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Neural Correlates of Self-Regulatory Fatigue and the Role of High Affinity Striatal Dopaminergic Receptors in Tourette Syndrome and Healthy Subjects

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Neural Correlates of Self-Regulatory Fatigue and the Role of High Affinity Striatal Dopaminergic Receptors in Tourette Syndrome and Healthy Subjects NEURAL CORRELATES OF SELF-REGULATORY FATIGUE AND THE ROLE OF HIGH AFFINITY STRIATAL DOPAMINERGIC RECEPTORS IN TOURETTE SYNDROME AND HEALTHY SUBJECTS Elia Abi-Jaoude, BSc, MSc, MD, FRCPC A thesis submitted in conformity with the requirements for the degree of Doctor of Philosophy Graduate Department of the Institute of Medical Science, Faculty of Medicine University of Toronto © Copyright by Elia Abi-Jaoude 2020 Neural Correlates of Self-Regulatory Fatigue and the Role of High Affinity Striatal Dopaminergic Receptors in Tourette Syndrome and Healthy Subjects Elia Abi-Jaoude Doctor of Philosophy Institute of Medical Science, Faculty of Medicine University of Toronto 2020 Abstract Tourette syndrome (TS) is a developmental neuropsychiatric condition characterized by motor and vocal tics. Tics are semi-voluntary movements or vocalizations that are stereotyped, repetitive and non-rhythmic. They usually occur in response to a premonitory urge, and can be suppressed temporarily. TS typically involves multiple comorbidities, in particular obsessive- compulsive disorder, attention deficit/hyperactivity disorder, and emotional dysregulation. Given the clinical phenomenology, TS has been conceptualized as a syndrome of inhibitory deficits involving motor, cognitive, emotional and behavioral domains. Neuroimaging studies have implicated the cortico-striato-thalamo-cortical circuitry, in particular the striatal dopamine system, and cortical control areas. However, despite numerous studies, findings have been mixed, and a definitive explanation of the neurobiology underlying TS has remained elusive. The objective of this body of work was to utilize novel neuroimaging approaches in an attempt to identify neural mechanisms that could contribute to the manifestation of TS. In a positron emission tomography (PET) imaging study of the striatum, I investigated striatal D2/3 dopamine ii receptors in TS using the radioligands [11C]raclopride and [11C]-(+)-PHNO, an agonist that binds preferentially to D3 receptors, thus allowing higher sensitivity and measurement of receptors in a high affinity state. Eleven adults with TS and 11 matched healthy control (HC) participants underwent [11C]raclopride and [11C]-(+)-PHNO PET scans. There were no significant group differences between TS and HC participant binding potentials (BPND) in ventral, motor and associative striatum. In a functional magnetic resonance imaging (fMRI) study of self-regulatory fatigability using an eye blink inhibition paradigm, high-performing HC participants had relatively higher activation in known prefrontal cortex (PFC) control areas – inferior frontal gyrus (IFG), dorsolateral prefrontal cortex (DLPFC), and supplemental motor area (SMA) – whereas self-regulatory fatigability was associated with relatively higher activation in ventromedial PFC, rostroventral anterior cingulate cortex (ACC), and orbitofrontal cortex (OFC). Based on these findings, I carried out a region of interest (ROI) analysis comparing 19 HC and 12 TS participants. There was substantially less percent signal change in the DLPFC/IFG and SMA ROIs in the TS group in comparison to the HC group. These findings suggests that self-regulatory deficits in TS arise from fatigability in cortical control. iii Acknowledgments and Contributions First and foremost, I would like to thank my PhD supervisor and mentor, Dr. Paul Sandor, for being so supportive over the years that I have known him. He introduced me to the field of Tourette syndrome when I met him initially as a medical student in 2003, and since then I have benefitted from working with him clinically and academically during my residency, fellowship, and since. His openness and support has allowed me to pursue various different projects, in the process gaining broad and rich experiences in various aspects of the field of Tourette syndrome and beyond. As well, I would like to thank my committee members, Dr. Mary Pat McAndrews and Dr. Tomáš Paus, for their invaluable feedback and guidance in developing my project, and support and encouragement throughout the process. In addition, I am grateful to the many friends and colleagues whom I have consulted both formally and informally, and those who have contributed to various aspects of this work, including: Drs. David Kideckel, Adrian Crawley, David Mikulis, Jane Lawrence-Dewar, Donna Stewart, Daniel Gorman, Aaron Kucyi, Karen Davis, Conny McCormick, Rostom Mabrouk, Robyn Stephens, Barbara Segura, Sang Soo Cho, Antonio Strafella, Ignacio Obeso, Sylvain Houle, Anthony Lang, Pablo Rusjan, Romina Mizrahi, Ariel Graff, Kelly Aminian, Lei Chen, Patrina Cheung, Ms. Zhe (Ann) Feng, and Ms. Tracy Bhikram. I would also like to thank Mr. Keith Ta, Mr. Eugen Hlasny, Ms. Alvina Ng, Ms. Laura Nguyen, and Ms. Anusha Ravichandran for technical help with scanning in my studies. iv I am deeply indebted to all the individuals who participated in my studies, to my patients from whom I get the most rewarding of interactions and who drive me to continue doing what I do, and from the Tourette syndrome community at large. I would like to thank the many friends, colleagues, and family members who have been an ongoing source of encouragement and moral support, and who will be pleased with the completion of this thesis. They are too numerous to list here, but as I write this they are definitely in my thoughts. My wife, Dr. Myriam Lafreniere-Roula, has been a constant and valuable sounding board, with her insight, wisdom, love and support since two decades, and my two daughters, Luiza and Chloe, are the joy and light in my life – they make me the fortunate human being that I am. My aunt, Dr. Siham Abu-Jawdeh, valued higher education and the pursuit of knowledge, and encouraged me to pursue my PhD. Unfortunately, she will not be able to fully appreciate the completion of my thesis given her current level of dementia. This thesis is dedicated to you, Siham. Last but not least, I would like to acknowledge the following sources of funding support that I have had: the University Health Network Department of Psychiatry Research Training Fellowship, Ontario Mental Health Foundation Research Studentship Award, Ontario Graduate Scholarship in Science and Technology, University of Toronto School of Graduate Studies Conference Grant, and the University of Toronto Institute of Medical Science Open Award. v Table of Contents Acknowledgments and Contributions ............................................................................................ iv Table of Contents ........................................................................................................................... vi List of Abbreviations ..................................................................................................................... ix List of Tables ............................................................................................................................... xiii List of Figures .............................................................................................................................. xiv List of Appendices .........................................................................................................................xv Chapter 1 ..........................................................................................................................................1 Introduction and Rationale ......................................................................................................1 Chapter 2 ..........................................................................................................................................4 Literature Review......................................................................................................................4 2.1 Introduction to Tourette Syndrome .................................................................................6 2.2 Clinical Assessment ............................................................................................................7 2.2.1 Diagnostic Criteria ...................................................................................................7 2.2.2 Screening for Co-morbid Disorders and Behaviors .................................................8 2.2.3 Investigations ...........................................................................................................9 2.2.4 Patient and Parent Information and Resources ......................................................10 2.2.5 Quality of Life........................................................................................................11 2.3 PANDAS ...........................................................................................................................12 2.4 Treatment of Tourette Syndrome...................................................................................15 2.4.1 Psychosocial and Behavioural Treatments ............................................................17 2.4.2 Pharmacological Treatment ...................................................................................21 2.4.3 Treating Comorbidities ..........................................................................................40 2.5 Integrated Clinical Practice ............................................................................................42 vi 2.6 Tourette Syndrome Pathophysiology .............................................................................44 2.6.1 Dopamine Receptor Imaging .................................................................................46
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