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Neurobiological and Metabolic Mechanisms of Binge-Eating in Anorexia and Bulimia Nervosa

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Neurobiological and Metabolic Mechanisms of Binge-Eating in Anorexia and Bulimia Nervosa Neurobiological and metabolic mechanisms of binge-eating in anorexia and bulimia nervosa Margaret Louise Westwater-Wozniak Department of Psychiatry University of Cambridge This thesis is submitted for the degree of Doctor of Philosophy Darwin College September 2020 ii A relevant quote from Sir Richard Morton, who was credited with the first English- language description of anorexia nervosa: “Mr. Duke’s daughter in St. Mary Axe, in the year 1684 and the eighteenth year of her age, in the month of July fell into a total suppression of her monthly courses from a multitude of cares and passions of her mind But without and symptom of the green- sickness following upon it. […] I do not remember that I did ever in all my practice see one that was conversant with the living so much wasted with the greatest degree of consumption (like a skeleton only clad with skin). […] A nervous atrophy, or consumption, is a wasting of the Body without any remarkaBle fever, cough, or shortness of Break; But it is attended with a want of appetite, and a Bad digestion, upon which there follows a languishing weakness of nature, and a falling away of the flesh every day more and more.” – Sir Richard Morton, 1689 iii Declaration This thesis is the result of my own work and includes nothing which is the outcome of work done in collaboration except as declared in the Acknowledgements and specified in the text. It is not substantially the same as any that I have submitted, or, is being concurrently submitted for a degree or diploma or other qualification at the University of Cambridge or any other University or similar institution. I further state that no substantial part of my thesis has already been submitted, or, is being concurrently submitted for any such degree, diploma or other qualification at the University of Cambridge or any other University or similar institution. It does not exceed the prescribed word limit for the relevant Degree Committee. This thesis contains fewer than 60,000 words excluding figures, tables, appendices, and bibliography and has fewer than 150 figures. Margaret Louise Westwater-Wozniak September 2020 iv Acknowledgements First and foremost, I am grateful to my supervisors, Prof Paul Fletcher and Dr Hisham Ziauddeen, for their limitless support, unwavering mentorship and incisive scientific and clinical insights. To Paul, thank you for encouraging me to pursue research that is as ambitious as psychiatric illnesses are complex; for shaping my scientific ‘backbone’ on principles, not p-values, and for upholding a sense of compassion for the patients we aim to help at every step. Hisham, thank you for always going above and beyond your duties as a mentor to foster my scientific and personal development; I can only hope that I will someday provide the same fierce support to my own students. The work presented herein would not have materialised without the encouragement of my Cambridge friends and labmates, Jakob, Laurel, Dan, Owen, Juliette, Johanna, Juliet, Emma, Jess, Kelly and Jake, and it is with the deepest respect and gratitude that I say thank you. To my NIH mentors, Drs Monique Ernst and Christian Grillon, thank you for welcoming me into your lab and for your willingness to foster my work within the enriching environment of the NIMH. To the women who took part in this study, this work is as much yours as it is mine; you inspired me with your courage, resilience and selflessness, and it was a privilege to learn from you. And finally, to Travis, for your love and support throughout this transatlantic journey. v vi Abstract Binge-eating is characterised by the recurrent consumption of large amounts of food, which co-occurs with a subjective loss of control over intake. This transdiagnostic syndrome results in significant distress, functional impairment and comorbidity. However, precise characterisation of the physiological and neurobiological mechanisms that give rise to, or maintain, this behaviour is lacking. This thesis integrates observations across metabolic, neural and behavioural levels in women with and without eating disorders, providing novel insights into how perturbations across each strata interact with one another in illness and in health to shape eating behaviour. In Chapter 1, I review the classification of binge-eating disorders prior to summarising the extant literature on homeostatic and non-homeostatic mechanisms that influence (ab)normal eating behaviour. This introductory chapter also reviews current perspectives on how psychological stress influences disordered eating, outlining the motivation for the multimodal neuroimaging protocol detailed in Chapter 2. Chapter 2 focuses on