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Brain Circuits, Modularity, and Childhood Syndromes

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Brain Circuits, Modularity, and Childhood Syndromes Brain Circuits, Modularity, and Childhood Syndromes Florence Levy A thesis submitted in fulfillment of the requirements for the degree of Doctor of Philosophy. University of New South Wales May 2010 COPYRIGHT, AUTHENTICITY, and ORIGINALITY STATEMENT I hereby grant the University of New South Wales or its agents the right to archive and to make available my thesis or dissertation in whole or part in the University libraries in all forms of media, now or here after known, subject to the provisions of the Copyright Act 1968. I retain all proprietary rights, such as patent rights. I also retain the right to use in future works (such as articles or books) all or part of this thesis or dissertation. I also authorise University Microfilms to use the 350 word abstract of my thesis in Dissertation Abstract International. I have either used no substantial portions of copyright material in my thesis or I have obtained permission to use copyright material; where permission has not been granted I have applied/will apply for a partial restric- tion of the digital copy of my thesis or dissertation, and I certify that the Library deposit digital copy is a direct equivalent of the final officially approved version of my thesis. No emendation of content has occurred and if there are any minor variations in formatting, they are the result of the conversion to digital format, and I hereby declare that this submission is my own work and to the best of my knowledge it contains no materials previously published or written by another person, or substantial proportions of material which have been accepted for the award of any other degree or diploma at UNSW or any other educational institution, except where due acknowledgment is made in the thesis. Any con- tribution made to the research by others, with whom I have worked at UNSW or elsewhere, is explicitly acknowledged in the thesis. I also declare that the intellectual content of this thesis is the product of my own work, except to the extent that assistance from others in the project’s design and conception or in style, presentation and linguistic expression is acknowledged. Signed ................................... Date ............................... iii Abstract The thesis explores the contribution of connectionist, cognitive and bio- logical models to a better understanding of childhood psychopathology at a time when rapid advances in brain mapping techniques are con- tributing to a ‘brain circuit’ understanding of child development and behaviour. The prototypic structure of all brain circuits is described as originating in the frontal lobes, projecting to striatal structures, thala- mic nuclei, and a final link back to the frontal lobes. The thesis postulates that early childhood behaviour is char- acterised by modular stimulus-bound behaviours, which utilize feed-forward responses. Development requires the establishment of feedback-controlled circuits. Failure of integration of higher-order cog- nition with subcortical gating functions, gives rise to a number of child- hood syndromes, discussed in the second part of the thesis. The initial chapters of the thesis examine neural network, and mechanistic cogni- tive models, evolution of language, and mirror systems, including analo- gies with birdsong development. In humans, integration of emotion with cognitive circuits is thought to occur at ventral striatal/basal ganglia levels. Higher-order functions are thought to require optimal arousal levels, maintained by complex integration of subcortical responsivity with cortical outputs. Working memory is believed central to control of higher order cognition, but like emotional and motor regulation, sub- cortical structures including the basal ganglia are crucial for sequenc- ing and ordering behaviour, controlled at prefrontal levels. Here lan- guage plays a role in allowing the abstraction of ‘chunks’ held in work- ing memory. Circuits involved in emotional regulation, as well as social cognition in terms of analogue mirror vs executive functions are inves- tigated. Chapters 6 to 12 discuss the development and malfunction of circuits involved in Attention Deficit Hyperactivity Disorder, Conduct Disorder, Autism/Aspergers Disorder, Obsessive Compulsive Disorder, Tourette’s Disorder, and Postraumatic Stress Disorder. The implications of dual cortical-subcortical functions for the frequent comorbidities de- scribed in childhood psychpathology are discussed. Cortical/subcortical models may provide a direction for candidate gene investigations where the same transmitter may have differing, but complementary functions. iv Contents Aims and Hypothesis 1 1 Introduction 5 1.1 Models of consciousness . 