The neural mechanisms of recognition memory: an investigation of study and test brain activity and their influence on memory outcomes by Yun Chen A thesis submitted in partial fulfillment of the requirements for the degree of Doctor of Philosophy Centre for Neuroscience University of Alberta ©Yun Chen, 2017 Abstract The ability to remember is fundamental to human cognition. The recognition memory paradigm has been widely used to investigate memory-related processes at both study and test phase. Two types of recognition memory are examined here, item and associative recognition memory. In an item recognition task, participants are instructed to remember a list of items (i.e., A, B, C, D . ), then they are asked to make old-new judgments regarding the items: “probe (B), old or new?” In an associative recognition task, participants are instructed to remember a list of pairs (i.e., A-B, C-D, E-F, . ), then they are asked to make intact-rearranged judgments regarding item-pairs: “probe (C-D), intact or rearranged”. The intact probes are composed of identical pairs from study (A-B), and the rearranged probes are composed of studied items from different study pairs (A-F). With electroencephalographic (EEG) methods, one can identify brain activity related to successful encoding and retrieval. At study, encoding processes are measured by the subsequent memory effect comparing brain activity related to later-remembered and later-forgotten. At test, retrieval processes are measured by the old/new effect comparing brain activity related to correctly identified targets (hits) and correctly identified lures (correct rejections), and the retrieval success effect comparing brain activity related to correctly identified targets (hits) and misidentified targets (misses). The objective of the four studies presented in this dissertation was to examine whether specific brain-activity features reflect recognition-memory encoding and retrieval processes, and to determine whether those features explain individual differences in memory perfor- mance. I measured event-related potentials (ERPs) and oscillatory activity during both study and test phase to explore the neural mechanisms of recognition memory. By using ii an individual-difference approach, one can ask whether these brain-activity measures reflect common or distinct processes. Using the ERP method, prior research has suggested many cognitive processes reflected in memory-related ERP features. Some of those proposed cognitive processes indexed by memory-related ERP features at study resemble other proposed cognitive processes indexed ERP features at test. In the first and the third studies, I asked whether the ERP features during study were functionally correlated with other ERP features during test, and in turn, influence memory performance. Some study ERP features were indeed correlated with test ERP features across participants; however, only a subset of those study-test ERP features explained individual differences in memory performance. Using the oscillation method, prior research has identified changes in theta oscillations (4 − 8 Hz) and alpha oscillations (∼ 10 Hz) to be crucial for memory functioning. In the second and fourth studies, I investigated the function of theta and alpha oscillations during memory encoding and retrieval. The two studies examined whether these oscillations were functionally correlated with the memory-related ERP features, and in turn, influence memory performance. Theta oscillations correlated with memory performance across participants, and while alpha oscillations correlated with ERP measures across participants, but did not explain the individual difference in memory performance. Taking an alternative approach to exploring the functions of brain activity in recognition memory tasks, the studies presented here revealed relationships between ERP features and oscillation measures and their influence on individual memory performance. Although the neural mechanisms for recognition memory are complex, the results suggest a possible uni- fied neural mechanism encompassing both ERP features and oscillations for both item and associative recognition memory. iii Preface This thesis is an original work by Y Chen. All research projects contributing to this work re- ceived ethics approval from the University of Alberta Research Ethics Board. Project Name “Organisation and Retrieval Timecourse of Human Memory”, No. Pro00009760. Chapter 2 of this thesis has been published as Chen, Y.Y., Lithgow, K., Hemmerich, J.A., & Caplan, J.B. (2014). “Is what goes in what comes out? encoding and retrieval event-related poten- tials together determine memory outcome”, Experimental Brain Research (232), 3175–3190. Copyright Springer. Reprinted with permission. Kristie Lithgow was