked Mappa if he had threatened
the people with this, and he said he had, and that he was angry. I
asked him if, when he went back to New Guinea, he or the Fly River
men could shoot tuk to Murray Island. He said they could, but he
was not sure about himself. I warned him to think about what he
was saying, and if he really believed that Wai could do such a thing.
He hummed and hawed, and said ‘No.’ That was all I wanted in
order to quiet the fears of the people, so I asked Mappa to tell the
Mamoose and the people that the Fly River men could not injure
them, and that neither he nor Wai knew tuk. He told them so, but at
the same time they did not believe him, and would rather have
heard him say that he and Wai were au kali tuk le (very big tuk
people). Mappa was dismissed from court, and advised not to
practise tuk any more whilst on his holidays. The whole tuk affair
has been very amusing. Mappa and his wife are now teaching the
Murray youths New Guinea dances, so that they may beat the Dauar
men on New Year’s Day.”
In a letter dated September 30th, 1900, Mr. Bruce gave us the
later history of some of our friends, and as it illustrates the social life
of the Murray Islanders in a very interesting manner, I do not
hesitate to print the greater part of it for the benefit of my readers.
“This year we are experiencing the results of a big drought. The
north-west monsoon, which generally brings a young deluge with it,
has been very mild this year, so mild, in fact, that but for the change
of winds we might say we had no ‘nor’-west.’ In December of 1899
we had good rains, which gave promise of a good harvest from the
gardens this year; but there has been such a dearth of rain in 1900
that all the garden stuffs died off. First the sweet potatoes went
(that is, the vines), for they never got to the length of tubers; then
the yams died off, but the people managed to get a few small ones
out of the crop. So the people are reduced to coconuts and bananas,
which are fairly plentiful. The natives are perfectly happy, carrying
on play night after night, and their boats lying idle at anchor, instead
of being at work getting black-lip shell, which has been a splendid
price this year, to buy flour and rice for their families. Douglas Pitt’s
son did very well with one boat working from here; he cleared £350
in six months with a crew of mainland boys, whilst the Murray men
did not clear as many shillings with seven boats which they obtained
from individuals to work out and on shares. They kept on getting
advances (‘draws’) of calico and tobacco, and do no work.
 “Your two ‘curry and rice chefs,’ Debe Wali and Jimmy Rice, both
got boats. Debe obtained all the draws he could out of the owner in
eight months, and collected about £4 worth of shell to pay about
£10 worth of draws. The consequence was, when he went to
Thursday Island for more draws the owner took possession of his
boat, and he was lucky to get it, because if she had remained much
longer at Murray Island she would have broken up on the beach.
Jimmy Rice, poor fellow, has not been quite so fortunate as his
friend Debe. In the first place, he could not get so many draws out
of his man as did Debe, and he had signed before the Shipping
Master, with a solicitor to see that all was fair and square. When
Jimmy got all the draws he could from the owner of the boat, he and
his crew refused to do any work, and they were taken before the
Shipping Master at Thursday Island. The Shipping Master prosecuted
them in court. All the crew, beside Jimmy Rice and Toik, decided to
go to work and finish the time they had signed for. Jimmy and Toik
held out, thinking they would be sent back to Murray Island by the
steamer, as she was coming out the day following; but they made a
mistake, and each of them got two months in jail to work out their
time. One of the young Pitts paid for a boat here in four months with
a mainland crew, and although the Murray men have these object
lessons before them, they seem to be no incentives to make them
go and do likewise, which they could easily do.
“Papi has a boat on half-shares from a Manila man named Zareal,
a jeweller at Thursday Island. Like the others, Papi was doing no
work after getting what he could out of Zareal; but he was lucky
enough to find a good pearl in a shell, so he took it to Thursday
Island and sold it for £150, then went flashing about town. Zareal
came to know of the pearl, and claimed half of its value for the boat;
but Papi objected, and got away from Thursday Island to Murray
Island with the cash. Not a bad haul for a Murray man! There is
likely to be trouble about it, but I bet my boots Papi comes off the
winner.
