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CHOLINERGIC MODULATION of the SUPERFICIAL LAYERS of the PARASUBICULUM Stephen D. Glasgow a Thesis in the Department of Psycholo

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CHOLINERGIC MODULATION of the SUPERFICIAL LAYERS of the PARASUBICULUM Stephen D. Glasgow a Thesis in the Department of Psycholo CHOLINERGIC MODULATION OF THE SUPERFICIAL LAYERS OF THE PARASUBICULUM Stephen D. Glasgow A Thesis in the Department of Psychology Presented in Partial Fulfillment of the Requirements for the Degree of Doctorate of Philosophy at Concordia University Montréal, Québec January, 2011 © Stephen D. Glasgow, 2011 CONCORDIA UNIVERSITY SCHOOL OF GRADUATE STUDIES This is to certify that the thesis prepared By: Stephen D. Glasgow Entitled: Cholinergic modulation of the superficial layers of the parasubiculum and submitted in partial fulfillment of the requirements for the degree of DOCTOR OF PHILOSOPHY (Psychology) complies with the regulations of the University and meets the accepted standards with respect to originality and quality. Signed by the final examining committee: Dr. J. Turnbull Chair Dr. S. Williams External Examiner Dr. R. Courtemanche External to Program Dr. D. Mumby Examiner Dr. W. Brake Examiner Dr. C. A. Chapman Thesis supervisor Approved by Dr. C. A. Chapman, Graduate Program Director Brian Lewis, Dean of Arts & Sciences ABSTRACT Cholinergic modulation of the superficial layers of the parasubiculum Stephen D. Glasgow, Ph.D. Concordia University, 2011 Recent evidence suggests that the parahippocampal area, including the entorhinal cortex and parasubiculum, may play a crucial role in spatial processing and memory formation. However, little is known about the basic cellular and network properties of the parasubiculum, an isocortical brain region that receives input from the hippocampus and other subcortical regions associated with spatial navigation, and projects exclusively to the superficial layers of the entorhinal cortex. Neurons in layer II of the parasubiculum demonstrate theta-frequency membrane potential oscillations at near-threshold voltages that are generated via an interplay between a persistent Na+ current and the hyperpolarization-activated cationic current Ih, and these rhythmic fluctuations in membrane potential may contribute to the generation of oscillatory local field potentials. Further, the parasubiculum receives strong cholinergic projections from the medial septum. Acetylcholine has been linked to theta-frequency oscillations via regulation of cellular and network dynamics through membrane depolarization, while concurrently suppressing excitatory synaptic transmission, and it is likely that cholinergic receptor activation has similar effects in the parasubiculum. I found that activation of cholinergic receptors depolarizes layer II cells of the + parasubiculum by exerting numerous effects on K channels, including IM and IKir, however also suppresses incoming excitatory synaptic transmission from the iii CA1. These results indicate that increases in cholinergic tone during network- level theta-frequency oscillations in the parasubiculum may increase neuronal excitability by exerting strong effects on postsynaptic conductances, but may also regulate network dynamics by reducing the strength of incoming afferents. iv ACKNOWLEDGEMENTS This dissertation represents the culmination of years of work, and is by far the most challenging endeavor I have ever undertaken. It would not have been possible without the immeasurable aid from countless people. First and foremost, I would like to express my infinite gratitude to my supervisor and mentor, C. Andrew Chapman. His knowledge, understanding, and patience have been crucial to the completion of this thesis, and he has helped shape my thinking as a research scientist, as an electrophysiologist, and as an individual. To my committee members, Drs. Wayne Brake and David Mumby, thank you for your erudite feedback and insightful discussions regarding my dissertation. I would also like to thank everyone at the Center for Studies in Behavioral Neurobiology for their limitless support and guidance throughout my graduate training, and everyone from Dr. Chapman’s lab, with specific thanks to Iulia Glovaci and Lila Karpowicz. Your assistance and dedication with experiments included in this dissertation are very much appreciated, and without your help, this would not have been possible. I have many people to thank for their support during the completion of my doctoral work, and preparation of my dissertation. Most importantly, to my mother, Susan Glasgow, this would not have been possible without your belief in me, and for that, I am forever indebted. Your tireless support of me through these many years of schooling are more than any son could ever hope for. To my sisters, Jennifer and Margaret Glasgow, thank you so much for your unwavering support. To Emilie Desclos-Beaudin, thank you for all the support