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Neural Basis of Motivational and Cognitive Control
Neural Basis of Motivational and Cognitive Control

edited by Rogier B. Mars, Jérôme Sallet, Matthew F. S. Rushworth, and

Nick Yeung

The MIT Press

Cambridge, Massachusetts
London, England
© 2011 Massachusetts Institute of Technology

All rights reserved. No part of this book may be reproduced in any form by any electronic or mechanical
means (including photocopying, recording, or information storage and retrieval) without permission in
writing from the publisher.

For information about special quantity discounts, please email [email protected]

This book was set in Times Roman by Toppan Best-set Premedia Limited. Printed and bound in the
United States of America.

Library of Congress Cataloging-in-Publication Data

Neural basis of motivational and cognitive control / edited by Rogier B. Mars . . . [et al.].
p. ; cm.
Includes bibliographical references and index.
ISBN 978-0-262-01643-8 (hardcover : alk. paper)
1. Motivation (Psychology)—Physiological aspects. 2. Cognition—Physiological aspects. 3. Frontal
lobes. I. Mars, Rogier B.
[DNLM: 1. Motivation—physiology. 2. Cognition—physiology. 3. Frontal Lobe—physiology.
QP 409]
QP409.N48 2012
612.8′233—dc22
2011010089

10 9 8 7 6 5 4 3 2 1
Contents

Preface ix

I ANATOMICAL BASIS OF CONTROL 1

1 Neuroanatomical Basis of Motivational and Cognitive Control: A Focus on

the Medial and Lateral Prefrontal Cortex 5
Jérôme Sallet, Rogier B. Mars, René Quilodran, Emmanuel Procyk,
Michael Petrides, and Matthew F. S. Rushworth
2 Neural Circuits of Reward and Decision Making: Integrative Networks
across Corticobasal Ganglia Loops 21
Suzanne N. Haber
3 Neurochemistry of Performance Monitoring 37
Markus Ullsperger

II A CORTICAL PERSPECTIVE ON THE FUNCTIONAL BASIS

OF CONTROL 51

4 Contributions of Ventromedial Prefrontal and Frontal Polar Cortex to

Reinforcement Learning and Value-Based Choice 55
Erie D. Boorman and MaryAnn P. Noonan
5 Decision Making in Frontal Cortex: From Single Units to fMRI 75
Steven W. Kennerley and Philippe N. Tobler
6 A Comparative Perspective on Executive and Motivational Control by
the Medial Prefrontal Cortex 95
Mark Laubach
7 Top-Down Control over the Motor Cortex 111
Rogier B. Mars, Franz-Xaver Neubert, and Matthew F. S. Rushworth
vi Contents

8 A Role for Posterior Cingulate Cortex in Policy Switching and Cognitive

Control 127
John M. Pearson, Benjamin Y. Hayden, and Michael L. Platt

III A SUBCORTICAL PERSPECTIVE ON THE FUNCTIONAL BASIS

OF CONTROL 145

9 Subcortical Contributions to the Motivational and Cognitive Control

of Instrumental Performance by Pavlovian and Discriminative
Stimuli 149
Mimi Liljeholm and John P. O’Doherty
10 The Influence of Dopamine in Generating Action from Motivation 163
Mark E. Walton, Jerylin O. Gan, and Paul E. M. Phillips
11 Fronto-Basal-Ganglia Circuits for Stopping Action 189
Ian Greenhouse, Nicole C. Swann, and Adam R. Aron
12 Learning, the P3, and the Locus Coeruleus-Norepinephrine System 209
Sander Nieuwenhuis

IV INDIVIDUAL VARIATIONS IN CONTROL 223

13 The Neurocognitive Development of Social Decision Making 227

Wouter van den Bos and Eveline A. Crone
14 Motivational Modulation of Action Control: How Interindividual Variability
May Shed Light on the Motivation-Control Interface and Its Neurocognitive
Mechanisms 243
K. Richard Ridderinkhof, Michael X Cohen, and Birte U. Forstmann
15 Pathological Changes in Performance Monitoring 263
Ellen R. A. de Bruijn and Markus Ullsperger

V COMPUTATIONAL MODELS OF MOTIVATIONAL AND

COGNITIVE CONTROL 281

16 Neural Correlates of Hierarchical Reinforcement Learning 285

José J. F. Ribas-Fernandes, Yael Niv, and Matthew M. Botvinick
17 Reinforcement Learning, Conflict Monitoring, and Cognitive Control:
An Integrative Model of Cingulate-Striatal Interactions and
the ERN 311
Jeffrey Cockburn and Michael Frank
Contents vii

18 An Integrative Theory of Anterior Cingulate Cortex Function: Option

Selection in Hierarchical Reinforcement Learning 333
Clay B. Holroyd and Nick Yeung
19 Meta-Learning, Cognitive Control, and Physiological Interactions between
Medial and Lateral Prefrontal Cortex 351
Mehdi Khamassi, Charles R. E. Wilson, Marie Rothé, René Quilodran,
Peter F. Dominey, and Emmanuel Procyk
20 Wherefore a Horse Race: Inhibitory Control as Rational Decision
Making 371
Pradeep Shenoy and Angela J. Yu

VI PERSPECTIVES 389

21 The Neuroeconomics of Cognitive Control 393

Gabriele Chierchia and Giorgio Coricelli
22 Frames of Reference in Human Social Decision Making 409
Laurence T. Hunt and Timothy E. J. Behrens
23 Model-Based Approaches to the Study of the Neural Basis of Cognitive
Control 425
Sven Bestmann and Rogier B. Mars

Contributors 441
Index 445
Preface

This volume deals with a simple question: How does the brain choose efficiently
and adaptively among available options to ensure coherent, goal-directed behavior?
Hidden behind this question are many problems that necessitate a multidisciplinary
approach. Indeed, to understand how humans and other animals solve this problem,
we need answers from researchers versed in anatomy, traditional psychology, learn-
ing theory, neuroimaging, and mathematical modeling. The goal of this book is
to provide the reader with an overview of key approaches that researchers are
currently pursuing in this quest.