“You remember old Gasu; his eyes were bad. He is now quite
blind; can only tell the difference between night and day. He looks
physically well, but takes no exercise whatever, as he tells me he is
ashamed to go walking about with a boy to lead him. When I visit
him I give him a spin along the road, and he enjoys it immensely.
Poor old Gasu! He had not his equal on the island; a thorough,
genuine old gentleman, and quite free from all cant, although he
had his fears of the ‘White Man’s Zogo’ (the Church) like all the rest.
“The great drought this year has been put down to many causes.
Your party came in for some of the blame for taking away the good
doioms, so that the rain-makers were handicapped in giving a
plentiful supply. But the principal cause for a time was our old friend
Debe Wali; he was charged with defiling and throwing down the yam
zogo at Dauar, named Zegnaipur—this is the principal yam zogo.
Debe’s brother, Komabre, and Harry, the Murray Mamoose, were the
two head zogo men who prepare it every year. Komabre died last
year, and Debe, of course, believes someone was the cause of his
death, and the people say that he was angry at the death of
Komabre and knocked down the zogo, hence the drought. Mamoose
and Pasi came to me to have a talk about it, and wished to know if
they could not prosecute Debe in court. I told them they would have
to get proof that he had done the injury, well knowing they could get
none. Mamoose said he was certain Debe did the thing to spoil the
yams and food, and that the law should punish him. I had to cool
him off as best I could. The next one accused was Joe Brown. They
said, because he has a quarrel with Jimmy Dei, he burnt the coconut
zogo at Zeub by wilfully setting fire to the grass, and that he had
stopped rain from coming and blighted all the crops. It was very
amusing when I asked Debe and Joe confidentially why they had
been and gone and done it. A knowing smile stole all over their
faces, as much as to say, ‘I’ll teach them to interfere with me!’ Still,
they would never confess to anything, but you could see how
pleased they were at the prominent place they held among the
people. When I represented to them how they were making me
suffer too from having empty water-tanks, old Joe said, ‘By-and-by,
Jack, you stop; I make him all right; you see your tank full up by-
and-by!’ That ‘by-and-by’ means so much to them, and is such a
handy phrase I don’t know what they would do without it now!
“In the early part of the year I was pestered by the men who had
boats, and also by their crews, coming every day inquiring when the
big blow was to be. I told them it was impossible for me to fix any
stated time, but they knew we always had strong winds in the north-
west. It was of no use, they kept on coming to inquire. At last I
asked if anyone had been telling them there was to be a big blow.
They said yes, one man told them; but who he was they would not
say. Of course it made a good excuse for not going to work, and
they made the most of it and let the boats lie up.
“The following is an example of the power zogo men are credited
with. After Debe’s and Joe’s reputation was on the wane and being
forgotten, Mamoose and Jimmy Dei were in my house one day, and
the conversation turned on the everlasting drought, which both were
bewailing. I began to twit them about the powers of the rain-
makers, trying to bring them out. Mamoose did not like it, and
began to converse with his optics to Jimmy (Murray men do a lot of
talk on the quiet with their eyes). Jimmy assented, so Mamoose got
up out of his seat, looked out of the front door, then out of the back
—to make sure there was no one about who would be likely to hear
—sat down again, and after sundry ahems Mamoose whispered to
me the real cause of the drought. He said the rain-makers were
afraid to make rain and prepare the ceremony, in case they might
make too much wind along with it, and therefore cause another big
hurricane, like that of last March, and they feared the Government
would punish them if many lives were lost; besides, Gasu being now
blind, he could not see to prepare the zogo properly, and they were
afraid to make it! I had to condole with them on the hard luck of
having to risk the chances of either a cyclone or a famine, and
agreed with them that a famine was the safest, for, as Mamoose
said, the hurricane might smash up the island altogether. But I
assured him at the same time that the Government would on no
account hold them responsible for any damage done by any cyclone
in this part of the world. I never heard of any Murray man getting
the credit of making the hurricane last year; no doubt they have
been afraid to hint at it, and I have no doubt the people give the
honour to some of the zogo le for having caused that disaster.
