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Salience Network in Psychosis

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Salience Network in Psychosis ! #$%"&'(&!)&*+,-.!"'!/01(2,0"0! 3&'$!/$%$'"1$44$'5!677#5!689/01(2! ! :2&0"0!0;<="**&>!*,!*2&!?'"@&-0"*1!,A!),**"'B2$=!A,-!*2&!>&B-&&!,A! C,(*,-!,A!/2"%,0,4215!>$*&>!D;%1!EFGH! ! "! !"#$%!&$! This thesis explores the role of a large-scale brain network comprising of the insula and anterior cingulate cortex in the pathophysiology of psychosis using structural and functional neuroimaging. Primarily, anatomical changes affecting the grey matter structure and patterns of dysconnectivity involving the insula are investigated. Various meta-analytic studies have reported consistent reduction in insular grey matter across various psychotic disorders. Despite these robust observations, the role played by this brain region in the generation of psychotic symptoms remains unexplored. In this thesis, using a meta-analytic approach, the relevance of insula for the clinical expression of psychosis is highlighted. Further, significant reduction in the cortical folding of the insula was noted in patients with schizophrenia. Reduced gyrification is accompanied by reduced functional connectivity between the insula and the rest of the brain. Using an effective connectivity approach (Granger Causal Analysis), the primacy of insula in driving the dorsolateral prefrontal cortex is demonstrated in healthy controls; this relationship is significantly affected in schizophrenia amounting to aberrant connectivity within a putative salience-execution loop. Reduced primacy of the salience-execution loop relates to illness severity. It is argued that the insula, as a key region of the salience network, plays a crucial role in the generation of symptoms of psychosis. The evidence in support of this theory is discussed, together with its implications for clinical practice aimed at reducing the burden of psychosis. ! ""! !"#$%&! '()*+,- .*/"0*! 123+,- 4"*5! 6789:;- <7"0*- ="*>6+) >+? =%@A+B C9 %>DE /F*+,- *+? 67- G5: ;3"0* *+H! - 12B7"*+5 A+I- J0K; A+/9- 0>L5; MI- NHO- PQ5*K /+K+; R*,- *S*,- T/UV KH7; (+*,- WI/I TH0Q; /+X*Y CZI!7 6[XF*HO- C&06; 4Z=H CH7+I !HQ,- C&06; 8H\9 /+7- *]IL *%&C ^7+I >Y_9I CK`;- 6Y&Y 015A+UO G5/$a 1bc- W%deY ^9f5 4%Q/$a 1bc- !H1I ?Qg5 >+2EfH '*LF*7- ^*hH 6+2EfH '1ij%K =A"*,- C&06; Ekj%K C>X*Y T*Zl- C&06 - >SAH m`;HQ7+5 T-6+.... 1B"I: >UQI TY& CF* 0/2%>; c`>%@a 1+5"I: >UQI. ***************** Ta1+ ... CI 0/%& N+n opqH%Qr- =s+ N+@+> 6+UO- c`>n *Z"I/"I:>+>. ***************** PiA+ ... ^K+)tE:'>Y&+-!0/5!1+)tEa!PB"**U;-"!6UQ!!Y&+/UkU;-# !!!!***************** ! """! !"#$%&'()*+($,!! ! Peter, thanks for inducing this preoccupation, infecting with your enthusiasm and also, furnishing all those missing ‘articles’! Bert, thanks a lot for teaching me the concept of ‘playing with softwares’. Vijender, thanks for being a good friend, conscientious colleague and uncertified squash guru. Tom, thanks for your early work on the insula which seeded this thesis. Rajeev, thanks for taking some of my ideas seriously and reducing the need for me to self-cite when pursuing the wicked h-index. ***** To the Wellcome Trust for funding my Research Training Fellowship ***** To Cris Glazebrook for supporting my PhD tuition fees To Ed Bullmore & Karl Friston, Chris Hollis and Dorothee Auer for supporting my Wellcome fellowship application To Elizabeth Liddle for setting up my first ANOVA To all users of the vibrant Freesurfer mailing list (Douglas Greve for VBM- SBM registration & Don Hagler for clarifying issues with surface area maps in particular) To anonymous peer reviewers for shaping this thesis, and correctly spelling my surname in every rejection letter. To Joaquim Radua for his help with the SDM software To Kay Head and Kathleen Shaw for their help with data collection To Marie Schaer for her excellent LGI script To Marije Jansen, Molly Simmonite and Kathrin Doege for their assistance in acquiring and analyzing the data reported in this thesis. ! "#! To MRC for sponsoring my attendance at the Cardiff Brain Research Summer School in 2011 To Nicol Ferrier for making me believe I could apply for Wellcome/MRC fellowships To Penny Gowland and Olivier Mougin for their assistance in acquiring the 7T data To Prof. Rajarathinam for ensuring that I remain a curious student of Psychiatry throughout my career. To the Academic Faculty of the RCPsych for Margaret Slack Award & the Research Prize 2011 To the General Adult Faculty of the RCPsych the Trainee Research Prize 2010 To Tim Crow for his constant inspiration (and of course the