How This Volume Came About

This volume was inspired by a meeting of the same name held at St. John’s College,
Oxford, June 2 through 4, 2010. The meeting was the fourth in a series that started
around the turn of the century with a meeting in Jena, Germany, organized by
Michael Coles and Wolfgang Miltner. That first meeting was motivated by an upsurge
of research interest in the error-related negativity (ERN), a component of the human
event-related brain potential that is elicited in the anterior cingulate cortex following
errors in simple choice reaction-time tasks. The discovery of the ERN by Michael
Falkenstein and colleagues in the early 1990s provided a clearly observable neural
correlate of a key aspect of cognitive control: the ability to monitor ongoing thought
and action to identify situations in which effortful, intelligent control is required.
The Jena meeting was followed in 2003 by a meeting in Dortmund, Germany,
organized by Markus Ullsperger and Michael Falkenstein. By the time of this
meeting, two prominent theories of the ERN had been proposed—the reinforce-
ment learning theory of Holroyd and Coles, and the conflict monitoring hypothesis
of Botvinick, Carter, and Cohen—giving rise to the meeting’s title: “Errors, conflicts,
and the brain.” Both theories were grounded in formal computational models
that could account for a number of behavioral and physiological phenomena
observed in the psychological literature and that proposed possible underlying
x Preface

neural architectures. Meanwhile, the ERN was being investigated in an increasing

number of research fields, extending from traditional cognitive neuroscience to
developmental psychology and psychopathology. This meeting resulted in a book
edited by the organizers and published by the Max Planck Institute for Human
Cognitive and Brain Sciences.
A third meeting, “Errors, conflicts, and rewards,” was organized in 2006 in
Amsterdam, the Netherlands, by Richard Ridderinkhof, Sander Nieuwenhuis, and
Rogier Mars. Reflecting the growing scope of research on cognitive control and
performance monitoring, this meeting also included researchers working on nonhu-
man primate and rodent models of control. The title of the meeting also featured
the word “reward,” signifying the increasingly evident convergence between research
on performance monitoring and cognitive control, on the one hand, and studies
of reward-guided learning and decision making on the other. Ridderinkhof, Nieu-
wenhuis, and Todd Braver edited a special issue of the journal Cognitive, Affective,
and Behavioral Neuroscience (2007, 7:4) with contributions from speakers at
this meeting.
The fourth meeting, held in Oxford in 2010, followed these trends of increasing
the scope of the research presented while maintaining an emphasis on conceptual
and methodological convergence in studies of the motivational and cognitive control
of behavior. In addition to psychologists and cognitive neuroscientists, the speaker
list included a zoologist, a behavioral economist, an anatomist, and a number of
researchers with a background in engineering and machine learning. From a meeting
focused on developments around a small number of event-related potentials, the
meeting has expanded into a medley of approaches, each addressing the same
underlying question: How does the brain choose efficiently and adaptively among
available options to ensure coherent, goal-directed behavior? We have invited
contributions to this volume from researchers working in a wide range of fields,
reflecting the spectrum of approaches present at the meeting.

Organization of the Book

This book is aimed at a graduate audience in all fields of research that deal with
motivational and cognitive control. We hope that, besides providing an overview
of cutting-edge research in the area, the volume will serve as a handbook that can
be used by psychologists, biologists, economists, and neuroscientists alike. The con-
tributors have been asked to situate their own findings and theories in the context
of authoritative overviews of the relevant fields. For ease of further study, each
chapter includes boxes with suggestions for further reading and questions that are
outstanding in the field. In addition, interim summaries between the parts aim to
integrate their contents into the wider literature.
Preface xi

The book begins with a consideration of the anatomical basis of control. The three
chapters in part I each deal separately with one core component of the control
system: the mechanisms of high-level control within the prefrontal cortex; the mech-
anisms of motivated action selection and learning in the basal ganglia; and the
mechanisms of modulatory control by monoamine neurotransmitter systems. In the
first chapter, Sallet and colleagues focus on anatomical aspects of the interaction
between lateral and medial prefrontal cortex, a prominent feature of many models
of cognitive control. The chapter by Haber focuses on the connectivity of basal
ganglia circuits, which are increasingly recognized as providing a crucial point
of convergence between cognitive and motivational influences on behavior.
Haber describes the various pathways of communication within reward circuits of
the brain and between reward and association circuits, and the interactions among
these networks. In the third chapter, Ullsperger describes the role of modulatory
neurotransmitters in control, focusing primarily on dopamine, serotonin, and
norepinephrine.
Part II addresses the contributions of the cerebral cortex to control. Building on
the anatomical perspective taken in the first section, these chapters focus on the
functional architecture of cortical control. The chapters by Boorman and Noonan
and by Kennerley and Tobler provide complementary perspectives on the contribu-
tions of subregions within prefrontal cortex to action selection and choice based on
reinforcement value. Laubach focuses on the frontal cortex in rats, providing a basis
for the expanded cortex in human and nonhuman primates discussed in the follow-
ing chapters. Mars and colleagues look at how the prefrontal cortex exerts control
via modulation of activity in posterior brain areas. Pearson and colleagues extend
the field of focus from the frontal lobes to the posterior cingulate cortex, a region
of the brain often seen in imaging experiments of control but thus far largely
neglected in the literature.
Part III considers the many ways in which subcortical brain regions underpin the
control functions of the cortex. Two of the contributions focus on the role of the
basal ganglia: Liljeholm and O’Doherty review evidence on the role of the basal
ganglia in instrumental behavior, while Greenhouse and colleagues discuss the
contribution of these structures to a hallmark feature of cognitive control: response
inhibition. In the other chapters in the section, the focus is on the role of monoamine
neurotransmitter systems: Walton and colleagues provide an in-depth look at the
most widely studied neurotransmitter in the field of motivational control, dopamine.
In the final chapter, Nieuwenhuis reviews work on the locus coeruleous norepineph-
rine system, which influences cortical functioning through its widespread network
of cortical connections.
Whereas most chapters in this volume focus on group-averaged data, assuming
that the neural systems in question operate in a similar manner across individuals,
xii Preface

