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Neural Mechanisms of Hippocampal Place Cell Sequences

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Neural Mechanisms of Hippocampal Place Cell Sequences NEURAL MECHANISMS OF HIPPOCAMPAL PLACE CELL SEQUENCES by Ting Feng A dissertation submitted to Johns Hopkins University in conformity with the requirements for the degree of Doctor of Philosophy Baltimore, Maryland December, 2015 © 2015 Ting Feng All Rights Reserved Abstract The hippocampus is important for learning and memory. Specifically, a type of pyramidal neuron in the rodent hippocampus, namely the “place cell”, encodes the current location of the animal in space. Sequential activations of hippocampal place cells occurs when the animal is under active exploration (theta sequence), and during the animal’s quiet immobility or sleep (hippocampal replay). These hippocampal place cell sequences have been proposed as fundamental neural substrates of learning and memory, because they carry precise temporal coordination between individual neurons. However, the mechanisms contributing to their development with experience have not been well understood. To address this gap in knowledge, we applied high-density electrophysiological recording techniques to simultaneously monitor the activities of hundreds of hippocampal place cells, and compared neuronal activities before and after, or between early and late experiences, while the animal explored a novel environment. I found that both theta sequences and hippocampal replay emerged immediately after the first experience, and were absent prior to that. In contrast, the activities of individual place cells advanced to earlier phases of hippocampal theta rhythm (the phenomenon of “phase precession”) independently with experience, and only became synchronized and formed temporally coordinated sequential activities after the first running experience. Further, the hippocampal replays, once developed, were continuously modulated by individual experiences, where the propagation speed of their represented spatial trajectories slowed down with learning. Examination of hippocampal replays in a fine temporal scale revealed that their spatial representations were discretized in alternating stages of static representation and rapid movement, and phase-locked to the slow-gamma rhythm. The change of the propagation speed of replay was reflected by an increased number of discrete alternating stages in the represented trajectory, ii accompanied by an increase in duration of the static representations, and a decrease of the duration of the rapid movements. In conclusion, hippocampal place cell sequences undergo rapid plasticity with experience, which involves synchronization between individual neurons, and a dynamic change in the content of spatial information represented by the place cell sequences. Thesis Committee David J. Foster, Ph.D. (Advisor, Reader) Marshall G. Hussain Shuler, Ph.D. (Second reader) James J. Knierim, Ph.D. Kechen Zhang, Ph.D. iii Preface and Acknowledgements First I would like to thank you for your interest in reading my dissertation. This dissertation contains five years of my work as a PhD student, where I investigated the cognitive function of learning and memory in the brain area of hippocampus by studying a particular type of neuron – “hippocampal place cell”, and by examining the relationship of spike timing between different neurons via high density in-vivo electrophysiology techniques in behaving rodents. I included three of my projects in separate chapters, the contents of which come from two published papers (chapter 3 – Journal of Neuroscience 2015, chapter 4 – Nature Neuroscience 2015; see Curriculum Vitae) and a manuscript in preparation (chapter 5). Words cannot express my gratitude for those who helped me along my way to complete the PhD degree. I would like to first thank my thesis advisor, Dr. David Foster, who introduced me to the world of place cells and directed me step by step to exciting discoveries. I would like to thank all my thesis committee members, Dr. James Knierim, Dr. Marshall Shuler and Dr. Kechen Zhang, who gave valuable suggestions to my research and ensured that I was in good standing with my progress every year. I would like to thank all my lab mates for their tremendous support, especially Dr. Delia Silva, who collaborated with me on the Nature Neuroscience publication. I would also like to thank accompanies of my friends in the Neuroscience department and the Johns Hopkins Chinese community through my six years in Baltimore. Finally, I would not succeed without my beloved family: special regards here to my parents Mr. Chaozhang Feng, Ms. Dexiu Zeng and my husband Dr. Gerald Sun. iv Table of Contents Abstract ........................................................................................................................................... ii Preface and Acknowledgements .................................................................................................... iv List of Figure.................................................................................................................................. ix Chapter 1 — Background ............................................................................................................... 1 1.1 Learning, memory and synaptic plasticity ............................................................................ 1 1.2 The function and anatomy of hippocampus .......................................................................... 3 1.3 Hippocampal place cells ....................................................................................................... 6 1.4 Hippocampal place cell sequences ...................................................................................... 10 1.4.1 Hippocampal theta sequences ...................................................................................... 12 1.4.2 Hippocampal replay ..................................................................................................... 15 Chapter 2 — General Methodology .............................................................................................. 21 2.1 Experiment protocol and subjects ....................................................................................... 22 2.2 Surgery and data acquisition ............................................................................................... 23 2.3 Position reconstruction from activity of hippocampal place cells ...................................... 24 2.4 Analysis of place cell sequences ......................................................................................... 26 2.5 Analysis of Local Field Potentials ...................................................................................... 27 Chapter 3 — Dissociation between the experience-dependent development of hippocampal theta sequences and single-trail phase precession ................................................................................. 29 3.1 Introduction ......................................................................................................................... 29 v 3.2 Methods............................................................................................................................... 31 3.2.1 Subjects and experiment overview .............................................................................. 31 3.2.2 Quantification methods for theta sequences ................................................................ 32 3.2.3 Quantifications of individual neuronal phase precessions ........................................... 35 3.3 Results ................................................................................................................................. 36 3.3.1 Individual theta sequences and single-lap phase precession........................................ 40 3.3.2 Theta sequence structure emerged rapidly after experience on a novel track ............. 41 3.3.3 Individual place fields demonstrated strong phase precession on the first experience on a novel track .......................................................................................................................... 55 3.3.4 The phase offset of phase precession became more synchronized among individual neurons after the first experience on novel track .................................................................. 60 3.4 Discussion ........................................................................................................................... 65 Chapter 4 — Trajectory events across hippocampal place-cells require previous experience ..... 71 4.1 Introduction ......................................................................................................................... 71 4.2 Methods............................................................................................................................... 73 4.2.1 Subjects and experiment overview .............................................................................. 73 4.2.2 Quantification of place fields and position reconstruction .......................................... 73 4.2.3 Place cell ensemble activity analysis ........................................................................... 74 4.3 Results ................................................................................................................................. 78 4.3.1 Absence of temporally sequenced events prior to experience ..................................... 79 vi 4.3.2 Trajectory events observed after experience ................................................................ 89 4.4 Discussion ..........................................................................................................................
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