Schizophrenia The Final Frontier A Festschrift for Robin M.
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The Maudsley Series
HENRY MAUDSLEY, from whom the series of monographs takes its name, was
the founder of The Maudsley Hospital and the most prominent English psychiatrist
of his generation. The Maudsley Hospital was united with the Bethlem Royal
Hospital in 1948 and its medical school, renamed the Institute of Psychiatry at the
same time, became a constituent part of the British Postgraduate Medical
Federation. It is now a school of King’s College, London, and entrusted with the
duty of advancing psychiatry by teaching and research. The South London &
Maudsley NHS Trust, together with the Institute of Psychiatry, are jointly known
as The Maudsley.
The monograph series reports high quality empirical work on a single topic of
relevance to mental health, carried out at the Maudsley. This can be by single or
multiple authors. Some of the monographs are directly concerned with clinical
problems; others, are in scientific fields of direct or indirect relevance to mental
health and that are cultivated for the furtherance of psychiatry.
Editor
Professor A. S. David MPhil MSc FRCP MRCPsych MD
Assistant Editor
Professor T. Wykes BSc PhD MPhil
Previous Editors
1955–1962 Professor Sir Aubrey Lewis LLD DSc MD FRCP and
Professor G. W. Harris MA MD DSc FRS
1962–1966 Professor Sir Aubrey Lewis LLD DSc MD FRCP
1966–1970 Professor Sir Denis Hill MB FRCP FRCPsych DPM and
Professor J. T. Eayrs PhD DSc
1970–1979 Professor Sir Denis Hill MB FRCP FRCPsych DPM and
Professor G. S. Brindley
1979–1981 Professor G. S. Brindley MD FRCP FRS and Professor G. F.
M. Russell MD FRCP FRC(ED) FRCPsych
1981–1983 Professor G. F. M. Russell MD FRCP FRCP(ED) FRCPsych
1983–1989 Professor G. F. M. Russell MD FRCP FRCP(ED) FRCPsych
and Professor E. Marley MA MD DSc FRCP FRCPsych DPM
1989–1993 Professor G. F. M. Russell MD FRCP FRCP(ED) FRCPsych
and Professor B. H. Anderton BSc PhD
1993–1999 Professor Sir David Goldberg MA DM MSc FRCP FRCPsych
DPM
The Maudsley Series
Schizophrenia
The Final Frontier — A Festschrift for
Robin M. Murray
Edited by Anthony S. David,
Shitij Kapur and Peter McGuffin
First published 2011
by Psychology Press
27 Church Road, Hove, East Sussex BN3 2FA
Simultaneously published in the USA and Canada
by Routledge
711 Third Avenue, New York, NY 10017
Psychology Press is an imprint of the Taylor & Francis Group,
an Informa Business
Copyright © 2011 Psychology Press
All rights reserved. No part of this book may be reprinted or reproduced
or utilised in any form or by any electronic, mechanical, or other means,
now known or hereafter invented, including photocopying and recording,
or in any information storage or retrieval system, without permission in
writing from the publishers.
British Library Cataloguing in Publication Data
A catalogue record for this book is available from the British Library
Library of Congress Cataloguing-in-Publication Data
Schizophrenia : the final frontier : a festschrift for
Robin M. Murray / edited by Anthony S. David,
Shitij Kapur, and Peter McGuffin.
p. ; cm. -- (Maudsley series)
Includes bibliographical references and index.