the contributions in part IV focus on three types of individual differences in control.

First, Van den Bos and Crone look at changes in neural control of social decisions
during the development from adolescence into adulthood, showing how neural
functioning and behavior undergo substantial changes during this period. Ridder-
inkhof and colleagues then review evidence regarding individual differences in
control in the adult population. Their chapter specifically focuses on how incorporat-
ing individual differences into one’s research can shed new light on the interface
between motivational and cognitive control. Finally, De Bruijn and Ullsperger
discuss performance monitoring in patient populations, showing how various neu-
rological and psychiatric conditions are associated with specific and identifiable
disturbances in cognitive control.
Research on cognitive and motivational control has historically benefitted greatly
from the use of explicit computational models of neural functioning. Part V takes
a closer look at recent developments in computational approaches that have been
particularly influential in this regard. Ribas-Fernandes and colleagues provide an
overview of formal models of learning, proposing a hierarchical reinforcement
model of behavior. This focus on reinforcement learning is followed in chapters by
Cockburn and Frank and by Holroyd and Yeung. Both chapters consider the rela-
tionship between the basal ganglia and prefrontal cortex in motivational and cogni-
tive control, while presenting somewhat contrasting accounts of the respective roles
of the basal ganglia and anterior cingulate cortex. The chapter by Khamassi and
colleagues provides a complementary perspective on “meta-control” and the mech-
anisms by which the control system is itself optimized. Once again, the focus is on
lateral and medial prefrontal regions. Finally, Shenoy and Yu adopt a Bayesian
approach that considers paradigmatic response inhibition tasks within a rational
decision-making framework.
The concluding part VI comprises three chapters that highlight recent overarch-
ing trends in the literature. Chierchia and Coricelli discuss the influence of concepts
and methodologies from economic decision theory on theorizing and experiments
in the study of control. Hunt and Behrens discuss how the approaches apparent in
this volume are now starting to be used to solve problems in more complex and
applied domains, focusing in particular on the neuroscience of social decision
making. Finally, Bestmann and Mars look at how computational models such as
those proposed in part V can be formally linked to the experimental data obtained
in neuroimaging and electrophysiology experiments.

Acknowledgments

As Jared Diamond and James Robinson state in their recent edited volume (Natural
Experiments of History, Harvard University Press, 2008), completing an edited book
Preface xiii

costs each editor on average two friends, because of the various levels of stress
involved in the process. We are grateful that this has not proven true in our case.
We thank all of our contributors, as well as the speakers and attendees of the Oxford
meeting, for making both the meeting and this book a success. We are tremendously
grateful to the International Brain Research Organization, the UK Neuroinformat-
ics Node, the Guarantors of Brain, and the McDonnell Network of Cognitive Neu-
roscience at the University of Oxford for their generous financial support, and to
the staff at St John’s College, Oxford, for their warm hospitality at the June meeting.
We thank MaryAnn Noonan, Laurence Hunt, and Vanessa Johnen for their able
assistance in organizing that meeting. We are delighted to be able to publish this
book with MIT Press, and would like to thank specifically Susan Buckley and Robert
Prior, who have provided unwavering support to a group of first-time editors. Finally,
we would like to thank our colleagues, friends, and families for their support during
periods of stress and strain as we worked on this volume deep into the night.
I ANATOMICAL BASIS OF CONTROL

The chapters in this section provide an overview of neuroanatomical and neuro-

modulatory systems at the core of control processes. In the first two chapters, the
focus is principally on two prefrontal regions—the anterior cingulate cortex (ACC)
and the dorsolateral prefrontal cortex (dlPFC)—and a basal ganglia region, the
ventral striatum. The last chapter of this section takes a complementary approach
to the classic neuroanatomical one by addressing the role of the different neu-
rotransmitter systems in monitoring performance.
One cannot understand the neural basis of control process without carefully
considering the architecture of the brain. As Richard Passingham stated: “Anatomy
is not tedious: it is fundamental.”8 One of the core criteria for subdividing the cortex
is its cytoarchitectonic properties, an endeavor that started with the pioneering work
of Brodmann and Von Economo. With the appearance of modern computational
and databasing techniques, it is now possible to compare individual differences
and create large databases and probabilistic maps of not only cytoarchitecture, but
also chemoarchitecture and connectivity.5 Indeed, connectivity has received much
attention recently, with demonstrations that each cortical area has a unique con-
nectivity fingerprint that constrains the information to which it has access.9 Neglect-
ing these fine anatomical properties of networks may prevent the identification of
functional subdivisions within each area, and then preclude any clear understanding
of integrated systems.
Chapters in this section emphasize the complexity of the connectivity patterns:
for instance, the clustering organization of prefrontal connectivity, the poor under-
standing of the interarea connectivity at a microscopic level, and the complex
convergent-divergent connections within basal ganglia pathways. Those results
show that a lot remains to be done to achieve a level of understanding of control
networks comparable to that of the visual system.2,6,11 Although recent progress in
imaging tools has allowed researchers to address the issue of the connectivity in
the human brain,4 most methods are constrained by the resolution of a voxel. Thus,
work on animal models remains essential,7 especially in order to understand brain
2 Part I