the specific methodology of this neuroimaging study, which examined the impact of acute, psychological stress on gut hormones, endocrine responses, and inhibitory control in women acutely ill with the binge-eating and purging subtype of anorexia nervosa, bulimia nervosa and matched controls. Chapters 3 through 5 report the results of this study. Chapter 3 focuses on findings of dissociable hormonal responses to stress in anorexia and bulimia nervosa, presenting novel evidence that links acute changes in mental state to altered gut hormone signalling in anorexia nervosa. Chapter 4 is dedicated to the functional magnetic resonance imaging arm of the protocol, which rigorously examined the impact of diagnosis and induced stress on two forms of response inhibition: proactive and reactive control. Chapter 5 provides insight into associations between peripheral metabolic markers and neural integrity of the cerebral cortex in patients and controls. vii Finally, Chapter 6 provides a brief summary, discusses the implications of these findings and presents some ongoing and future research that extends this original work. In summary, this thesis represents, to my knowledge, the first attempt to generate a multi-level framework for understanding the physiological and psychological mechanisms of illnesses characterised by binge-eating. Findings identify important metabolic and neurobiological distinctions between two eating disorders with shared symptomatology, demonstrating the need for, and value in, integrative models of mental illness. viii Publications arising from this thesis Westwater, ML, Mancini, F, Gorka, AX, Shapleske, J, Serfontein, J, Grillon, C, Ernst, M, Ziauddeen, H & Fletcher, PC. (2020) Prefrontal responses during proactive and reactive inhibition are differentially impacted by stress in anorexia and bulimia nervosa. BioRxiv. https://doi.org/10.1101/2020.02.27.968719. Under review. Westwater, ML, Mancini, F, Shapleske, J, Serfontein, J, Ernst, M, Ziauddeen, H & Fletcher, PC. (2020). Dissociable hormonal profiles for psychopathology and stress in anorexia and bulimia nervosa. Psychological Medicine, 1–11. https://doi.org/10.1017/S0033291720001440. Other puBlications during this PhD: Pan, P, Sato, J, Paillère Martinot, ML, Martinot, JL, Pentila, J, Grimmer, Y, van Noort, B, Becker, A, IMAGEN Consortium, Westwater, ML, Grillon, C, Stringaris, A. & Ernst, M. (2020). Developmental trajectory of a ventral striatal-depression link in adolescence. Under review. Westwater, ML, Vilar-Lopez, R, Ziauddeen, H, Verdejo-Garcia, A & Fletcher, PC. (2019). Combined effects of age and BMI are related to altered cortical thickness in adolescence and adulthood. Developmental Cognitive Neuroscience, 40, 100728. doi:10.1016/j.dcn.2019.100728. Westwater, ML, Seidlitz, J, Diederen, KMJ, Fischer, S & Thompson, JC. (2018). Associations between cortical thickness, structural connectivity and severity of dimensional bulimia nervosa symptomatology. Psychiatry Research: Neuroimaging, 271, 118 - 125. doi:10.1101/127910. Fischer, S, Breithaupt, LE, Wonderlich, JA, Westwater, ML, Thompson, JC, Crosby, RD, Engel, S, Lavender, J, & Wonderlich, SA. (2017). Impact of the neural correlates of stress and cue reactivity on stress and binge eating in the natural environment. Journal of Psychiatric Research, 92, 5 – 23. doi:10.1016/j.jpsychires.2017.03.017. ix Awards Based on the work presented in this thesis: International Biomedical Research Alliance Translational Award for Advances in Medical Science (2020) x List of Figures Figure 1.1 Control of food intake via hypothalamic signalling and the gut-brain axis Figure 1.2 Ghrelin signalling modulates hypothalamic and dopaminergic projections Figure 1.3 Fronto-striatal circuits associated with distinct facets of impulsivity in humans Figure 1.4 Schematic of four fronto-striatal loops putatively associated with impulsivity and compulsivity Figure 2.1 Illustration of the independent race model of Go and Stop processes Figure 2.2 Overview of study design and blood sampling protocol Figure 2.3 Schematic of the stop-signal anticipation task Figure 2.4 Acute stress increased negative affect across pre- and post-ad libitum meal time points Figure 2.5 Subjective ratings of electrical stimulation Figure 3.1 Diagnostic and dimensional correlates of salivary cortisol awakening response Figure 3.2 Associations between acute psychological stress and metabolic markers Figure 3.3 Associations between pre-prandial hormones, BMI and eating behaviour across neutral and stress conditions Figure 4.1 Whole-brain activation in anorexia nervosa, bulimia nervosa and controls during proactive inhibition Figure 4.2 Region of interest analyses identify altered inferior frontal and premotor activity during proactive inhibition in anorexia and bulimia nervosa Figure 4.3 Impaired proactive inhibition in bulimia nervosa is associated with increased
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