ISBN 978-1-84872-077-0 (hbk)
1. Schizophrenia. I. David, Anthony S., editor. II. Kapur, Shitij, editor.
III. McGuffin, Peter, editor. IV. Murray, Robin M., 1944- , honoree.
V. Series: Maudsley series.
[DNLM: 1. Murray, Robin M., 1944- 2. Schizophrenia—Festschrift. WM 203]
RC514.S336445 2011
616.89’8–dc22 2010044157
ISBN: 978-1-84872-077-0 (hbk)
ISBN: 978-0-203-80877-1 (ebk)
Typeset in Times New Roman by RefineCatch Limited, Bungay, Suffolk
Printed and bound in Great Britain by TJ International Ltd, Padstow, Cornwall
Contents
List of plates ix
List of figures x
List of tables xii
List of contributors xiii
Foreword by Daniel R. Weinberger xvii
Preface xxi
Acknowledgements xxiii
PART I
Development 1
1 The neurodevelopmental hypothesis of schizophrenia 3
K A T H E R I N E H . KARL S GODT , L AURE N M. E L L MAN ,
D A Q I A N G S U N , VI JAY MI T T AL AND T YRONE D. CA N N O N
2 Is earlier intervention for schizophrenia possible?
Identifying antecedents of schizophrenia in children
aged 9–12 years 19
K R I S T I N R . L A U RE NS , S HE I L AGH HODGI NS , E RI C A .
T A Y L O R A N D ROBI N M. MURRAY
3 The black hole of the adolescent brain 33
M A T T A L L I N A ND CHI ARA NOS ART I
4 The contribution of Nordic population registers to the
search for the causes of schizophrenia and other psychiatric
disorders 45
P E T E R B . J O N E S , MAT T I I S OHANNI , JAANA S UVI SA A R I,
J A R I H A U K K A A ND JOUKO MI E T T UNE N
PART II
Neuroscience 69
5 The search for madness: A metaphasical trip
through the basal ganglia 71
P A U L D . M O R R I S ON
vi Contents
6 Neurophysiological endophenotypes for psychosis 87
M A D I H A S HAI KH AND E L VI RA BRAMON
7 Glutamate and GABA transmitter systems: Post-mortem
studies and the neuropathology of amino acids in
schizophrenia 103
P A U L J . H A RRI S ON
8 Animal models of schizophrenia revisited 115
T R E V O R W . ROBBI NS
PART III
Neuroimaging 129
9 Application of neuroimaging to the study of psychosis 131
P H I L I P M C GUI RE
10 Brain networks and schizophrenia 139
E D B U L L M O RE
11 Neuroimaging and psychosis: Are brain changes in
individuals with psychosis neurodevelopmental for some
and progressive for others? 147
P A O L A D A ZZ AN, KE VI N MORGAN, JUL I A L A PPIN A N D PA U L FEA R O N
12 Gray matter alterations in schizophrenia:
Are they reversible? 155
M A T C H E R I S . KE S HAVAN AND T E JAS BHOJR A J
PART IV
Genetics 177
13 A short (and partial) history of genetics at the Institute
of Psychiatry 179
P E T E R M C GUF F I N
14 From first contact to the final frontier: A star trek along
the DISC1 pathway to schizophrenia 193
D A V I D P O R T E OUS
15 Dopamine gene variants and schizophrenia:
A scheme for investigating nominally significant
or discrepant associations 205
V I S H W A J I T L . NI MGAONKAR, KODAVAL I V. CH O WD A R I,
K O N A S A L E M. P RAS AD, ANNI E M. WAT S ON, H A D ER MA N SO U R,
J O E L A . W OOD AND A. JAVI E R L OP E Z
16 Ebb and flow in biological psychiatry 219
TIM J. CROW
Contents vii
PART V
Cognition 233
17 Cognitive models of psychosis, the jumping to conclusions
reasoning bias and improving psychological treatment for
delusions 235
P H I L I P P A G A RE T Y, DANI E L F RE E MAN, S UZ ANNE JO LLEY ,
KERRY ROSS, HELEN WALLER AND GRAHAM DUNN
18 Giftedness and psychosis 247
J A M E S H . M A CCABE
PART VI
Social psychiatry 257
19 Towards a social aetiology of psychosis:
The case of child sexual abuse 259
P A U L B E B B I N G T ON
20 Does urban density matter? 273
J A N E B O Y D E L L AND JUDI T H AL L ARDYCE
21 Does higher potency cannabis mean
higher risk for psychosis? 281