mechanisms at infra-voxel resolution—that is, at cortical layers, cell, and synaptic

levels. Furthermore, understanding the microarchitecture of a network also implies
one has to determine the neurochemical nature of the connections. For instance,
dopamine (DA) is a key molecule in many models of motivational and cognitive
control. In the reinforcement learning theory of performance monitoring,3 it is sug-
gested that DA acts on ACC pyramidal cells via D1 receptor. In the prefrontal
cortex, D1 and D5 receptors can be found on medium spiny neurons, with D5 recep-
tors also found on aspiny neurons typical of cholinergic interneurons.1 Those recep-
tors are principally found in layers I through III. Because DA effects within the
prefrontal cortex are complex and vary depending on the family of DA receptors,10
it is important to determine how DA is acting in the considered network.
In this section, but also in the wider literature, the focus is primarily on the pre-
frontal cortex and the basal ganglia. However, other areas are thought to play impor-
tant roles in cognitive or motivational control. The pre-supplementary motor area
(pre-SMA), inferior frontal junction (IFJ), intraparietal cortex, and insula have all
been suggested to play an important role in control mechanisms. However, apart from
pre-SMA, none of the aforementioned structures correspond to a specific cytoarchi-
tectural territory. The IFJ refers to the region at the junction of the inferior frontal
sulcus and the inferior branch of the precentral sulcus. In humans, caudal to this
precentral sulcus lies the rostral premotor cortex, in front of it and ventral to the
inferior frontal sulcus is area 44, and dorsal to this last sulcus is area 8. In monkeys,
these sulci do not exist, making identification of between-species homologs difficult,
although an equivalent area exists around the inferior branch of the arcuate sulcus.
Furthermore, the term intraparietal cortex refers to a number of cytoarchitectonic
areas lying within the intraparietal sulcus. In monkeys, those areas include the ventral,
lateral, medial, and anterior intraparietal areas (VIP, LIP, MIP, and AIP). Although
multiple areas are also found within the human intraparietal sulcus, the precise
homologs in humans and monkeys remain a topic of debate. Finally, the term insula
does not refer to only one cortical territory. On the basis of their degree of lamination,
three areas can be distinguished: agranular, dysgranular, and granular insula. It is
suggested that the insula, in interaction with the ACC, plays a role in motivational
control. As with the anterior cingulate and dorsolateral prefrontal cortex and basal
ganglia, which are the topic of this section, the terms insula, intraparietal cortex, and
IFJ should be used very carefully, as the ambiguity in the application of anatomical
labels complicates our understanding of the neuroanatomical basis of control.

References

1. Bergson C, Mrzljak L, Smiley JF, Pappy M, Levenson R, Goldman-Rakic PS. 1995. Regional, cellular,
and subcellular variations in the distribution of D1 and D5 dopamine receptors in primate brain.
J Neurosci 15: 7821–7836.
Anatomical Basis of Control 3

2. Douglas RJ, Martin KA. 2004. Neuronal circuits of the neocortex. Annu Rev Neurosci 27: 419–451.
3. Holroyd CB, Coles MG. 2002. The neural basis of human error processing: reinforcement learning,
dopamine, and the error-related negativity. Psychol Rev 109: 679–709.
4. Johansen-Berg H, Rushworth MF. 2009. Using diffusion imaging to study human connectional
anatomy. Annu Rev Neurosci 32: 75–94.
5. Mazziotta J, Toga A, Evans A, Fox P, Lancaster J, Zilles K, Woods R, et al. 2001. A probabilistic atlas
and reference system for the human brain: International Consortium for Brain Mapping (ICBM). Philos
Trans R Soc Lond B Biol Sci 356: 1293–1322.
6. Nassi JJ, Callaway EM. 2009. Parallel processing strategies of the primate visual system. Nat Rev
Neurosci 10: 360–372.
7. Passingham R. 2009. How good is the macaque monkey model of the human brain? Curr Opin
Neurobiol 19: 6–11.
8. Passingham RE. 2007. Commentary on Devlin and Poldrack. Neuroimage 37: 1055–1056.
9. Passingham RE, Stephan KE, Kotter R. 2002. The anatomical basis of functional localization in the
cortex. Nat Rev Neurosci 3: 606–616.
10. Seamans JK, Yang CR. 2004. The principal features and mechanisms of dopamine modulation in the
prefrontal cortex. Prog Neurobiol 74: 1–58.
11. Vezoli J, Falchier A, Jouve B, Knoblauch K, Young M, Kennedy H. 2004. Quantitative analysis of
connectivity in the visual cortex: extracting function from structure. Neuroscientist 10: 476–482.
1 Neuroanatomical Basis of Motivational and Cognitive Control:
A Focus on the Medial and Lateral Prefrontal Cortex

