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The Role of Gamma Oscillations and Cortical Inhibition in the Development of Working Memory in Adolescence

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The Role of Gamma Oscillations and Cortical Inhibition in the Development of Working Memory in Adolescence The Texas Medical Center Library DigitalCommons@TMC The University of Texas MD Anderson Cancer Center UTHealth Graduate School of The University of Texas MD Anderson Cancer Biomedical Sciences Dissertations and Theses Center UTHealth Graduate School of (Open Access) Biomedical Sciences 12-2019 THE ROLE OF GAMMA OSCILLATIONS AND CORTICAL INHIBITION IN THE DEVELOPMENT OF WORKING MEMORY IN ADOLESCENCE Christopher P. Walker Follow this and additional works at: https://digitalcommons.library.tmc.edu/utgsbs_dissertations Part of the Behavior and Behavior Mechanisms Commons, Cognitive Neuroscience Commons, Cognitive Psychology Commons, Developmental Psychology Commons, and the Other Psychiatry and Psychology Commons Recommended Citation Walker, Christopher P., "THE ROLE OF GAMMA OSCILLATIONS AND CORTICAL INHIBITION IN THE DEVELOPMENT OF WORKING MEMORY IN ADOLESCENCE" (2019). The University of Texas MD Anderson Cancer Center UTHealth Graduate School of Biomedical Sciences Dissertations and Theses (Open Access). 975. https://digitalcommons.library.tmc.edu/utgsbs_dissertations/975 This Dissertation (PhD) is brought to you for free and open access by the The University of Texas MD Anderson Cancer Center UTHealth Graduate School of Biomedical Sciences at DigitalCommons@TMC. It has been accepted for inclusion in The University of Texas MD Anderson Cancer Center UTHealth Graduate School of Biomedical Sciences Dissertations and Theses (Open Access) by an authorized administrator of DigitalCommons@TMC. For more information, please contact [email protected]. THE ROLE OF GAMMA OSCILLATIONS AND CORTICAL INHIBITION IN THE DEVELOPMENT OF WORKING MEMORY IN ADOLESCENCE by Christopher Paul Walker, M.S. APPROVED: ______________________________ Raymond Y. Cho, M.D., M.Sc., Advisory Professor ______________________________ Scott D. Lane, Ph.D., Onsite Advisor ______________________________ Michael S. Beauchamp, Ph.D. ______________________________ Shane R. Cunha, Ph.D. ______________________________ Jair C. Soares, M.D., Ph.D. APPROVED: ____________________________ Dean, The University of Texas MD Anderson Cancer Center UTHealth Graduate School of Biomedical Sciences THE ROLE OF GAMMA OSCILLATIONS AND CORTICAL INHIBITION IN THE DEVELOPMENT OF WORKING MEMORY IN ADOLESCENCE A DISSERTATION Presented to the Faculty of The University of Texas MD Anderson Cancer Center UTHealth Graduate School of Biomedical Sciences in Partial Fulfillment of the Requirements for the Degree of DOCTOR OF PHILOSOPHY by Christopher Paul Walker, M.S. Houston, Texas December, 2019 Copyright © 2019 Christopher Paul Walker. All rights reserved. [email protected] iii ACKNOWLEDGMENTS In reflecting on my journey through graduate school and life, I am extremely humbled to be able to write statements like this. The support and encouragement that I have received from family, friends, and colleagues throughout this process has been amazing. I would like to start by thanking my mentor, Dr. Raymond Cho, for his patience, guidance, and support. He has provided me the space to learn and grow and develop as a scientist in this word. I cannot begin to repay the opportunities he has opened in my life. I would also like to thank my advisory committee: Dr. Michael Beauchamp, Dr. Shane Cunha, Dr. Scott Lane, and Dr. Jair Soares. Their professional insight and guidance over the past several years have helped me achieve the goals I set out for myself. I must also thank the many colleagues and friends throughout the years who have helped me along. I know that I would not be here without a team I trust backing me up. In particular, I would like to thank Nithya Ramakrishnan, Danica Womack, Cristin Ridriguez, Megan Rafferty, Nik Murphy, Nicola Polizzotto, Jeanie Henderson, and Norma Moncayo to whom I owe most of the credit for making my project as success. I would like to thank GSBS and the Neuroscience program for offering me an intellectual home and community to further my growth as a scientist and researcher. I would like to thank the Division of Neuropsychiatry at the Baylor College of Medicine for providing me with the space and resources to be able to see this project through. And I would like to thank the families who spared their time to participate in my study. iv Most especially, I must thank my family. Jane Walker, my mom. Jim Walker, my dad. Rusty Walker, my brother, and his wife Lauren Walker. Through years of ups and downs, they have been a constant source of encouragement, helping me to persevere, supporting me at my lows, and celebrating me at my highs. I hope that now that I will be near home again I can begin to return the favor. Finally, to