M A R T A D I F O RT I , AL E S S ANDRA P AP ARE L L I
A N D P A O L A CAS ADI O
22 The social determinants of psychosis
in migrant and minority ethnic populations 289
C R A I G M O R G A N, GE RARD HUT CHI NS ON, P AOL A D A ZZA N , K EV IN
M O R G A N A N D P AUL F E ARON
23 Stress and psychosis: Professor Murray’s
contribution (so far) to the vulnerability–stress model 303
V A L E R I A M O N DE L L I AND CARMI NE M. P ARI ANTE
24 Chasing gene–environment interactions
across the psychiatric universe 313
J I M V A N O S , B ART P . F . RUT T E N, RUUD VAN WIN K EL A N D
M A R I E K E W I CHE RS
PART VII
Treatment 325
25 How antipsychotics work:
Examining trans-synaptic realities 327
S R I D H A R N A TE S AN AND S HI T I J KAP UR
26 Metabolic disturbance and schizophrenia 343
E M M A N I C H O LS ON AND DAVI D J. CAS T L E
viii Contents
27 Clinical trials and schizophrenia 357
SHÔN LEWIS
28 What new evidence tells us about dopamine’s
role in schizophrenia 365
O L I V E R D . HOWE S
PART VIII
Afterword 373
29 Robin M. Murray: A biographical note 375
A N T H O N Y S. DAVI D
30 Robin M. Murray: Top 12 publications 381
A N T H O N Y S. DAVI D AND ROBI N M. MURRAY
Index 385
Plates
Colour section between pages 32 and 38
3.1 Decreased and increased grey matter and white matter volume in VPT
adolescents compared to controls
3.2 Increased and decreased regional brain activation in preterm-born young
adults compared to controls
9.1 Acute induction of psychotic symptoms by tetrahydrocannabidiol
9.2 Altered hippocampal function in subjects with prodromal signs of psychosis
9.3 Neurochemical dysfunction in subjects with prodromal signs of psychosis
9.4 Correlation between subcortical dopamine dysfunction and altered cortical
activation in subjects with prodromal symptoms of psychosis
9.5 Brain areas in subjects with prodromal symptoms where grey matter
volume was related to thalamic glutamate levels
10.1 Disease-related disorganization of brain anatomical networks derived from
structural MRI data
10.2 Developmental antecedents of adult human brain structure
11.1 Brain changes in subjects on (A) typical and (B) atypical antipsychotics
versus drug-free subjects
Figures
1.1 Developmental model of schizophrenia 4
5.1 Bidirectional plasticity at cortical inputs to the striatum 76
5.2 The role of CB1 receptors at GABA-ergic synapses in
the striatum 77
5.3 Opposition of the D2→CB1 axis and adenosine receptors 80
7.1 A simplified and speculative schematic of glutamate and
GABA involvement in the pathogenesis and neuropathology
of schizophrenia 104
8.1 The aetiology of schizophrenia 123
12.1 A schematic representation of putative causes of neuropil
reduction in schizophrenia acting at different points
throughout the lifetime 162
15.1 Recursive functional analysis (RFA) 210
15.2 Progress with dopamine gene-association studies using RFA 211
17.1 A cognitive model of the positive symptoms of psychosis 236
17.2 Reasoning processes in delusional conviction 240
18.1 Rates of psychosis, by grade point average 253
19.1 Percentage of responding psychiatrists rating each factor
as relevant to the aetiology of depression or schizophrenia 260
19.2 Frequency of CSA in the English national population 263
19.3 CSA involving intercourse 265
22.1 Adjusted odds ratios for each level of social disadvantage
and isolation, current and long term 295
22.2 Rate ratios for schizophrenia by ethnic density in recent studies 297
Figures xi
23.1 Schematic diagram of the hypothalamic–pituitary–adrenal
(HPA) axis 305
23.2 The pituitary gland visualized using MRI 306
24.1 Gene–environment interaction 314
24.2 Gene–environment correlation 314