Jérôme Sallet, Rogier B. Mars, René Quilodran, Emmanuel Procyk,

Michael Petrides, and Matthew F. S. Rushworth

Understanding the neural mechanisms of control regulation requires delineating

specific functional roles for individual neural structures, and consequently their
functional relationships. Higher-order control over behavior has traditionally been
seen as the function of the prefrontal cortex (PFC). Models of various aspects of
control, including top-down processing, decision making, and performance monitor-
ing focus primarily on two subdivisions of the PFC, namely, the dorsolateral pre-
frontal cortex (DLPFC) and the medial frontal cortex, particularly the anterior
cingulate cortex (ACC). Within these frameworks, DLPFC is allocated a role in the
maintenance of representations of goals and means to achieve them in order to bias
processes that depend on posterior brain areas,58 while medial frontal areas, again
especially ACC, participate in performance monitoring, action evaluation and detec-
tion of events that indicate the need for behavioral adaptation and action revalua-
tion.75,76 Furthermore different hierarchical levels of cognitive control are thought
to be supported by different prefrontal subdivisions.4,46,47,68
One prominent example of framework of control is the conflict model proposed
by Cohen et al.15 This model posits that the ACC tracks evidence for a need to
increase cognitive control and sends this information to the DLPFC, which then
exerts control over the processes occurring in posterior brain areas. The ACC-
DLPFC interactions can be direct11 or indirect.15 A related model proposed by
Brown and Braver also posits that the activity of the ACC regulates the activity of
structures involved in implementing cognitive control.14 A rather different model,
based on the principles of reinforcement learning has been proposed by Holroyd
and Coles and ascribes to the ACC a role in action selection37,38 in response to a
dopaminergic teaching signal.38 For simplicity’s sake these models either supposed
the existence of a homogenous ACC and DLPFC, or else they are focused on some-
times undetermined subdivisions of these two regions. Furthermore, most models
have emphasized a unidirectional flow of information between the structures; in
some cases, however, the direction emphasized is from the ACC to the DLPFC,11,14,15
while in other cases it is from the DLPFC to the ACC.38
6 Jérôme Sallet and colleagues

A feature of these computational models is that they often do not consider all
aspects of the underlying neuroanatomy of these cortical regions. However, a more
detailed analysis of the connections between these brain areas may be of extreme
importance to the functionality of models. Indeed, as Passingham et al. suggest, each
cytoarchitectonic area has a unique connectivity pattern that is likely to be related
to its function.65 Thus, paying careful attention to the details of the anatomical
properties of networks may facilitate the identification of functional subdivisions
within each area, which may in turn generate a clearer understanding of integrated
system function. In this chapter, we review neuroanatomical data concerning two
key nodes in cognitive and motivational control models, the ACC and the DLPFC.
Our aim is to review neuroanatomical data related to these two regions in the hope
that it may help improve our understanding of control networks and how structures
within these networks are interacting. Furthermore, we discuss the degree of cor-
respondence in the anatomy of these areas in the human brain and the monkey
brain, a model on which much of our knowledge is based.

Cytoarchitecture of ACC and DLPFC

Though both terms are commonly used, neither ACC nor DLPFC corresponds to
a unique cortical area. They refer to a collection of areas (or subareas) with distinct
cytoarchitectonic properties and connectivity profiles.
The abbreviation ACC commonly refers to cytoarchitectonic areas 24 and 32
(figure 1.1a). Based on cytoarchitectural properties and quantification of neu-
rotransmitter receptors it has been proposed that the ACC in monkeys extends to
the middle of the dorsal bank of the cingulate sulcus,53,54,61,88 or lies just ventrally to
the bottom of the cingulate sulcus.12,20,87 Vogt et al. consider that most of the cortex
on the dorsal bank of the cingulate sulcus belongs to the adjacent medial frontal
cortex.87 Area 32 is located rostrally to area 24. Petrides and Pandya proposed that
the latter area extended caudally to form, on the dorsal bank of the cingulate sulcus,
a transition area between the ACC and the medial prefrontal cortex.68 Some dis-
agreement also exists over the nature of the cingulate cortex. While Petrides and
Pandya distinguished an agranular (area 24) and granular ACC (area 32), others
considered area 32 to be dysgranular, and argued that area 24,8 or at least the area
24c subdivision,20 was dysgranular. Similar discrepancies also exist concerning the
number of subdivisions of the ACC. Various studies find from four to nine subdivi-
sions54,87 in ACC area 24. Vogt et al. divide area 24 into an anterior division (the
ACC) and a posterior division, which they call the midcingulate cortex (MCC).87
The ACC then corresponds to areas 24a, b, and c; the MCC corresponds to subdivi-
sions 24a′, b′, c′, and d.
 Neuroanatomical Basis of Motivational and Cognitive Control 7

a) b)

Figure 1.1
Cartography of medial and lateral prefrontal cortex. (a) Cytoarchitecture maps of human (top) and
monkey (bottom) medial prefrontal cortex (adapted from Vogt et al.83,87 by permission of Oxford Uni-
versity Press). (b) Cytoarchitecture maps of human (top) and monkey (bottom) lateral prefrontal cortex
(adapted from Petrides and Pandya69). The dashed lines on the left and right figures correspond to the
boundaries of the ACC and DLPFC, respectively. VCA, vertical line through the anterior commissure.
8 Jérôme Sallet and colleagues