8 1.1.1 Consciousness theories . 10 1.1.2 Comment . 12 1.1.3 Global Workspace . 13 1.2 Modularity . 22 1.2.1 Comment . 30 1.2.2 Dual processing circuits . 31 1.3 Neural network models . 34 1.3.1 Temporal sequencing . 37 1.3.2 Discussion . 42 1.4 Cortical-basal ganglia loops . 43 1.4.1 Robotic models . 46 1.5 Discussion . 47 2 Evolution, language and social cognition 53 2.0.1 Introduction . 53 2.0.2 Language evolution . 54 2.1 Speech perception . 58 2.1.1 Comment . 60 2.1.2 Dual language systems . 61 2.1.3 The Language hypothesis . 63 2.1.4 Comment . 66 2.1.5 Mirror systems . 66 2.2 Ontogenesis of social cognition . 69 v vi CONTENTS 2.2.1 Language development . 71 2.2.2 The RR model of language development . 71 2.2.3 Nature nuture . 76 2.2.4 Birdsong analogy and neural circuits . 79 2.2.5 Comment . 83 2.2.6 Genes, circuits and behaviour . 83 2.2.7 Cognitive function of language . 85 2.2.8 Discussion . 90 2.3 Reading, language and neural circuits . 92 2.3.1 Neural reading circuits . 93 2.3.2 Attention and reading . 95 2.3.3 Comment . 97 3 Neural circuits and behaviour control 99 3.1 Circuit plans of cortex, cerebellum and basal ganglia . 100 3.1.1 Circuit plan of neocortex . 100 3.1.2 Circuit plan of the cerebellum . 103 3.1.3 Circuit plan of the basal ganglia . 103 3.1.4 Basal ganglia and executive functions . 104 3.1.5 Comment . 106 3.1.6 New Anatomy of the Basal Forebrain . 107 3.1.7 Comment . 117 3.2 Oscillation networks . 118 3.2.1 Comment . 122 3.3 Temporally structured replay of behaviour . 122 3.4 Prefrontal cortex: cognitive and executive functions . 123 3.4.1 Comment . 127 4 Development and working memory 129 4.1 Structural development . 130 4.2 Working memory . 136 4.2.1 Higher Order Cognition and Working Memory . 143 4.2.2 Comment . 148 5 The emotional brain 151 5.1 Emotion circuits . 155 5.1.1 Comment . 161 CONTENTS vii 5.1.2 Basal forebrain organisation . 161 5.1.3 Comment . 167 5.1.4 Discussion . 171 5.2 Social cognition and neural circuits . 172 5.2.1 Comment . 180 5.2.2 Reappraisal theory . 181 5.2.3 Discussion . 186 6 Attention Deficit/Hyperactivity Disorder 189 6.1 Theories of ADHD . 190 6.1.1 ADHD circuits . 192 6.1.2 Comment . 202 6.2 Age effects . 203 6.2.1 ADHD and early onset bipolar disorder . 205 6.2.2 Working memory and ADHD . 205 6.2.3 Imaging studies . 208 6.2.4 Resting/default state and vigilance variability . 210 6.2.5 Continuous Performance Task (CPT) . 211 6.2.6 Discussion . 213 6.3 Treatment models . 215 7 Conduct Disorder and neural circuits 221 7.1 Diagnostic issues . 221 7.2 Basic emotion theories . 225 7.2.1 Fear circuits . 226 7.2.2 Reward circuits . 230 7.3 Genetic effects . 231 7.3.1 Comment . 234 7.3.2 Discussion . 236 8 Autistic Disorder/Asperger’s Syndrome 239 8.1 Autism . 239 8.1.1 Language in Autism . 240 8.1.2 Theory of Mind and Autism . 246 8.1.3 Central coherence theory . 249 8.1.4 Face processing in autism . 254 8.1.5 Neural abnormalities in autism . 257 viii CONTENTS 8.2 Asperger’s Disorder . 268 8.2.1 Discussion . 268 8.2.2 Therapeutic implications . 269 9 OCD and Tourette’s Disorder 271 9.1 Neural circuits in OCD . 272 9.1.1 The glutamate hypothesis . 276 9.2 Obsessive Compulsive Spectrum Disorders . 277 9.2.1 Developmental perspective . 282 9.2.2 Therapeutic implications . 283 9.2.3 Comment . 284 9.2.4 Discussion . 289 10 Posttraumatic Stress Disorder 291 10.1 Neural circuits in PTSD . 292 10.1.1 Neurocircuitry models . 303 10.1.2 Nucleus Accumbens/Ventral striatum and Anxiety Syndromes . 305 10.1.3 Sensitive period: gene environment interaction . 310 10.1.4 Comment . 311 11 Comorbidity 313 11.1 Diagnostic issues . 313 11.2 Circuit models . 317 11.2.1 Dual system model and comorbidity . 319 11.2.2 Interaction between cognitive and affective systems 321 11.2.3 Comment . 322 11.2.4 Cognitive/motor comorbidity . 323 11.2.5 Circuit pharmacology . 327 11.2.6 ADHD and Autistic spectrum disorder . 331 11.2.7 Comment . 331 12 Conclusions 333 Bibliography 343 Author Index 403 CONTENTS ix List of Figures 413 x CONTENTS CONTENTS 1 The ancient subject matter of psychology - the mind and its vari- ous manifestations - is distressingly invisible, and a science with invisible content is likely to become an invisible science. Miller, Galanter and Pribram, 1960. Aims and Hypothesis The present thesis aims to explore the contribution of connec- tionist, cognitive, and biological models to a better understanding of childhood psychopathology, at a time when rapid advances in brain mapping techniques are contributing to a ‘brain circuit’ un- derstanding of development and behaviour. In particular, brain circuit models and cognitive and connectionist approaches are thought to provide insights into the differences between stimulus- bound, rapid modular vs sequential cortico-striatal-cortical con- trol of behaviour.
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