24.3 Development of experimental G×E approaches 319
24.4 The different levels and axes of gene–environment
interactions in psychiatry 320
25.1 Trans-synaptic abnormalities in schizophrenia linked to
dopamine transmission 330
26.1 St Vincent’s Mental Health metabolic monitoring form 346
28.1 Showing a direct relationship between prodromal symptom
severity and striatal dopamine availability in people with
prodromal signs of schizophrenia 367
28.2 Showing how risk factors for schizophrenia may all converge
to cause dopamine dysregulation and hence psychosis 368
29.1 Robin Murray in primary school uniform 376
29.2 Robin Murray graduation photo Glasgow University 377
Tables
2.1 The percentages of children (total sample, boys, and girls)
who present each putative antecedent of schizophrenia 23
2.2 The percentages of children displaying antecedents within
each domain of the antecedent triad and the percentages of
children with each antecedent who reported impact from
psychotic-like experiences 25
2.3 The prevalence of the antecedent triad and each
antecedent domain comprising the triad within each
ethnic group 27
4.1 Inception date for various nationwide health-care registers
in Nordic countries 46
8.1 MATRICS 116
8.2 Models of schizophrenia 120
16.1 Ebb (“pink spots” or hopeful theories) and flow
(“red herrings” or discarded theories) in biological psychiatry 220
21.1 Longitudinal studies in the general population: Strength
of the association between cannabis use and onset of
later schizophrenia spectrum disorders 283
21.2 Differences in pattern of use and potency of cannabis
chosen between cases and controls, in a first-episode
psychosis study from southeast London 286
22.1 Basic characteristics of the AESOP sample 291
22.2 Incidence rates and rate ratios by ethnic group in the
AESOP study 292
27.1 The hierarchy of assessing effectiveness 357
27.2 The pros and cons of randomized controlled trials 358
Contributors
Judith Allardyce, Department of Psychosis Studies, Institute of Psychiatry,
King’s College London, London, UK
Matt Allin, Institute of Psychiatry, King’s College London, London, UK
Paul Bebbington, Department of Mental Health Sciences, University College
London, London, UK
Tejas Bhojraj, Harvard Medical School, Boston, MA, USA
Jane Boydell, Department of Psychosis Studies, Institute of Psychiatry, King’s
College London, London, UK
Elvira Bramon, Department of Psychosis Studies, Institute of Psychiatry, King’s
College London, London, UK
Ed Bullmore, Department of Psychiatry, University of Cambridge, Cambridge,
UK
Tyrone D. Cannon, Departments of Psychology & Psychiatry & Behavioural
Sciences, University of California, Los Angeles, CA, USA
Paola Casadio, Department of Psychosis Studies, Institute of Psychiatry, King’s
College London, London, UK
David J. Castle, University of Melbourne, Melbourne, Australia
Kodavali V. Chowdari, Department of Psychiatry, University of Pittsburgh
School of Medicine, Pittsburgh, PA, USA
Tim J. Crow, SANE Prince of Wales International Centre, Warneford Hospital,
Oxford, UK
Anthony S. David, Section of Cognitive Neuropsychiatry, Institute of Psychiatry,
King’s College London, London, UK
Paola Dazzan, NIH Biomedical Research Centre, Institute of Psychiatry, King’s
College London, London, UK
xiv Contributors
Marta Di Forti, Department of Psychosis Studies, Institute of Psychiatry, King’s
College London, London, UK
Graham Dunn, Community Based Medicine, Manchester University,
Manchester, UK
Lauren M. Ellman, Departments of Psychology & Psychiatry & Behavioural
Sciences, University of California, Los Angeles, CA, USA
Paul Fearon, St Patrick’s University Hospital and Trinity College Dublin,