Although most of these debates have concerned the nature of ACC in the
macaque, similar debates concern the human ACC. The presence of an additional
sulcus known as the paracingulate sulcus, dorsal to the cingulate sulcus, further
complicates the problem.84 This sulcus is present in only 30 to 60% of cases29 and,
when present, shows highly variable morphology across individuals.84 The morphol-
ogy of the paracingulate sulcus affects the extent of areas 24 and 32 and is suggested
to be related to performance in demanding cognitive tasks.30 One hypothesis explain-
ing the interindividual differences in sulcal anatomy is that they reflects differences
in the connectivity between dorsal ACC and DLPFC.30 As in monkeys, several
subdivisions of the area 24 can be distinguished, and a similar organization has been
proposed63,86 (figure 1.1a).
The DLPFC is also a heterogenous region (figure 1.1b). In monkeys, it is located
within the principal sulcus and extends dorsally. Based on cytoarchitectonic proper-
ties, one can distinguish multiple areas: areas 8A and 8B, area 9, area 46. Some
authors proposed even further subdivisions, including transition areas around the
lip of the principal sulcus and subdivisions based on the position in the principal
sulcus. Those areas are labeled area 9/46 dorsal and ventral,68,69 and a distinction
is often made between area 46 ventral and dorsal.3,7 Finally, area 8 is subdivided
into area 8A, located at the level of the genu of the arcuate sulcus, and area 8B
dorsal to it.
As is immediately apparent, the human lateral prefrontal cortex is more
folded than that of the monkey (figure 1.1b). Instead of one sulcus (the principal
sulcus), there are three: the superior frontal sulcus, the complex intermediate
frontal sulcus, and the inferior frontal sulcus.70 The inferior frontal sulcus is
suggested to be the ventral boundary of the DLPFC. Despite this discrepancy
between humans and monkeys, Petrides and Pandya proposed similar organization
of the DLPFC.69

Connectivity of ACC and DLPFC

Mediolateral Prefrontal Cortex Connectivity in Monkeys

Before discussing DLPFC-ACC connectivity, it is important to underline the fact

that it is difficult to perfectly describe the relationships between cingulate cytoar-
chitectonic areas and connectivity patterns. Indeed, in the literature most of the
tracers injected in the cingulate cortex targeted either the cingulate gyrus (area 24a,
b) or the rostral/caudal cingulate motor areas (rCMA, cCMA). rCMA and cCMA
are cingulate subregions defined by their projections to the primary motor area
(M1), the spinal cord, and their excitability.51,59,73 In the interest of clarity, we con-
sider the portion of area 24 that includes all the cingulate motor areas as the pos-
Neuroanatomical Basis of Motivational and Cognitive Control 9

terior ACC (pACC). Area 24 rostral to pACC is referred to as the rostral ACC
(rACC). Connectivity of area 32 is considered separately.
A number of models of control emphasize interactions between ACC and
DLPFC.11,14 Surprisingly, the emphasis on the ACC-DLPFC functional relationships
in fact relies on relatively weak anatomical connections (figure 1.2). For instance,
pACC receives roughly 20 to 40 times more projections from the preSMA and
cCMA than from area 46,36 and area 46 projects more to medial prefrontal areas
(areas 8B, 9) than to rCMA.80 Note that the rACC also receives projections from
the DLPFC,7,72 and the ACC projects back to the DLPFC. Despite a lack of fully
quantitative data, the anterior part of area 24 (and area 32) seems to project more
to the principal sulcus than its caudal part.50
This last result suggests that the connectivity patterns between the ACC and
the DLPFC differ between cytoarchitectonic areas. Labeled cells often form
clusters and are not evenly distributed across the entire area. Note that the clus-
tering organization of connections may reflect a modular organization of the pre-
frontal cortex.49 For instance, area 8B but not area 8A projects to the rACC.64,71
However, area 8A is interconnected with pACC and receives afferents from
rACC.1,39,89 The efferents from area 8A to pACC are limited to two separate
clusters—one just anterior to rCMA and one adjacent to the ventral cCMA—that
are then defined as cingulate eye field rostral and caudal, respectively.89 Note that
no projection in the cingulate sulcus was found after an injection of isotope spe-
cifically in the ventral subdivision of area 8A.71 Areas 8A and 8B also present
different connectivity patterns with other areas of the DLPFC. They are connected
to each other as well as to areas 10, 9, and 9/46d; however, only the rostral part
of area 8A is connected with area 46d, whereas area 8B is connected with
area 46v.64,71
ACC receives projections from areas 10, 9, 46, and 9/46d.6,7,42,59,60,71,72,85 But even
within one cytoarchitectonic territory, the projections are not even. For instance, the
connectivity of the ACC with the medial part of areas 9 and 8B is stronger than that
with their lateral parts. Indeed, while area 8B and medial area 9 project to both the
sulcal and gyral part of the rostral ACC, the lateral part of area 9 only projects to
the rostral cingulate sulcus.6,60,71 The dorsal part of area 46 receives projection from
area 32, rACC and pACC, but only the ventral part of area 46 receives afferent
inputs, from pACC.1,7 The projections from area 10 to the ACC principally target
the cingulate gyrus and are reported to be organized in columnar manner.72 Area
10 projections to the cingulate sulcus area are restricted to its more rostral part.72
Note that only the rACC and area 32 project back to area 10; no projection from
pACC to the frontopolar cortex has been reported.1,6,85 Finally, rACC (at the depth
of the cingulate sulcus) and pACC (only the more ventral subdivision) project to
9/46v66; only pACC receives inputs from area 9/46v.77
a)

b)

c)

Figure 1.2
Connectivity of medial and lateral prefrontal cortex. (a,b) Lateral (a) and medial (b) view of macaque
prefrontal areas. Clustering of prefrontal areas based on their connectivity patterns (adapted from Aver-
beck and Seo3). (c) Profile of inputs characterizing the five clusters illustrated in (b). The y-axis corre-
sponds to the proportion of the connections. The top row represents the prefrontal interconnections; the
bottow row corresponds to connections with extraprefrontal systems (adapted from Averbeck and Seo3).
Note that DMPFC-DLPFC interconnections represent only between 20 and 30% of their prefrontal
connections; connections that are themselves a subset of the total connections of these clusters.
Neuroanatomical Basis of Motivational and Cognitive Control 11

This overview of the mediolateral prefrontal connectivity shows the expected

interconnectivity between the different areas but also highlights the complexity of
the connection patterns. Consistent with this, a meta-analysis of prefrontal cortex
connectivity based on the COCOMAC database (<http://cocomac.org>) reveals
that the ACC and DLPFC do not simply correspond to two different entities3 (figure
1.2). Instead, a cluster analysis suggested that one can consider the medial part of
area 9, the cingulate sulcus (24c), and part of the cingulate gyrus (area 24b) as a
dorsomedial prefrontal cortex whereas areas 24a and 32 form part of a ventromedial
prefrontal cortex. On the lateral surface areas 8A, 46d, and the lateral part of area
9 form the dorsolateral cluster.