“I had a gentleman living with me for a month or so; he came
from New Zealand, and is travelling all round, doing the ‘grand tour
of Australia, New Guinea,’ etc. He was grand company, although a
very strict churchman and an extreme ritualist. I had no idea colonial
high churchmen could be so high! He out-ritualed everything I had
ever seen or heard of, but he was one of the good sort who could
give and take a joke.
“We had a trip to Dauar one Saturday; went in the whale-boat,
and several passengers accompanied us. We had a walk all round,
and had a nice day of it. After we had returned home and had had
supper, and were sitting talking and smoking, a deputation headed
by Pasi, who is Mamoose of Dauar, came to inform me that those
who had accompanied us to Dauar had gone on purpose to see the
zogo of Wiwar. This is a round stone (sandstone) about the size of a
pumpkin; if it is prepared by a zogo man it has the power of causing
constipation, and the person affected will die if there is no antidote
used in the form of taking off the power of this zogo. Pasi had a
small packet in his hand, wrapped up very carefully, like tobacco, in
a dried banana leaf. He asked me if I would examine it, and spread
it out, telling me this was the cause of the sickness of an old lady
named Sibra. She remembered that the last time she had been over
to Dauar she had passed the zogo Wiwar, and now knew the cause
of her sickness. Her friends had gone over with us to find out if the
zogo was prepared; they were to take away the power of the zogo
by cleansing it with sea-water, and placing the leaf of a plant called
gebi on top of the stone, and pouring water over the stone. Pasi
wished to know if the police could apprehend old Lui, as he was the
only Dauar man who knew how to prepare the zogo. I asked Pasi
how the zogo was prepared; he said, ‘The zogole, after having a
stool, placed the excreta on the stone, using an incantation, in which
he referred to the person he wishes to blight.’ To prove the case, the
friends went to the stone and found it had been prepared, and
brought away a sample of the excreta with them. My visitor could
not refrain from laughing, although I warned him to keep serious.
Pasi said there was no chance of Sibra’s recovery, as the zogo had
been prepared too long. I was giving the old lady medicine, and
thought she was going on nicely, but on the Monday afternoon she
died. Of course old Lui got the credit of removing her, because they
had had a quarrel of words. The friends of Sibra do not consider our
law of much account, as Lui cannot be punished, even after the
strong evidence they brought to me. When Lui dies, his relatives will
charge Sibra’s relations with using a zogo, appropriate to whatever
sickness he may have been afflicted with.
“It was too much when Pasi asked my visitor to have a sniff, and
tell him if it was the real thing or not. He fairly exploded and roared,
and spoiled the whole effect, as I had to follow suit. The deputation
did not remain much longer, but carefully rolled up their sacred
bundle and left. They are very sensitive to ridicule, and do not like
their customs laughed at. The consequence was that they would not
for some time tell me anything that occurred of a similar nature. You
will perhaps think I ought to rebuke them and advise them not to
follow these old customs, but it is of no use doing this, as these are
so engrained into their everyday existence that they could not, as
yet, live without them. Their disappearance is, I think, only a matter
of time.
“It is very seldom that houses are burned down on Murray Island,
considering the inflammable material they are constructed of, and
the carelessness of the people with fire. This year, however, three
houses were burned down. The first one belonged to a widow
named Nicky. The people were all at one of their night plays, and
Nicky’s house was burned, and nothing saved. The play was a long
way from Nicky’s place, but it is considered that the spirit of her
deceased husband (Arus) was angry with her for her conduct, and
burned her house down. It was a serious loss to Nicky, as she has a
large family. I spoke to the Mamooses about getting the people to
assist her, and another widow, Anai, whose goods were also all lost
in the fire. The poor women had really saved nothing except their
petticoats. I gave them a start in goods, and I was really astonished
at the manner in which the people assisted; some gave her a
camphor-wood box, others half-bolts of calico, plates, spoons,
knives, and so forth, so the camphor-wood boxes were well filled
with useful articles, and calico galore. All vied in beating each other
in the giving line, and of course a ceremony was made in presenting
the goods. I only hope the next unfortunate will come off as well,
but I fear not, as it is so foreign to the Murray Islanders to give
without getting an equivalent in exchange. However, they deserve all
credit for the way in which they assisted Nicky and Anai, and ought
to make Arus’s lamar (spirit) leave the widow’s house alone in
future. The other houses were burned down in the daytime, and all
the contents saved.
