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UC San Diego UC San Diego Electronic Theses and Dissertations Title Associative encoding in episodic memory : binding items across time Permalink https://escholarship.org/uc/item/1f8823rh Author Hales, Jena Bresnihan Publication Date 2011 Peer reviewed|Thesis/dissertation eScholarship.org Powered by the California Digital Library University of California UNIVERSITY OF CALIFORNIA, SAN DIEGO Associative Encoding in Episodic Memory: Binding Items Across Time A Dissertation submitted in partial satisfaction of the requirement for the degree Doctor of Philosophy in Neurosciences by Jena Bresnihan Hales Committee in charge: Professor James B. Brewer, Chair Professor David P. Salmon Professor John T. Serences Professor Larry R. Squire Professor John T. Wixted 2011 Copyright Jena Bresnihan Hales, 2011 All rights reserved. The dissertation of Jena Bresnihan Hales is approved, and is acceptable in quality and form for publication on microfilm and electronically: Chair University of California, San Diego 2011 iii DEDICATION I dedicate this dissertation to my family and friends. To my loving husband Tyler- thank you for your unwavering support and confidence in me and for your endless love and encouragement throughout the last eleven years. To my mom, dad, and sister Ariana - thank you for always believing in me and for your unconditional love and support; despite the distance, I have known that you were here with me every step of the way. To my friends, old and new, near and far- thank you for always being there for me either in person or in spirit. To my friend Jen- thank you for your invaluable advice, love, and friendship over the past few years; Tyler and I feel lucky to have made such lifelong friends as you and Paul. To my undergraduate advisor Seth- thank you for seeing the researcher in me even before I did and for helping me believe that I could achieve whatever I set my mind to. To my labmates- thank you for all of your daily and limitless guidance, support, knowledge, and friendship; you all have made coming to lab each and every day so enjoyable. To Sarah- thank you for taking me under your wing and teaching me so much about science, research, life, and friendship; you have made a permanent impact on my life, and I cannot imagine it without you. To Jim- thank you for taking a chance on a new graduate student coming straight from undergrad with no imaging or programming experience; while I have gained so much knowledge and scientific understanding from working with you over the past five years, I have learned even more about how to be an effective P.I. and successful researcher, for which I am forever grateful. iv TABLE OF CONTENTS Signature Page ..................................................................................... iii Dedication ........................................................................................... iv Table of Contents ................................................................................ v Acknowledgments .............................................................................. vii Vita ...................................................................................................... ix Abstract ............................................................................................... xi Chapter 1: Introduction ....................................................................... 1 Chapter 2: Dissociation of frontal and medial temporal lobe activity in maintenance and binding of sequentially presented paired associates ................................................................................ 16 Chapter 3: Activity in the hippocampus and neocortical working memory regions predicts successful and associative memory for temporally discontiguous events ....................................... 39 Chapter 4: The timing of associative memory formation: frontal lobe and anterior medial temporal lobe activity at associative binding predicts memory ………………................................ 64 Chapter 5: The path to memory is guided by strategy: distinct networks are engaged in associative encoding under visual and verbal strategy and influence memory performance in healthy and impaired individuals …........................................ 92 Chapter 6: Distinct parietal and frontal contribution to sequential v object-location associative encoding ….…............................. 116 Chapter 7: Conclusions ....................................................................... 127 Tables .................................................................................................. 132 Figures ................................................................................................. 