v that you’ve shown, and everything that you have done (including listening to countless hours of my science ramblings). You have made this massive undertaking seem so much easier. I would also like to extend gratitude to my friends who were incredibly supportive of my work from the very beginning. The research reported in this dissertation was supported by grants to Stephen Glasgow and C. Andrew Chapman from the Natural Sciences and Engineering Research Council of Canada. C. Andrew Chapman also received funds that contributed to this work from the Canada Foundation for Innovation. Dr. Chapman is also a member of the Center for Studies in Behavioral Neurobiology funded by the Fonds pour Récherche en Santé du Québec. vi TABLE OF CONTENTS Page Contribution of Authors . x List of Figures . xii List of Abbreviations .. xiv Chapter 1 __________________________________________________ 1 PART I. THE PARASUBICULUM AND ACETYLCHOLINE: AN OVERVIEW .......................................................... 1 PART II. CONNECTIONS OF THE PARASUBICULUM AND ASSOCIATED REGIONS .. 13 2.1. General Anatomy and Physiology ..... 13 2.2. Cytoarchitectonics of the hippocampal formation ... 14 2.3. Connections of the hippocampal formation ..... 18 2.4. Entorhinal cortex as an interface for the hippocampal formation .... 20 2.5 Anatomy and Physiology of the parasubiculum ... 23 2.6. Efferent intrahippocampal connections of the parasubiculum . 25 2.7. Afferent intrahippocampal connections of the parasubiculum . 28 2.8. Extrahippocampal connections of the parasubiculum . 29 PART III. THE PARASUBICULUM AND SPATIAL PROCESSING ..... 35 3.1. Effects of parasubicular damage on spatial behavior .... 36 3.2. Place-dependent cell firing in the hippocampal formation ....... 41 3.3. Cholinergic modulation of theta-frequency activity in the parasubiculum ....... 48 PART IV. SUMMARY OF EXPERIMENTAL CHAPTERS .............. 60 Chapter 2 __________________________________________________ 64 ABSTRACT 65 INTRODUCTION .. 66 METHODS . 70 Slice preparation .................................................................... 70 Whole cell recording .... 71 vii Pharmacological manipulations ................ 72 Analysis ................................................................................. 73 RESULTS ... 74 Oscillations are Dependent on Sodium Currents . 75 Oscillations do not Require Ca2+ Currents ............................. 76 Potassium currents ................................................................ 77 Hyperpolarization-activated current Ih .................................... 79 DISCUSSION . 81 Conductances generating oscillations ..................... 83 Extrinsic mechanisms contributing to theta activity . 88 Chapter 3 __________________________________________________ 104 ABSTRACT . 105 INTRODUCTION 107 METHODS .. 111 Slice preparation .................................................................... 111 Electrophysiological recordings and data analysis ............. 112 Immunohistochemistry ......................................... 116 Pharmacological manipulations ............................................. 117 RESULTS 118 Properties of morphologically identified stellate and pyramidal neurons . 119 Cholinergic modulation of layer II parasubicular neurons ...... 122 Cholinergic depolarization is not mediated by changes in synaptic inputs . 126 Carbachol-induced depolarization is dependent on M1 receptors ..... 127 Cholinergic depolarization is mediated by IM and an additional K+ conductance ..... 128 Carbachol induces a Ba2+-sensitive potassium conductance ... 132 Carbachol blocks an outward K+ conductance .... 132 DISCUSSION . 133 Layer II parasubicular neurons show electrophysiological homogeneity despite morphological differences .. 135 Cholinergic modulation of layer II parasubicular neurons is dependent on muscarinic receptors ................................... 137 Cholinergic modulation of ion channels associated with passive cell properties ............ 138 Conductances mediating cholinergic depolarization of layer II parasubicular neurons 142 viii Functional implications .......................................................... 146 Chapter 4 __________________________________________________ 169 ABSTRACT . 170 INTRODUCTION 171 METHODS .. 176 Slice preparation .................................................................... 176 Stimulation and recording ........................................ 177 Data analysis ............................................. 180 RESULTS 180 DISCUSSION . 188 Carbachol-induced suppression is not due to increased inhibitory tone . 189 Carbachol-induced suppression is mediated by M1 Receptors .. 190 Cholinergic suppression of presynaptic glutamate release .... 192 Functional significance ............ 197 Chapter 5 __________________________________________________ 212 Summary of major findings .. 214 Ionic conductances that mediate
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