“This year (1900) has been a fairly healthy year. Up to the present
there have been five deaths—two adults and three children. Matey is
dead; he was a young man about thirty years old; he died of
consumption, I think, and was ill for a long time. I tried to get him to
go to the hospital at Thursday Island, but he would not go. There is
a Queensland Aboriginal working in the boats at Darnley, who has
quite a reputation as a medicine-man. When Matey was very weak
he wished to be taken to Darnley to see this mainland boy. He was
taken over in a dying state. The mainlander had a look at him and
told him, ‘You fellow, you die; no more blood stop along you; two
day, three day, you finish!’ This consultation was quite satisfactory to
Matey and his friends, so Matey requested them to take him back to
Murray Island to die there. They started back with him, and as soon
as the anchor was dropped at Murray, poor Matey’s spirit took flight
to Boigu (an island to the west of Murray, where spirits are supposed
to live in a very happy state without any fears of brimstone).
“Murray Islanders have a great dread of dying anywhere than on
Murray, and no people have a greater love of their native land than
they have. Since this mainland boy on Darnley gave so good a
prognosis in Matey’s case, his reputation has gone up like a rocket,
and has not yet come down, several have gone over to consult him.”
 The natives of Erub and the Murray Islands frequently used to
make mummies of their dead relations. The details of the process
are not particularly edifying, and need not be narrated here. The
wizened corpse, which might almost have been made of papier-
mâché, so light was it, was lashed to a bamboo framework. To be
made more presentable it was painted red and pieces of mother-of-
pearl from a nautilus shell were inserted in the orbits, a round spot
of black beeswax serving for a pupil. Finally the mummy was decked
with various ornaments. When it was complete and inodorous a final
feast would be provided, and it would be suspended in the house.
There the mummy would remain, swinging with every breath of
wind and turning its gleaming eyes with each movement of the
head, until it fell to pieces with old age.
When the body crumbled away word was sent to the friends to
come and assist in cutting off the head. A big feast was held, and a
man who was skilled in making portrait faces in beeswax on skulls
was also present. Later the artist made the wax model of the
deceased’s face; anyhow, the length of the nose was accurate, as
immediately after death the length of the nose was measured with a
piece of wood, which was safely kept for the purpose of securing the
right proportion of the imitation nose.
When the face was finished the head was given to the nearest
male relative. The men then cried. Later it was taken to the women,
who also had a good cry. The inevitable feast followed, at which the
artist received a large share of food.
The modelled and decorated skulls of relatives were kept probably
partly for sentimental reasons, as the people are of an affectionate
disposition, and like to have memorials of deceased friends, but
mainly for divinatory purposes.
A duly decorated skull when properly employed became a divining
zogo of remarkable powers, and was mainly used in discovering a
thief, or the stolen article, or a man who had by means of sorcery
made someone sick. But this could only be done by bezam le, or
members of the shark clan, who were also members of the Malu
fraternity. All who engaged in this hunt went in the early evening to
the zogo house, and one of the zogole took the Main mask and put
it on, repeating a certain formula. After leaving the house, the
zogole carried the skull in front of him, and all marched with a
particular gait till they heard a kind of grasshopper called kitoto, and
they rushed in the direction from which the noise proceeded. One
particular kitoto was believed to guide the men to the house of the
offender. Should the men lose the right direction the kitoto would
wait for them to come up, ever and again making its sound, “Sh, sh.”
Ultimately they were led to a house, and this must, of course,
according to their ideas, be the house of the malefactor.
