Current Topics in Behavioral Neurosciences 37 Robert E. Clark Stephen J. Martin Editors Behavioral Neuroscience of Learning and Memory Current Topics in Behavioral Neurosciences Volume 37 Series editors Mark A. Geyer, La Jolla, CA, USA Bart A. Ellenbroek, Wellington, New Zealand Charles A. Marsden, Nottingham, UK Thomas R. E. Barnes, London, UK Susan L. Andersen, Belmont, MA, USA Current Topics in Behavioral Neurosciences provides critical and comprehensive discussions of the most significant areas of behavioral neuroscience research, written by leading international authorities. Each volume offers an informative and contemporary account of its subject, making it an unrivalled reference source. Titles in this series are available in both print and electronic formats. With the development of new methodologies for brain imaging, genetic and genomic analyses, molecular engineering of mutant animals, novel routes for drug delivery, and sophisticated cross-species behavioral assessments, it is now possible to study behavior relevant to psychiatric and neurological diseases and disorders on the physiological level. The Behavioral Neurosciences series focuses on “transla- tional medicine” and cutting-edge technologies. Preclinical and clinical trials for the development of new diagnostics and therapeutics as well as prevention efforts are covered whenever possible. More information about this series at http://www.springer.com/series/7854 Robert E. Clark • Stephen J. Martin Editors Behavioral Neuroscience of Learning and Memory 123 Editors Robert E. Clark Stephen J. Martin University of California San Diego Medical Research Institute School of Medicine Ninewells Hospital and Medical School La Jolla Dundee USA UK and VA Medical Center San Diego USA ISSN 1866-3370 ISSN 1866-3389 (electronic) Current Topics in Behavioral Neurosciences ISBN 978-3-319-78755-8 ISBN 978-3-319-78757-2 (eBook) https://doi.org/978-3-319-78757-2 Library of Congress Control Number: 2018937089 © Springer International Publishing AG 2018 This work is subject to copyright. All rights are reserved by the Publisher, whether the whole or part of the material is concerned, specifically the rights of translation, reprinting, reuse of illustrations, recitation, broadcasting, reproduction on microfilms or in any other physical way, and transmission or information storage and retrieval, electronic adaptation, computer software, or by similar or dissimilar methodology now known or hereafter developed. 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Cover illustration: Artistic representation of oscillatory synchrony and timing of neurons in networks by Gyorgy Buzsaki Printed on acid-free paper This Springer imprint is published by Springer Nature The registered company is Springer International Publishing AG The registered company address is: Gewerbestrasse 11, 6330 Cham, Switzerland Preface Fundamentally, learning can be understood as an experience-based process that acquires or modifies behaviors, knowledge structures, preferences or values. Memory is a closely related concept whereby information that has been learned or “encoded,” is maintained and available to be utilized. Memory, in the colloquial sense, is the type of memory that we are consciously aware of having. These types of memories adorn our mental life. They are the psychological accoutrements of a lifetime of experience. They allow us to recon- struct our past, appreciate our present, and to an extent, predict and control our future. Our memories provide us with a sense of self. They are our connection to others and to our environment. Memories are stored representations of the world and of our self and, as such, they greatly influence how we perceive and interpret our inner and external environments. Yet in actuality, these types of memory make up only a fraction of the stored representations acquired and maintained by the brain. The multiple neuroanatomical regions of the brain support an impressive variety of distinct learning and memory processes; many of these processes are detailed within the chapters of this volume. Learning and memory have been systematically and extensively studied since the pioneering work of Hermann Ebbinghaus (1850–1909) which began in the late 1870s. Presently, an enormous amount of experimental research is directed toward elucidating the neurobiological substrates that support the many forms of learning and memory as well as those cognitive processes that utilize memory. This work includes the evaluation of neural and behavioral plasticity at all levels of analysis from molecular biology to complex forms of human behavior. v vi Preface The volume Behavioral Neuroscience of Learning and Memory represents a broad collection of articles that examine the neurobiological underpinnings of processes that support memory encoding (learning), storage, organization (and reorganization), retrieval, and the utilization of memory for decision-making. The opening chapter provides a brief history of the behavioral neuroscience of learning and memory and a summary of each subsequent chapter. La Jolla, USA Robert E. Clark, Ph.D. Dundee, UK Stephen J. Martin, Ph.D. Contents A History and Overview of the Behavioral Neuroscience of Learning and Memory .................................... 1 Robert E. Clark Current Topics Regarding the Function of the Medial Temporal Lobe Memory System ....................................... 13 Robert E. Clark Neural Activity Patterns Underlying Spatial Coding in the Hippocampus ............................................. 43 Marielena Sosa, Anna K. Gillespie and Loren M. Frank What Versus Where: Non-spatial Aspects of Memory Representation by the Hippocampus ........................... 101 Howard Eichenbaum The Functional and Structural Neuroanatomy of Systems Consolidation for Autobiographical and Semantic Memory .......... 119 Adam J.O. Dede and Christine N. Smith Memory Reconsolidation .................................... 151 Josue Haubrich and Karim Nader The Sensory Neocortex and Associative Memory .................. 177 Dominik Aschauer and Simon Rumpel The Representational Basis of Working Memory .................. 213 Derek Evan Nee and Mark D’Esposito The Neuroscience of Human Decision-Making Through the Lens of Learning and Memory ............................. 231 Lesley K. Fellows Basal Forebrain Cholinergic System and Memory ................. 253 M.G. Blake and M.M. Boccia vii viii Contents Habit Formation and the Striatum ............................. 275 Barbara J. Knowlton and Tara K. Patterson The Anatomy and Physiology of Eyeblink Classical Conditioning ..... 297 Kaori Takehara-Nishiuchi Exploration of the Neurobiological Basis for a Three-System, Multiattribute Model of Memory .............................. 325 Raymond P. Kesner A History and Overview of the Behavioral Neuroscience of Learning and Memory Robert E. Clark Abstract Here, I provide a basic history of important milestones in the develop- ment of theories for how the brain accomplishes the phenomenon of learning and memory. Included are the ideas of Plato, René Descartes, Théodule Ribot, William James, Ivan Pavlov, John Watson, Karl Lashley, and others. The modern era of learning and memory research begins with the description of H.M. by Brenda Milner and the gradual discovery that the brain contains multiple learning and memory systems that are supported by anatomically discrete brain structures. Finally, a brief overview is provided for the chapters that are included in current topics in Behavioral Neuroscience—Learning and Memory. Keywords Plato Á Descartes Á Ribot Á William James Á Ivan Pavlov John Watson Á Karl Lashley Á H.M Á Brenda Milner Contents 1 Multiple Learning and Memory Systems ........................................................................... 6 2 General Overview of the Volume....................................................................................... 8 The only impressions that can be made upon [the brain] are… through the sensory nerve-roots… The currents, once in, must find a way out. In getting out they leave their traces in the paths which they take. The only thing they can do, in short, is to deepen old paths or to make new ones; and the whole plasticity of the brain sums itself up in two words when we call it an organ in which currents pouring in from the sense-organs make with extreme facility paths which do not easily disappear. For, of course, a simple habit, R. E. Clark (&) Veterans Affairs San Diego Healthcare System, San Diego, CA 92161, USA e-mail: [email protected] R. E. Clark Department of Psychiatry, University of California, La Jolla, San Diego, CA 92093, USA © Springer International Publishing AG 2018 Curr Topics Behav Neurosci (2018) 37: 1–11 DOI 10.1007/7854_2017_482 Published Online: 05 January 2018 2 R. E. Clark like every other