my wife, Isabel Roth, I owe her more than I can say. She has been the most amazing presence and stabilizing force in my life. I am enormously grateful to the wonderful luck that brought us both to Houston at the same time. And I am excited to see our future unfold together. v ABSTRACT THE ROLE OF GAMMA OSCILLATIONS AND CORTICAL INHIBITION IN THE DEVELOPMENT OF WORKING MEMORY IN ADOLESCENCE Christopher Paul Walker, M.S. Advisory Professor: Raymond Y. Cho, M.D., M.Sc. Adolescence is a dynamic period of social, cognitive, and biological changes. In particular, working memory, the ability to actively encode and maintain information over a short period of time, develops early in childhood and gradually increases in capacity and stability during adolescence. The precise neurophysiological mechanism by which working memory capacity increases during adolescence is unclear. The objective of this investigation was to evaluate the role of cortical gamma-band (> 30 Hz) oscillations— which are associated with working memory in adults—for the development of working memory capacity in adolescents, and to identify the extent to which the temporal profile of gamma-aminobutyric acid (GABA)-mediated cortical inhibition underlies these changes. I hypothesized that cortical gamma-band rhythms would become faster during adolescence in a manner that supports improved working memory capacity, and that the kinetics of cortical inhibition would also become faster to support these faster rhythms. To this end, I recruited two cohorts of typically developing children (10 – 12 years) and adolescents (15 – 17 years) for a combined electrophysiology (EEG) and transcranial magnetic stimulation (TMS) study. First, I investigated the endogenous rhythmic activity generated by children and adolescence when performing a serially presented working memory task of varying set size. I found evidence of maturation in the vi generation of gamma-band rhythms which differed in power between groups, but identified no effects of a change in the central frequency of gamma-band activity. Next, I used TMS to exogenously evoke oscillatory activity in the left prefrontal cortex to identify the cortical natural (i.e., resonant) frequency. Using this measure, I found that adolescents exhibit higher median natural frequencies (MdCHILD = 16 Hz; MdADO = 24 Hz, Z = 2.35, p = 0.009), but that sex may play a mediating role when this change emerges. While this measure positively correlated with working memory capacity (rs = 0.47, p = 0.007), this effect disappeared when controlling for age and sex (rs = 0.29, p = 0.128). Finally, I investigated the role of inhibitory timing as a potential mechanism for improved cognition and increased natural frequency using classic paired pulse TMS techniques. Six inter-pulse intervals (IPI) in the range of short- and long-intracortical inhibition (SICI, LICI) were tested to assess the temporal characteristics of GABA type- A and type-B receptor-mediated inhibition (GABAAR, GABABR, respectively). For SICI, I found alpha-band (9-14 Hz) facilitation in children and suppression in adolescents. For LICI, adolescents demonstrated greater suppression of gamma-band power compared to children, and equal suppression to children in the beta-band (15-30 Hz). I found no evidence for a change in timing of SICI- or LICI-induced modulations though LICI suppression of gamma- and beta-band power correlated with working memory capacity. The overall hypothesis that the prefrontal cortex can produce faster rhythms during adolescent development was supported, but the hypothesized relationships between those rhythms, working memory capacity, and the timing of GABA-mediated inhibition were not. Rather, I observed several developmental differences in oscillatory power that suggest excitation-inhibition balance underlies the developmental increases in working memory capacity and gamma-band synchrony. vii TABLE OF CONTENTS APPROVAL PAGE ........................................................................................................... i TITLE PAGE ................................................................................................................... ii COPYRIGHT ................................................................................................................. iii ACKNOWLEDGMENTS ................................................................................................ iv ABSTRACT .................................................................................................................... vi TABLE OF CONTENTS ............................................................................................... viii LIST OF FIGURES ......................................................................................................... x LIST OF TABLES ..........................................................................................................
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