Dublin, Ireland
Daniel Freeman, Department of Psychology, Institute of Psychiatry, King’s
College London, London, UK
Philippa Garety, Department of Psychosis Studies, Institute of Psychiatry,
King’s College London, London, UK
Paul J. Harrison, Department of Psychiatry, University of Oxford, Oxford, UK
Jari Haukka, Department of Mental Health and Substance Abuse Services,
National Institute for Health and Welfare, Helsinki, Finland
Sheilagh Hodgins, Department of Forensic Mental Health Science, Institute of
Psychiatry, King’s College London, London, UK
Oliver D. Howes, Department of Psychosis Studies, Institute of Psychiatry,
King’s College London, London, UK
Gerard Hutchinson, Psychiatry Unit, University of the West Indies, Trinidad
Matti Isohanni, Department of Psychiatry, University of Oulu, Oulu, Finland
Suzanne Jolley, Department of Psychology, Institute of Psychiatry, King’s
College London, London, UK
Peter B. Jones, Department of Psychological Medicine, University of Cambridge,
Cambridge, UK
Shitij Kapur, Department of Psychological Medicine & Psychiatry, Institute of
Psychiatry, King’s College, London, UK
Katherine H. Karlsgodt, Departments of Psychology & Psychiatry & Behavioural
Sciences, University of California, Los Angeles, CA, USA
Matcheri S. Keshavan, Harvard Medical School Department of Psychiatry,
Boston, MA, USA
Julia Lappin, Department of Psychosis Studies, Institute of Psychiatry, King’s
College London, London, UK
Kristin R. Laurens, Department of Forensic Mental Health Science, Institute of
Psychiatry, King’s College London, London, UK
Contributors xv
Shôn Lewis, Department of Adult Psychiatry, University of Manchester,
Manchester, UK
A. Javier Lopez, Department of Biological Sciences, Carnegie Mellon University,
Pittsburgh, PA, USA
James H. MacCabe, Department of Psychosis Studies, Institute of Psychiatry,
King’s College London, London, UK
Hader Mansour, Department of Psychiatry, University of Pittsburgh School of
Medicine, Pittsburgh, PA, USA
Peter McGuffin, MRC Social, Genetic & Developmental Psychiatry Centre,
Institute of Psychiatry, King’s College London, London, UK
Philip McGuire, Department of Psychosis Studies, Institute of Psychiatry, King’s
College London, London, UK
Jouko Miettunen, Department of Psychiatry, University of Oulu, Oulu, Finland
Vijay Mittal, Departments of Psychology & Psychiatry & Behavioural Sciences,
University of California, Los Angeles, CA, USA
Valeria Mondelli, Section of Perinatal Psychiatry & Stress, Psychiatry and
Immunology, Institute of Psychiatry, King’s College London, London, UK
Craig Morgan, NIH Biomedical Research Centre, Institute of Psychiatry, King’s
College London, London, UK
Kevin Morgan, Department of Psychology, Westminster University, London,
UK
Paul D. Morrison, Department of Psychosis Studies, Institute of Psychiatry,
King’s College London, London, UK
Robin M. Murray, Department of Psychosis Studies, Institute of Psychiatry,
King’s College London, London, UK
Sridhar Natesan, Department of Psychological Medicine & Psychiatry, Institute
of Psychiatry, King’s College, London, UK
Emma Nicholson, University of Melbourne, Melbourne, Australia
Vishwajit L. Nimgaonkar, Department of Psychiatry, University of Pittsburg
School of Medicine, Pittsburg, PA, USA
Chiara Nosarti, Department of Psychosis Studies, Institute of Psychiatry, King’s
College London, London, UK
Alessandra Paparelli, Department of Psychosis Studies, Institute of Psychiatry,
King’s College London, London, UK
Carmine M. Pariante, Section of Perinatal Psychiatry & Stress, Psychiatry and
Immunology, Institute of Psychiatry, King’s College London, London, UK