It was of no use for the man to deny the evil deed, for kitoto had
found him out; and, moreover, the bezam le were so powerful that it
was as much as his life was worth to resist. If he happened to be a
bezam le himself he might try to brazen it out among his friends; but
if he was an outsider it would be useless, and he would have to pay
the fine.
I was naturally anxious to obtain one of these divining heads;
even by the time of my former visit they had all been done away
with, at least, so I was informed. I had therefore to be content to
have a model made for me. (Plate XII., B, No. 2; p. 139.)
First a skull had to be procured—and for other reasons I was very
desirous of making a collection of skulls; but it was long before I
could obtain any (I am referring now to my former visit), though I
constantly said, “Me fellow friend belong you fellow. ’Spose you get
me head belong dead man, I no speak. ’Spose you get him, I no
savvy what name you catch him, that business belong you fellow.
What for I get you fellow trouble?”
Eventually I came across a man who volunteered to get me some,
and I promised to give him sixpence per head; or, as I put it to him,
“One head belong dead man he sixpence, one head belong dead
man he sixpence; you savvy?” and as I spoke I touched and turned
down, native fashion, the fingers of the left hand, beginning with the
little finger. He understood perfectly.
 Next day he brought me a basket of skulls, and he could tell me
the names of some of them, too! As he handed out one skull and
mentioned a man’s name, I noticed that the nursemaid of the
missionary’s wife, who was standing by, looked rather queer; but as
it was none of my business, I took no notice. Later I found that the
skull in question belonged to the girl’s uncle! I do not believe she
objected to my having the skull, but that the other man should have
the sixpence—the money had gone out of the family. When paying
the man I ticked off each skull on the fingers of my left hand, and
paid for it; but I had not enough sixpences, and so gave him half a
crown for five skulls. At this he looked very askance, although I
assured him the payment was quite correct. Fortunately Bruce was
standing by, and said he would give him five sixpences for it at the
store. My friend Baton made me one or two divining heads from
these skulls in the “old-time fashion.”
Hearing one day, during my former stay at Murray, that a woman
had died, and being grieved at the particular circumstances
attending her death, I determined to pay my visit of condolence.
After dark I went to the village where she had lived, and found her
laid on the beach with her head to the sea, and clothed in her best
dress and wearing her new hat, all her fancy calico being laid on the
body. The husband was sitting at the head, and close by were
several men, women, and children laughing and chattering over their
evening meal. Then the brother came up and bent over the body,
wailing and sobbing.
Shortly afterwards a canoe was brought to convey the corpse to a
more populous village, so that they might have a good cry.
Then I saw one of the most impressive sights it has yet been my
lot to witness. It was a beautiful tropical moonlight night, the sand
beach being illuminated with soft whiteness by the moon, and
countless stars glittered overhead. On one side the strand was
bordered by the gently lapping waves of the calm ocean, and on the
other by a grove of coconut palms, their grey stems, arising from a
confused shadow of undergrowth, topped by sombre feathery
crowns, a peaceful adjunct to a scene of sorrow, and the antithesis
of the ghastly mockeries of the funeral plumes of the professional
upholstery, which have only lately been abolished in England. A
small crowd of some twenty or so of us were walking along the
beach with the noiseless footfall of bare feet, keeping abreast of the
canoe which, with its sad freight, was poled along by the husband at
one end, and the brother at the other. As I saw the black silhouette
of the canoe and its crew against the moonlit sky and sea, silently
gliding like a veritable shadow of death, and heard the stillness of
the air broken by the moaning of the bereaved ones, my mind
wandered back thousands of years, and called up ancient Egypt
carrying its dead in boats across the sacred Nile—there with pomp,
ceremony, and imagery, here with simplicity, poverty, and stern
realism.
At length we came to the village, the inclosure of which was
covered with family groups, mothers with babies surrounded by their
families, and many a little one was laid asleep upon the sand, well
wrapped up to keep off the flies.