Mac computer!) To Verghese Joseph & Pavan Mallikarjun for acquiring crucial clinical data. To Schizophrenia and Bipolar Research Societies - SIRS (2012) and IBDS (2011) - for awarding me Travel Fellowships To the editors of Neuroimage, Biological Psychiatry, Psychiatry Research: Neuroimaging, Journal of Psychiatry & Neuroscience, Human Brain Mapping, Schizophrenia Bulletin, Schizophrenia Research, Molecular Psychiatry, Brain Structure & Function, PLOSOne, Frontiers in Psychiatry, Cortex, Neuroscience & Biobehavioural Reviews and Cerebral Cortex for providing me with opportunities not only to review others’ work but also to reconsider my own work in the process. To Robert Sommers Award Society (Giessen), European Science Foundation, Guarantors of Brain, Royal College of Psychiatrists and Graduate Travel funds from the University of Nottingham for supporting my attendance at various meetings !"#$"%&'(")'#*&+,-"+.'"/,$&'.,0"1#*2&/*0"34."%.-,/*&&'&5"+.'"*4&"2$#)2/)" 1'.6&7*0"'&1.'*&5"2/"*420"3.'8 ! "! !"#$%&#! The work presented in this thesis has resulted from a collaborative effort of a team of researchers led by Prof. Peter Liddle and funded by various bodies including the Medical Research Council (Liddle), The Wellcome Trust (Palaniyappan) and internal grants from the Nottingham Institute of Neuroscience and School of Community Health Sciences (Pump Priming and Postgraduate Research Funds - Palaniyappan). Some of the imaging data used in this thesis (Chapter 5 and 6) were supported by New Investigator grant from the University of Nottingham and a Interdisciplinary Research Award from the Nottingham Institute of Neuroscience, University of Nottingham (Mallikarjun). All the data analyses presented in this thesis were designed, performed and written up by myself. The literature searches for the meta-analyses presented in Chapters 3 and 4 were independently cross-validated by Dr. Balain. Drs. Mallikarjun, Verghese and I acquired the clinical data reported in chapters 5 and 6. Dr Balain and I acquired the clinical data reported in chapters 7 and 8. All of the chapters presented here (except some sections of chapters 1 and 9) have been published in peer-reviewed journals; a list of the published manuscripts attached as an appendix to this thesis. The contributions of the co-authors are acknowledged in each manuscript, and elaborated in the Acknowledgements section. I was registered as a part-time PhD student throughout the period of my doctoral study. Between October 2009 and February 2012, I was supported by a HEFCE funded Clinical Lectureship (5 clinical sessions). From February 2012 onwards the Wellcome Trust supports me as a Research Fellow. I do not have any conflicts of interest related to this work. I received a Young Investigator Travel Fellowship to attend 9th Bipolar Disorder Meeting at Pittsburgh, PA, USA through a competition organized by International Bipolar Disorder Society. This award was sponsored by Eli Lilly. ! "#! Acronyms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bstract !!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!""#" Acknowledgments !!!!!!!!!!!!!!!!!!!!!!!!!!!!!!"""$" Preface !!!!%%%!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!!%""&'" Acronyms !!!!%%%!!!!!!!!!!!!!!!!!!!!!!!!!!!!!%%""vii" Chapter 1: The Pathogenesis Of Schizophrenia: A Guided Inquiry .... 1 1.1 Studies of brain structure in schizophrenia ................................. 5 1.2 Localisation of grey matter deficits in schizophrenia ................. 8 1.3 Developing a neuroanatomic model ............................................ 12 1.4 Outline of the thesis ...................................................................... 13 Chapter 2: A Hypothesis Of Insular Dysfunction ................................ 17 2.1 The nature of the structural deficits of the SN ........................... 18 2.2 Time course of structural changes in the SN ............................. 22 2.3 Effect of antipsychotics on the structure of the SN ................... 24 2.4 Functional attributes of the SN: the proximal salience ............ 26 2.5 fMRI studies of the SN in schizophrenia ..................................... 31 2.6 Correlation of insular deficits with clinical symptoms .............. 32 2.7 Insular dysfunction model of psychosis ..................................... 34 2.8 Dopamine and the Salience Network .......................................... 40 2.9 Unanswered questions ................................................................. 42 Chapter 3: The Neuroanatomy Of Psychotic Diathesis
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