141 References ............................................................................................ 162 vi ACKNOWLEDGMENTS I would like to acknowledge Dr. James Brewer for his invaluable support and guidance throughout graduate school and for being the chair of my dissertation committee. Additionally, I would like to acknowledge Drs. David Salmon, John Serences, Larry Squire, and John Wixted for the guidance and wisdom they have shared with me. I would also like to acknowledge the members of the Human Memory Laboratory, Sarah Gimbel, Tyler Seibert, Elizabeth Murphy, Emilie Schwager, and Erik Kaestner, for their endless support, constant guidance, and lasting friendship. Chapter 2, in full, is a reprint of the material as it appears in Journal of Cognitive Neuroscience, 2009. Hales, Jena B.; Israel, Sarah L.; Swann, Nicole C.; Brewer, James B. The dissertation author was the primary investigator and author of this paper. Chapter 3, in full, is a reprint of the material as it appears in Neuropsychologia, 2010. Hales, Jena B.; Brewer, James B. The dissertation author was the primary investigator and author of this paper. Chapter 4, in full, is a reprint of the material as it appears in Journal of Neurophysiology, 2011. Hales, Jena B.; Brewer, James B. The dissertation author was the primary investigator and author of this paper. Chapter 5, in full, is a reprint of the material as it was submitted for consideration for publication. Hales, Jena B.; Brewer, James B. The dissertation author was the primary investigator and author of this paper. vii Chapter 6, in full, is a reprint of the material as it was submitted for consideration for publication as a brief communication. Hales, Jena B.; Brewer, James B. The dissertation author was the primary investigator and author of this paper. This work was supported by the National Institute of Neurological Disorders and Stroke NINDS K23 NS050305, the General Electric Medical Foundation, and the University of California, San Diego Departments of Neurosciences and Radiology. JBH was supported by the National Science Foundation through the Graduate Research Fellowship Program. viii VITA 2006 Bachelor of Arts, Bowdoin College 2008 Master of Science, University of California, San Diego 2011 Doctor of Philosophy, University of California, San Diego PUBLICATIONS Hales, J. B., & Brewer, J. B. The path to memory is guided by strategy: distinct networks are engaged in associative encoding under visual and verbal strategy and influence memory performance in healthy and impaired individuals. (In review). Hales, J. B., & Brewer, J. B. Distinct parietal and frontal contributions to sequential object-location associative encoding. (In review). Schwager, E.T., Gimbel, S.I., Hales, J. B., & Brewer, J. B. Search-related suppression of hippocampus and default network activity during associative memory retrieval. (In review). Hales, J. B., & Brewer, J. B. (2011). The timing of associative memory formation: Frontal lobe and anterior medial temporal lobe activity at associative binding predicts memory. Journal of Neurophysiology, 105(4), 1454-1463. Hales, J. B., & Brewer, J. B. (2010). Activity in the hippocampus and neocortical working memory regions predicts successful associative memory for temporally discontiguous events. Neuropsychologia, 48(11), 3351-3359. Hales, J. B., Israel, S. L., Swann, N. C., & Brewer, J. B. (2009). Dissociation of frontal and medial temporal lobe activity in maintenance and binding of sequentially presented paired associates. Journal of Cognitive Neuroscience, 21(7), 1244-1254. Ramus, S. J, Davis, J. B., Donahue, R. J., Discenza, C. B., & Waite, A. A. (2007). Interactions between the orbitofrontal cortex and the hippocampal memory system during the storage of long-term memory. Annals of the New York Academy of Sciences, 1121, 216-231. *Name change from Jena Bresnihan Davis to Jena Bresnihan Hales ix RESEARCH EXPERIENCE 2005-2006 Department of Psychology , Bowdoin College Advisor: Dr. Seth Ramus 2006-2011 Department of Neuroscience, University of California, San Diego Advisor: Dr. James Brewer x ABSTRACT OF THE DISSERTATION Associative Encoding in Episodic Memory: Binding Items Across Time by Jena Bresnihan Hales Doctor of Philosophy in Neurosciences University of California, San Diego, 2011 Professor James B. Brewer, Chair As individuals navigate the world, they encounter a constant stream of stimuli, some of which are important to attend to, encode, and associate with other stimuli separated in time. How does the brain attempt to form and succeed in forming associative memories for temporally-discontiguous stimuli? Does using different associative strategies influence which brain regions are engaged in encoding, and could this have clinical implications for potential treatment approaches in patients with neurological damage