The corpse was carried to a clear space, and again the gay
trappings of life were spread over the dead. An old woman, I believe
the deceased’s mother, came to the head, and sitting down, bent
over the body and commenced wailing. Then on all sides the cry was
taken up mainly by the groups of women who by this time had taken
their places round the dead. As one dropped out, another would join
in, and so with varying accessions in volume, occasionally dying
away to all but silence, the mournful sound continued through the
night, rising and falling in weird manner, recalling to my memory the
keening I had heard in far-away Kerry eighteen months previously.
Then I left them. The dead one surrounded by a changing circle of
weeping women; beyond, the family groups each illumined by its
own flickering fire, babies asleep, children playing, adults talking,
young men laughing, and a little love-making taking place in the
background; and above all the quiet, steady, bright face of the moon
impassively gazing, like Fate, on the vicissitudes of human life.
 CHAPTER VII
KIWAI AND MAWAITA

We left Murray Island at 10 a.m., September 8th, by the Nieue,

which the Rev. James Chalmers very kindly sent to us. A small crowd
assembled to bid us farewell, and I know many of the natives were
genuinely sorry that we were leaving. We spent such a happy and
profitable time there, that we shall always have a soft corner in our
hearts for this beautiful island.
We reached Erub (Darnley Island) about 3 p.m., landed, and
called on Captain H⸺, who entertained us with his reminiscences
of New Guinea. We sailed at daybreak next morning, and reached
Daru in the early afternoon. About midday we ran on to a sandbank,
but as the tide was rising this did not much matter; in fact, it was
rather convenient, as we were thus enabled to have a meal on a
steady boat, a matter of importance to some of our party.
At Daru we were boarded by Mr. H. W. de Lange, the Sub-
Collector of Customs. Our little formal business was soon over, and
we then called on the Hon. Bingham A. Hely, the very efficient
Resident Magistrate. He kindly asked us to dinner, and we had an
interesting talk about the natives of his division. Mr. Hely has lately
made some observations on the important subject of totemism. On
Sunday, September 11th, we arrived at Saguane in the forenoon,
and Tamate, my old friend the Rev. James Chalmers, who has been
described as the Livingstone of New Guinea, gave us a hearty
welcome.
Unfortunately Mrs. Chalmers was ill with fever, which had
prostrated her for some time. Tamate, as he likes to be called by his
black and white friends, had also been quite ill from the effects of a
nasty fall from a verandah in the dark, and he was scarcely well yet;
indeed, it appeared to me that his health was much shaken, and no
wonder, when one remembers all the hardships and privations he
has undergone during his strenuous life of self-sacrifice.
Saguane is a small village at the southern extremity of Kiwai
Island. The native village is dilapidated, and has a poverty-stricken
appearance, probably owing to the fact that the village is only
occupied for part of the year.
The Mission premises were adequate, but as little money as
possible had been spent upon them, as even then it was by no
means certain that Saguane would remain the permanent
headquarters of the Fly River branch of the London Missionary
Society. The buildings consisted of the Chalmers’ comfortable house,
the church, which was also used as a schoolroom, a good
schoolroom for the seniors, a study, and other rooms, also the South
Sea teachers’ houses, the students’ houses, and various offices.
Saguane was a central and convenient spot for the Mission, but
that is about all that could be said in its favour. The whole island is
but little above sea-level; it is malarial, and the water-supply is poor.
Although the place does not look healthy, Chalmers says it is the
healthiest part of the district, except Daru. A considerable amount of
Mission land had already been washed away by the sea, that end of
the island having been greatly reduced in size of late years; indeed,
since this account was written, the Mission station had practically
been devastated by the sea, and Mr. Chalmers had commenced to
build a new station on Daru.
From many points of view it was a disheartening place, and it was
a wonder Tamate bore up so cheerfully. He had great difficulties with
teachers, South Sea men are often unsatisfactory, and the Torres
Straits islanders are practically useless as native teachers; so Tamate
was endeavouring to educate his own men as teachers, but it was a
long and wearisome task. Tamate had a very large area under his
charge, his district was undermanned, and he was greatly in need of
money help, as he was naturally very anxious to have a steam-
launch for river work. Alas! Tamate will never require the steamer for