involved with concep- tualization of the study and Jumjury Hemmerich assisted with the data collection. I was responsible for implementing the experimental paradigm, acquiring and analyzing the data and drafting the manuscript. Chapter 3 of this thesis is published as Chen, Y.Y. & Caplan, J.B. (2017), “Rhythmic activity and individual variability in recognition-memory: theta os- cillations correlate with performance whereas alpha oscillations correlate with event-related potentials”, Journal of Cognitive Neuroscience (29), 183–202. Jumjury Hemmerich assisted with the data collection. I was responsible for implementing the experimental paradigm, acquiring and analyzing the data and drafting the manuscript. Chapters 3 and 4 of this thesis have not been published elsewhere. Angela Wan assisted with data collection and I was responsible for implementing the experimental paradigm, acquiring and analyzing the data and drafting the manuscript. In conjunction with my supervisor Jeremy B. Caplan, I was involved in concept formation, data collection, interpretation of the data for all chapters. iv Acknowledgements I am indebted to many people and organizations that made this work of dissertation pos- sible. First, foremost, I would like to express my sincere gratitude to my supervisor, Dr. Jeremy Caplan for his excellent mentorship, immense knowledge, and enormous support. Without his encouragements and guidance, this work would not have been possible. I would like to thank my supervisory committee, Drs. Jacqueline Cummine and Anthony Singhal for their helpful advice and encouragements. I thank my fellow lab members, Leanna Cruik- shank, Sucheta Chakravarty, Yang Liu, Kenichi Kato, Christopher Madan, Ulises Rodriguez and many undergraduate research assistants for their stimulating discussions, supports, and friendships. Special thanks to Kathryn Lambert, Tomi Ann Limcangco and Hanna Warawa for their help during the writing of my thesis. I would also like to acknowledge all the funding supports that made my research possi- ble, Alberta Ingenuity Fund, Canada foundation for innovation (CFI), the Natural Sciences and Engineering Research Council of Canada (NSERC), Neuroscience and Mental Health Institute of the University of Alberta, and University of Alberta International. Last but not the least, I would like to thank my family and friends for supporting me and encouraging throughout my studies. Thank you! v Table of Contents Abstract iii Preface iv List of Tables xii List of Figures xvi List of Abbreviations xvii 1 General Introduction 1 1.1Introduction.................................... 1 1.2Theoreticalperspectivesonrecognitionmemory................ 3 1.2.1 Itemrecognitionmemory......................... 3 1.2.2 Associativerecognitionmemory..................... 5 1.3Investigatingmemory-relatedbrainactivity................... 6 1.3.1 Event-RelatedPotentials......................... 6 1.3.2 Oscillations ................................ 11 1.4 Summary ..................................... 14 1.5Chapteroverview................................. 16 2 Item memory: study and test event-related potentials affect memory out- come 18 2.1Introduction.................................... 20 2.1.1 ERPs at encoding and retrieval ..................... 21 2.1.2 RelatingERPsatencodingtoERPsatretrieval............ 25 2.2Methods...................................... 26 vi 2.2.1 Participants................................ 26 2.2.2 Materials................................. 27 2.2.3 Procedure................................. 27 2.2.4 Electroencephalography (EEG) Recording and Analyses ....... 27 2.3Results....................................... 29 2.3.1 Behavior.................................. 29 2.3.2 ERPs................................... 29 2.3.3 Relationship between encoding and retrieval ERPs .......... 32 2.3.4 Relationship between memory-related ERPs and behavioral measures 35 2.4Discussion..................................... 37 2.5 Conclusion: Implications for interpretating the cognitive meaning of memory- relatedERPs................................... 42 2.6 Robustness to the selection of time windows .................. 42 3 Rhythmic activity and individual variability in item recognition memory 45 3.1Introduction.................................... 47 3.2Methods...................................... 53 3.2.1 Participants................................ 53 3.2.2 Materials................................. 54 3.2.3 Procedure................................. 54 3.2.4 Electroencephalography (EEG) Recording and Preprocessing ..... 55 3.2.5 ERPanalysis............................... 56 3.2.6 Oscillation analysis . ......................... 56 3.3Results....................................... 58 3.3.1 Replication of subsequent memory and retrieval-success