Microarchitecture of Mediolateral Prefrontal Cortex Connectivity

Not merely the presence of connections, but also their laminar distribution pattern
is important. Indeed, it may reflect some key functional properties of the
network.9,16,25,82 A simplified approach is to consider terminations that principally
target layer IV as driving or feedforward projections. Terminations that principally
target supragranular (layers I to III) or infragranular (layers V and VI) layers are
considered as modulating or feedback projections, respectively. A similar logic could
be applied depending on the localization of the cell bodies of efferent projections.
If the majority of the cell bodies are found in the supragranular layers or in the
infragranular layers, the projections are feedforward or feedback, respectively.
This hierarchical organization originally proposed for the visual system has been
proposed for the prefrontal cortex as well.19
As is the case for the presence of the projections, their laminar patterns are also
heterogenous. The afferents to rACC (areas 24a, b) from area 9 are distributed
throughout the different cortical layers.1 But rACC afferents from the principal
sulcus are denser in supragranular layers than in the infragranular layers.1,85 The
same pattern is observed in pACC.50,85 However, rACC efferences to both areas 46
and 9 are distributed over all cortical layers with a lower density in area IV.1 Note
that cingulate (area 32) projections to DLPFC originate mainly in the deep layers,
layer V and VI.5
A quantitative analysis of connectivity analogous to that applied in interpreting
the neuroanatomy of the visual system9,82 might potentially be applied to the study
of the prefrontal cortex. Nevertheless, the data available concerning ACC-DLPFC
connectivity suggest that ACC may modulate DLPFC activity (feedback projec-
tions), while the DLPFC may drive ACC activity (feedforward projections). One
can go a step further and try to understand how these two structures are interacting
at a synaptic level.
At a more microscopic level, the literature is principally concerned with the
intrinsic connectivity, that is, the intra-areal connectivity, of the DLPFC or the ACC
12 Jérôme Sallet and colleagues

each in isolation.21,22,32,33,61,74 In recent experiments, Medalla and Barbas addressed

the issue of the mediolateral prefrontal connectivity at a synaptic level.56,57 In a first
experiment they injected tracers in areas 32 and 46 and examined the labeled axon
terminals in layers I through III of area 9.56 Both areas predominantly formed single
synapses on the spines of spiny dendrites of excitatory cells. However, area 32 had
more synapses with inhibitory neurons in area 9 than area 46 had, and the nature
of inhibitory neurons receiving afferents from those two pathways was also differ-
ent. Although the majority of synaptic boutons were small, those from area 32 were
bigger than those from area 46, suggesting the synapses had a higher efficacy. The
interneurons receiving projections from area 32 are thought to be involved in the
enhancement of the signal-to-noise ratio (calbindin-positive cells, or CB cells), or
in the enhancement of signals (calretinin-positive cells, or CR cells) in highly
demanding cognitive situations. In their subsequent experiment Medalla and Barbas
also investigated area 32 connectivity with area 10.57 Area 32 is also connected with
area 10; however, some features of the pathway were distinct from the one that links
area 32 and area 46. For instance, area 32 projections largely target the area 10
excitatory cells. This suggests that, instead of enhancing inhibition, area 32 enhances
excitatory activities in area 10. These results highlight the importance not only
of inferring the existence of connections, but also of understanding the nature of
these connections.

Mediolateral Prefrontal Cortex Connectivity in Humans

Our knowledge of connectivity patterns comes principally from studies on animal

models. The recent development of the diffusion tensor imaging (DTI) method
enables investigation of connectivity in the human brain.43 There is a strong similar-
ity between the results obtained with classic labeling (injection of tracers) and those
obtained with DTI.17,78 Apart from methods assessing structural connections, func-
tional connectivity and effective connectivity, as assessed using functional magnetic
resonance imaging (fMRI), provide another route to information about the con-
nectivity of the human brain. Functional connectivity is thought to reflect temporal
correlations between areas; effective connectivity refers to the influence of one
neural system over another.79 Although these can be modulated by polysynaptic
connections, patterns of effective and functional connectivity have often been
related to direct anatomical connections.28
A recent DTI study in humans confirmed the heterogeneity of the cingulate
cortex (figure 1.3a). The study reported that the ACC could be divided into different
regions on the basis of their probability of interconnection with the rest of the
brain.10 One cluster corresponded to the supracallosal part of the cingulate gyrus
(cluster 7), and one is likely to include area 32 (cluster 2). Three other clusters
correspond to different regions of the cingulate sulcus and paracingulate sulcus.
Neuroanatomical Basis of Motivational and Cognitive Control 13

