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The Effect of Chronic Stress on the Adolescent Brain, Learning, and Memory

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The Effect of Chronic Stress on the Adolescent Brain, Learning, and Memory The effect of chronic stress on the adolescent brain, learning, and memory Anthea Aphrodite Stylianakis Bachelor of Psychology (Hons) A thesis in fulfilment of the requirements for the degree of Doctor of Philosophy School of Psychology Faculty of Science UNSW Sydney January 2021 Thesis Title TTitle:The effect of chronic stress on the adolescent brain, learning, and memory. Thesis Abstract Adolescence is a period in which major psychological and neural changes occur, along with changes in the stress response. This has resulted in some researchers characterising this developmental period as one of "storm and stress". Interestingly, the brain regions implicated in learning and memory processes are both particularly sensitive to stress and undergoing major development during adolescence. Therefore, the broad aim of this thesis was to examine the impact of chronic stress exposure early in life on learning and memory processes that underlie a number of mental disorders. In the first two empirical Chapters, I examined pharmacological and endogenous activation of Tropomyosin receptor kinase B (TrkB}, a key mediator of activity-dependent plasticity underlying memory, during Pavlovian fear conditioning and extinction in adolescent rats. In Chapter 2 I examined the effects of an agonist of TrkB on extinction retention in both non-stressed adolescent rodents and those that had been exposed to chronic levels of corticosterone, a stress-related hormone. Pharmacological activation of TrkB during extinction training facilitated extinction retention in non-stressed adolescent rats, but not in those exposed to chronic corticosterone. In Chapter 3 I examined levels of full-length, truncated, and activated (phosphorylated} TrkB receptors in three key brain regions involved in extinction: the ventral hippocampus, prefrontal cortex, and basolateral amygdala, of adult and adolescent rats following extinction training. One pertinent finding of this work was a significantly higher ratio of truncated to full-length TrkB receptors in the ventral hippocampus of adults than adolescents. In Chapter 4 human participants (older adolescents and adults) were exposed to an acute stressor (the cold pressor test) prior to viewing trauma images and provided salivary samples for analyses of the stress hormone cortisol. Participants recorded instances of ii intrusive, involuntary memories of these images over subsequent days. No age differences were detected in relation to the number of intrusive memories reported by participants, or their cortisol response to the cold pressor test. However, individuals with higher levels of early-life adversity were significantly more affected by exposure to trauma images. Taken together, these experiments extend knowledge of the impact of chronic stress and adversity in adolescence on learning and memory. ORIGINALITY STATEMENT Iii' 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 acknowledgement is made in the thesis. Any contribution 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. COPYRIGHT STATEMENT Iii' I hereby grant the University of New South Wales or its agents a non-exclusive licence to archive and to make available (including to members of the public) my thesis or dissertation in whole or part in the University libraries in all forms of media, now or here after known. I acknowledge that I retain all intellectual property rights which subsist in my thesis or dissertation, such as copyright and patent rights, subject to applicable law. I also retain the right to use all or part of my thesis or dissertation in future works (such as articles or books}. For any substantial portions of copyright material used in this thesis, written permission for use has been obtained, or the copyright material is removed from the final public version of the thesis. AUTHENTICITY STATEMENT Iii' I certify that the Library deposit digital copy is a direct equivalent of the final officially approved version of my thesis. Abstract Adolescence is a period in which major psychological and neural changes occur, along with changes in the stress response. This has resulted in some researchers characterising this developmental period as one of “storm and stress”. Interestingly, the brain regions implicated in learning and memory processes are both particularly sensitive to stress and undergoing major development during adolescence. Therefore, the broad aim of this thesis was to examine the impact of chronic stress exposure early in life on learning and memory processes that underlie a number of mental disorders. In the first two empirical Chapters, I examined pharmacological and endogenous activation of Tropomyosin receptor kinase B (TrkB), a key mediator of activity-dependent plasticity underlying memory, during Pavlovian fear conditioning and extinction in adolescent rats. In Chapter 2 I examined the effects of an agonist of TrkB on extinction retention in both non-stressed adolescent rodents and those that had been exposed to chronic levels of corticosterone, a stress-related hormone. Pharmacological activation of TrkB during extinction training facilitated extinction retention in non-stressed adolescent rats, but not in those exposed to chronic corticosterone. In Chapter 3 I examined levels of full-length, truncated, and activated (phosphorylated) TrkB receptors in three key brain regions involved in extinction: the ventral hippocampus, prefrontal cortex, and basolateral amygdala, of adult and adolescent rats following extinction training. One pertinent finding of this work was a significantly higher ratio of truncated to full-length TrkB receptors in the ventral hippocampus of adults than adolescents. In Chapter 4 human participants (older adolescents and adults) were exposed to an acute stressor (the cold pressor test) prior to viewing trauma images and provided salivary samples for analyses of the stress hormone cortisol. Participants recorded instances of i intrusive, involuntary memories of these images over subsequent days. No age differences were detected in relation to the number of intrusive memories reported by participants, or their cortisol response to the cold pressor test. However, individuals with higher levels of early-life adversity were significantly more affected by exposure to trauma images. Taken together, these experiments extend knowledge of the impact of chronic stress and adversity in adolescence on learning and memory. ii Table of Contents Acknowledgements .................................................................................................................. v Publications ............................................................................................................................ vii Presentations ........................................................................................................................... ix Care and use of animals .......................................................................................................... x List of Abbreviations .............................................................................................................. xi Chapter 1: General Introduction ........................................................................................... 1 Fear Conditioning and Extinction .......................................................................................... 5 Neural Mechanisms of Extinction ......................................................................................... 8 Improving Extinction Retention in Adolescents .................................................................. 14 Chronic Stress and Adolescent Extinction Retention .......................................................... 15 Adolescence as a Stress-Sensitive Period of Development ................................................. 17 Chronic Stress Exposure and Extinction Retention ............................................................. 19 The Current Thesis ............................................................................................................... 23 Chapter 2: The impact of the TrkB agonist 7,8-DHF on extinction retention in non- stressed adolescent rats and those exposed to chronic corticosterone .............................. 25 General Method ................................................................................................................... 31 Experiment 2.1 ..................................................................................................................... 36 Experiment 2.2 ..................................................................................................................... 44 Analysis 2.1: The Efficacy of 7,8-DHF in Non-Stressed Adolescent Rats ......................... 50 Experiment 2.3a ................................................................................................................... 55 Experiment 2.3b ..................................................................................................................
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