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Relations between the theta rhythm and activity patterns of hippocampal neurons. Item Type text; Dissertation-Reproduction (electronic) Authors Skaggs, William E. Publisher The University of Arizona. Rights Copyright © is held by the author. Digital access to this material is made possible by the University Libraries, University of Arizona. Further transmission, reproduction or presentation (such as public display or performance) of protected items is prohibited except with permission of the author. Download date 11/10/2021 10:14:49 Link to Item http://hdl.handle.net/10150/187234 INFORMATION TO USERS This manuscript ,has been reproduced from the microfilm master. UMI films the text directly from the original or copy submitted. Thus, some thesis and dissertation copies are in typewriter face, while others may be from any type of computer printer. The quality of this reproduction is dependent upon the quality of the copy submitted. 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Contact UMI directly to order. UMI A Bell & Howell InformatIon Company 300 North Zeeb Road. Ann Arbor. MI4S106-1346 USA 313/761-4700 800:521-0600 RELATIONS BETWEEN THE THETA RHYTHM AND ACTIVITY PATTERNS OF HIPPOCAMPAL NEURONS by William Skaggs A Dissertation Submitted to the Faculty of the PROGRAM IN NEUROSCIENCE In Partial Fulfillment of the Requirements For the Degree of DOCTOR OF PHILOSOPHY In the Graduate College THE UNIVERSITY OF ARIZONA 1 995 UMI Number: 9603381 OMI Microform 9603381 Copyright 1995, by OMI Company. All rights reserved. This microform edition is protected against unauthorized copying under Title 17, United States Code. UMI 300 North Zeeb Road Ann Arbor, MI 48103 2 THE UNIVERSITY OF ARIZONA GRADUATE COLLEGE As members of the Final Examination Committee, we certify that we have read the dissertation prepared bY~W~i~1~1~1~·a~m~E~.~S~k~a~g~g~s~ ___________________ entitled Relations between the theta rhythm and ~ctiYity patterns of hippocampal neurons and recommend that it be accepted as fulfilling the dissertation requirement for the Degree of __~P~h~.~D~. __________________________________ _ J~ S-- JD - ,J- Date S/3U/7f Date 7 Date Date Final approval and acceptance of this dissertation is contingent upon the candidate's submission of the final copy of the dissertation to the Graduate College. I hereby certify that I have read this dissertation prepared under my direction and recommend that it be accepted as fulfilling the dissertation requirement. ~~ 3 STATEMENT BY AUTHOR This dissertation has been submitted in partial fulfillment of requirements for an advanced degree at The University of Arizona and is to be deposited in the University Library to be made available to borrowers under the rules of the Library. Brief quotations from this dissertation are allowable without special permission, provided that accurate acknowledgement of source is made. Requests for permission for extended quotation from or reproduction of this manuscript in whole or in part may be granted by the head of the major department or the Dean of the Graduate College when in his or her judgement the proposed use of the material is in the interests of scholarship. In all other instances, however, permission must be obtained from the author. 4 ACKNOWLEDGEMENTS Nobody ever makes it through to a Ph.D. without a lot of help, but I feel as though I have been helped more than most. My greatest debt is certainly to Bruce McN aughton and Carol Barnes, for taking me into their lab in Boulder and guiding me through my graduate career, giving me equipment, data, space, and rats, as well as plenty of financial and sometimes emotional support. I also owe a great debt to Art Winfree, for giving me a way to make the transition from mathematics to b.iology, along with a wonderful example of how to do science with esprit and elan. Several people have kindly permitted me to make use of data they collected in the course of their own experiments. For this I thank Matt Wilson, Jim Knierim, Kati Gothard, Bruce McNaughton, and Carol Barnes. For excellent technical support, including design and construction of hardware and software, and help with running animals, I am grateful to Matt Wilson, Casey Stengel, Michael Williams, Kevin Moore, Chris Duffield, Matt Suster, Rowena D'Monte, and Loren Frank. If not for