The caudal clusters have been suggested to be the cingulate motor areas (clusters
4 and 5).
Studies of cingulate functional connectivity at rest revealed that ACC activity
is correlated with DLPFC activity, but again emphasized that parts of the ACC
are differently correlated with the DLPFC.34,52 The most striking result of a recent
study by Margulies et al.52 is the difference between ventral and dorsal cingulate
regions (figure 1.3b). Unfortunately, it is difficult to infer from the results presented
in their study with which different DLPFC regions ACC activity correlates. Nev-
ertheless the caudal ACC (x = 5, y = 14, z = 42, MNI space) did not correlate
with the frontopolar cortex whereas the more anterior ACC did. Two patterns of
functional connectivity with the DLPFC could be observed for anterior regions
at coordinates [5 25 36], [5 34 28], and regions at coordinates [5 42 21], [5 47 11].
The two most anterior regions are unlikely to contain the cingulate motor areas
and showed less correlation with the middle frontal gyrus. Note that the cCMA
also showed less correlation with the DLPFC than rCMA. Furthermore, the
DLPFC region showing correlation with cCMA activity was more posterior
[-30 37 32] than the one [-28 44 32] for which correlation was observed with
rCMA activity.34
Not only at rest, but also during the performance of a variety of tasks are the
ACC and DLPFC coactivated. Paus and Koski’s meta-analysis of positron emission
tomography (PET) studies revealed that supracallosal cingulate cortex activations,
more precisely area 24c and 32, were very often associated with activation in the
middle frontal cortex.47 In addition, they distinguished within this supracallosal
activity a caudal cingulate region (y < 10) in which activations co-occurred more
frequently with activations in the precentral gyrus and the medial frontal gyrus than
was the case for the more rostral cingulate region (y > 10) did.
For modeling purposes, one is probably more interested in effective connectivity
than in structural connectivity. Not only coactivation but also interactions have
been reported between rCMA and the middle frontal gyrus, peaking at (44, 30, 24),
while subjects were performing a flanker task.24 According to Kouneiher et al.,48
interaction between these two regions is related to motivational control, rather than
cognitive control. Caudal paracingulate activity predicting behavioral adaptation
did not interact with the middle frontal gyrus activity associated with behavioral
adjustements.40,44,45
In summary, resting state functional connectivity confirmed the existence of net-
works linking the ACC to the DLPFC in the human brain. It also confirmed the fact
that different regions of the ACC are communicating with different regions of the
DLPFC (see figure 1.3b). Task-related activity in fMRI and PET functional studies
suggested that a network centered on rCMA and middle frontal gyrus (areas 46 and
9/46) is of particular interest.
a) CMAc, CMAr

Cluster 6 Cluster 5 Cluster 4

Cluster 9

Cluster 3

Cluster 2

Cluster 1

Cluster 7
b) Cluster 8

s3 i3

s4 i6

s5

Superior
Inferior

s6

s7 p < 0.05, corrected

Neuroanatomical Basis of Motivational and Cognitive Control 15

Beyond the ACC or the DLPFC

This chapter principally focused on the ACC and the DLPFC; however, we are
aware that motivational and cognitive control processes do not simply rely on these
two regions. For instance, noradrenergic (NA) and dopaminergic (DA) systems both
play a critical role in cognitive control2,15,38 (see chapter 3, this volume).
The locus coeruleus and its two modes of response (tonic and phasic) are pro-
posed to induce alternation between explorative and exploitative behaviors. This
structure projects to the entire neocortex and receives projections back from the
rACC and adjacent medial prefrontal areas, but not the lateral prefrontal areas.2
The interactions between ACC, DLPFC, and the DA system are quite complex. The
DA has direct (mesocortical pathway) and indirect influences on the ACC and
DLPFC via the striatum (nigrostriatal pathway) or the thalamus (nigrothalamocor-
tical pathway).35,41,90,91
The conflict-monitoring model developed by Cohen et al. focuses on the effect
of DA on the DLPFC, while the model developed by Holroyd and Coles is centered
on DA inputs to the ACC.15,38 Nevertheless, both of them implied the involvement
of the direct mesocortical pathway. Though both ACC and DLPFC receive direct
DA afferents, there is a regional difference in the origin of the inputs.91 Similarly,
ACC and DLPFC send sparse projections to the midbrain DA nuclei with a similar
spatial organization.31 The DLPFC receives more afferents from more lateral DA
midbrain nuclei, the distribution of ACC afferents originates more in the medial
midbrain nuclei. The topographic segregation of DLPFC and ACC projections is
more obvious in the caudal part of the midbrain nuclei while they tend to overlap
more anteriorly.
This anatomical compartmentalization could reflect a functional compartmental-
ization. Indeed, in a recent study, Brischoux et al. found some functional differences
between dorsal and ventral VTA in rats13 and along a dorsoventral axis in monkeys
DA midbrain nuclei.55 Some DA cells discharge preferentially for positive outcome
related events,13,27,55,80 but some DA cells discharge also, or preferentially for nega-
tive events.13,55 Earlier studies also reported functional heterogeneity in VTA/SN

Figure 1.3
Connectivity-based parcellation and functional connectivity at rest of the human cingulate cortex. (a)
Connectivity-based parcellation of human ACC (adapted from Beckmann et al.10). The ACC(/MCC)
corresponds to clusters 2, 3, 4, 5 and part of cluster 7. (b) Functional connectivity at rest of cingulate
regions (adapted from Margulies et al.52). Positive correlations (p < 0.05, corrected) of different cingulate
regions, or seeds (represented on the medial view) are shown in black on cortical surface maps for
superior (s3, s4, s5, s6, s7) and inferior seeds (i3, i6). Inferior seeds are located 5 mm from the corpus
callosum, starting at y = −10 mm, and spaced 10 mm apart along the curve parallel to the corpus callosum.
Superior seeds are located 15 mm from the corpus callosum along the radial axis from each of the first
seven inferior seeds.
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