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The Role of Habituation in Social Fear by Suzanne N. Avery Dissertation Slow to Warm Up: The Role of Habituation in Social Fear By Suzanne N. Avery Dissertation Submitted to the Faculty of the Graduate School of Vanderbilt University in partial fulfillment of the requirements for the degree of DOCTOR OF PHILOSOPHY in Neuroscience August, 2015 Nashville, Tennessee Approved: David Zald, Ph.D. Bunmi Olatunji, Ph.D. Brandon Ally, Ph.D. Jennifer Blackford, Ph.D. Copyright © 2015 by Suzanne N. Avery All Rights Reserved ii To my husband, Stacy, for his unending support, and my daughter, Sophie, for whom I do everything iii ACKNOWLEDGMENTS I would first and foremost like to thank my advisor, Dr. Jennifer Blackford, who is a truly exceptional scientist, teacher and mentor. She has encouraged me to pursue every opportunity for scientific achievement and has mentored me closely through each step. Her enthusiasm to help me become an excellent scientist and her generosity with her time and effort have made my graduate training an incredible experience. She has an incredible passion for science and possesses a brilliant combination of curiosity, creativity, motivation, intelligence and passion that inspires all of those who have the pleasure to work with her. I am eternally grateful for your mentorship—thank you is not enough. I would also like to thank the current and former members of the Blackford lab, including Jacqueline Clauss, Ross VanDerKlok, and Brittany Matthews, whose assistance and encouragement have made this work possible. My gratitude goes out to my dissertation committee, who have provided invaluable feedback and whose suggestions have significantly improved this project. Thank you for your insights and help Dr. David Zald, Dr. Bunmi Olatunji, and Dr. Brandon Ally—you have made generous contributions with your time, and have been my allies throughout this process, for which I am forever grateful. Finally, I would like to thank Dr. Stephan Heckers, without whose early confidence in me I would never have been able to pursue my true passion. This work was supported by the generous financial support of the National Institute of Mental Health (1F31-MH102008-01, K01-MH083052), the Vanderbilt Institute for Clinical and Translational Research (UL1-TR000445 from NCATS/NIH), a Vanderbilt Graduate School Dissertation Enhancement award, and the Vanderbilt University Institute of Imaging Science. iv TABLE OF CONTENTS Page DEDICATION.................................................................................................................. iii ACKNOWLEDGEMENTS............................................................................................... iv LIST OF TABLES........................................................................................................... v LIST OF FIGURES......................................................................................................... vi LIST OF ABBREVIATIONS........................................................................................... vii CHAPTER I. Introduction.................................................................................................. 1 1.1. The social fearfulness spectrum..................................................... 1 1.2. Evidence for disrupted threat processing in social fear.................. 6 1.3. Faces are salient social cues......................................................... 11 1.4. Novel faces are cues of potential social threat............................... 12 1.5. Habituation as a mechanism for social fearfulness........................ 14 1.6. A social fearfulness network........................................................... 17 1.7. Summary........................................................................................ 19 1.8. Specific aims.................................................................................. 20 II. Associations between social fearfulness and neural response to novel and repeated faces..................................................................................... 23 2.1. Introduction.................................................................................... 23 2.2. Methods......................................................................................... 26 2.2.1. Participants..................................................................... 26 2.2.2. Experimental paradigm................................................... 30 2.2.3. MRI data......................................................................... 31 2.2.4. Regions of interest (ROIs).............................................. 32 2.2.5. Data analysis................................................................... 35 2.3. Results........................................................................................... 38 2.3.1. Arousal/valence ratings................................................... 38 2.3.2. Initial amplitude............................................................... 39 2.3.3. Habituation...................................................................... 39 2.3.4. Laterality.......................................................................... 45 2.4. Discussion...................................................................................... 45 2.5. Conclusions.................................................................................... 55 III. Associations between social fearfulness and functional connectivity during novel and repeated faces................................................................ 57 3.1. Introduction..................................................................................... 57 v 3.2. Methods.......................................................................................... 59 3.2.1. Participants...................................................................... 59 3.2.2. Functional connectivity.................................................... 60 3.2.3. Data analysis................................................................... 60 3.3. Results........................................................................................... 62 3.3.1. Initial connectivity............................................................ 62 3.3.2. Habituation of functional connectivity.............................. 67 3.3.3. Exploratory functional connectivity across regions.......... 68 3.4. Discussion...................................................................................... 70 3.5. Conclusions.................................................................................... 74 IV. Specificity of neural response to faces in social fearfulness........................ 76 4.1. Introduction..................................................................................... 76 4.2. Methods.......................................................................................... 77 4.2.1. Participants...................................................................... 77 4.2.2. Experimental paradigm.................................................... 77 4.2.3. MRI data.......................................................................... 78 4.2.4. Regions of interest (ROIs)............................................... 79 4.2.5. Data analysis................................................................... 79 4.3. Results........................................................................................... 82 4.3.1. Response to objects........................................................ 82 4.3.2. Functional connectivity to objects.................................... 88 4.3.3. Specificity of effects of social stimuli............................... 94 4.4. Discussion...................................................................................... 97 4.5. Conclusions................................................................................. 101 V. Specificity of effects to social fearfulness.................................................. 102 5.1. Introduction.................................................................................. 102 5.2. Methods....................................................................................... 103 5.2.1. Participants................................................................... 103 5.2.2. Data analysis................................................................ 103 5.3. Results........................................................................................ 104 5.3.1. Specificity of associations with social fearfulness......... 104 5.4. Discussion................................................................................... 112 5.5. Conclusions................................................................................. 113 VI. Discussion and future directions............................................................... 115 6.1. Discussion................................................................................... 115 6.2. Clinical implications..................................................................... 125 6.3. Future directions.......................................................................... 126 vi REFERENCES............................................................................................................. 130 vii LIST OF TABLES CHAPTER II Table Page 1. Participant characteristics.......................................................................... 27 2. Correlations between social fearfulness and neural response to faces..... 41 3. Percent signal change by face presentation number................................
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