the help of Luann Synder in the final stages, I would probably not ever have come to the end of this. For helpful discussions, and critical reading of earlier versions of portions of this dissertation, I give thanks to, in no particular order: Patrick Lynn, Brian Leonard, Audrey Guzik, Cindy Erickson, Misha Tsodyks, Kati Gothard, Jim Knierim, Gyuri Buzsaki, Jay McClelland, Neil Burgess, John O'Keefe, Iris Ginzburg, Mayank Mehta, Terry Sejnowski, Hemant Kudrimoti, Yulin Qin, Bin Shen, and of course to the members of my committee. Perhaps more important than anything else are the people who have made it all seem worth the effort with their unwavering support and encouragement, including especially my mother and father, brother Matt, sister Melanie, and brother-in-law Ken. Portions of chapters 2 and 11 are derived from manuscripts written together with Bruce McNaughton; our individual contributions are too intertwined to distinguish at this point. The rest of this dissertation is entirely my own writing, except for brief quotations identified as such. The chapter-heading quotations are all from Lewis Carroll's "The Hunting of the Snark"; they are taken from the Internet edition transcribed under the auspices of Project Gutenberg. 5 TABLE OF CONTENTS LIST OF FIGURES 9 ABSTRACT .... 12 CHAPTER 1: INTRODUCTION. 14 CHAPTER 2: THE HIPPOCAMPUS AND MEMORY . 22 2.1 Overview..................... 26 2.2 An Architecture for Autoassociation ..... 32 2.3 Selection of a Hippocampal Representation . 40 2.4 The Problem of Time. 42 2.4.1 The theta cycle is too short . 44 2.4.2 The theta cycle is too long 45 2.4.3 Resolution? 47 2.5 Conclusions . 48 2.5.1 The possibility of other hippocampal functions . 49 CHAPTER 3: ANATOMICAL ORGANIZATION OF HIPPOCAMPAL CIR- CUlTS. 50 3.1 Overall structure ........ 51 3.2 Cells and Local Connections . 53 3.2.1 The Entorhinal Cortex 56 3.2.2 The Fascia Dentata . 57 3.2.3 CA3 61 3.2.4 CAl 62 3.2.5 The Subiculum . 63 6 3.2.6 The Presubiculum and Parasubiculum . 64 3.2.7 Subcortical projections . 65 3.3 Septum ...'............,... 67 3.3.1 Septo-hippocampal connections . 69 3.3.2 The supramammillary nucleus and posterior hypothalamus 71 CHAPTER 4: FIRING CORRELATES OF HIPPOCAMPAL CELLS. 73 4.1 Behavioral correlates of CAl and CA3 pyramidal cells. 75 4.1.1 General features of CAl and CA3 place-related firing 78 4.1.2 Sensory control of place-related firing . 82 4.1.3 Task dependence of pyramidal cell firing . 90 4.1.4 Development and evolution of place fields. 92 4.1.5 Directionality................ 94 4.1.6 Non-place-related correlates of complex spike cell activity. 95 4.1. 7 Topography of the hippocampal "map" 97 4.1.8 Summary............... 98 4.2 Behavioral correlates of dentate granule cells 101 4.3 Behavioral correlates of theta cells ..... 102 4.4 Place specificity of entorhinal unit activity 104 4.5 Conclusions . 106 CHAPTER 5: THE HIPPOCAMPAL THETA RHYTHM 108 5.1 Overview.... 109 5.2 Technical issues 111 5.3 Location of the pacemaker for theta . 112 5.4 A brief history. 115 5.5 Two types of theta . 120 5.6 Generators of theta . 122 5.6.1 The relationship between generators and amplitude maxima 124 5.7 Relations between hippocampal theta and movement 129 5.8 Theta in hippocampal slices . 134 7 5.9 Hippocampal unit activity in relation to theta . .. 135 5.10 Medial septum ..................... 139 5.11 The supramammillary areal posterior hypothalamus 141 5.12 Pharmacology of theta . 145 5.12.1 Acetylcholine 145 5.12.2 GABA .. 147 5.12.3 Serotonin. 148 5.12.4 Dopamine 150 5.12.5 Norepinephine .. 150 5.12.6 Glutamate .......... 150 5.13 The 7.7 Hz Minimum for Septal Driving of Theta 151 5.14 Species Differences .. 154 5.15 A hypothetical model. 155 5.16 Theta and learning .. 157 CHAPTER 6: RECORDING METHODS 160 6.0.1 Quantification of theta rhythm .. 166 6.1 Spatial firing measures . 169 CHAPTER 7: RELATIONS BETWEEN THE THETA RHYTHM AND SPATIAL FIRING OF CAl COMPLEX SPIKE CELLS ...... 171 7.1 Theta modulation of complex spike cell population activity. 171 7.2 The O'Keefe-Reece phase precession effect . 175 7.3 Two-dimensional environments 184 7.4 Summary and Conclusions . 193 CHAPTER 8: INTERACTIONS BETWEEN THETA AND ACTIVITY OF DENTATE GRANULE CELLS . 196 8.1 Criteria for identifying granule cells .. 197 8.2 Results... 200 8.3 Theta cells.
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