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Assessing Neuronal Synchrony and Brain Function Through Local Field Potential and Spike Analysis Samuel Stuart Mcafee University of Tennessee Health Science Center

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Assessing Neuronal Synchrony and Brain Function Through Local Field Potential and Spike Analysis Samuel Stuart Mcafee University of Tennessee Health Science Center University of Tennessee Health Science Center UTHSC Digital Commons Theses and Dissertations (ETD) College of Graduate Health Sciences 12-2017 Assessing Neuronal Synchrony and Brain Function Through Local Field Potential and Spike Analysis Samuel Stuart McAfee University of Tennessee Health Science Center Follow this and additional works at: https://dc.uthsc.edu/dissertations Part of the Medical Neurobiology Commons Recommended Citation McAfee, Samuel Stuart (http://orcid.org/0000-0003-4121-0592), "Assessing Neuronal Synchrony and Brain Function Through Local Field Potential and Spike Analysis" (2017). Theses and Dissertations (ETD). Paper 448. http://dx.doi.org/10.21007/ etd.cghs.2017.0445. This Dissertation is brought to you for free and open access by the College of Graduate Health Sciences at UTHSC Digital Commons. It has been accepted for inclusion in Theses and Dissertations (ETD) by an authorized administrator of UTHSC Digital Commons. For more information, please contact [email protected]. Assessing Neuronal Synchrony and Brain Function Through Local Field Potential and Spike Analysis Document Type Dissertation Degree Name Doctor of Philosophy (PhD) Program Biomedical Sciences Track Neuroscience Research Advisor Detlef H. Heck, Ph.D. Committee Max L. Fletcher, Ph.D. Robert C. Foehring, Ph.D. Shalini Narayana, Ph.D. Robert J. Ogg, Ph.D. ORCID http://orcid.org/0000-0003-4121-0592 DOI 10.21007/etd.cghs.2017.0445 This dissertation is available at UTHSC Digital Commons: https://dc.uthsc.edu/dissertations/448 Assessing Neuronal Synchrony and Brain Function Through Local Field Potential and Spike Analysis A Dissertation Presented for The Graduate Studies Council The University of Tennessee Health Science Center In Partial Fulfillment Of the Requirements for the Degree Doctor of Philosophy From The University of Tennessee By Samuel Stuart McAfee December 2017 Portions of Chapter 5 © 2016 by Elsevier BV. Portions of Chapter 5 © 2017 by Nature Publishing Group. Copyright © 2017 by Samuel Stuart McAfee. All rights reserved. ii DEDICATION To my family and friends, who are entirely excellent. To my beautiful wife, Gal, for her endless love and support. And to my dog, Bucky, for being a good boy. iii ACKNOWLEDGEMENTS First and foremost, I would like to thank my advisor, Dr. Detlef Heck, and all of our lab members for their invaluable help and guidance throughout the course of this project. In particular, I would like to thank Dr. Heck for offering me endless encouragement to discover which questions I was most interested in, and the freedom to find the answers in my own way. Thank you Dr. Yu Liu, for your patience and diligence every day, and for teaching me how to perform experiments properly. And lastly, thank you Shuhua Qi for being so helpful and making sure we always had the right tools at hand. I would also like to thank the members of my graduate committee for their help in focusing my project: Dr. Robert Foehring, Dr. Robert Ogg, Dr. Shalini Narayana, and Dr. Max Fletcher. Additionally I would like to thank the Neuroscience Institute for its generous support with my graduate fellowship. Lastly, I would like to thank the students within the graduate program for being a constant source of support, curiosity, and constructive criticism. I would like to offer a special thanks in that regard to Kevin Hope, Matthew Kirchner, Zachary Goldsmith, and Cameron Ogg. iv ABSTRACT Studies of neuronal network oscillations and rhythmic neuronal synchronization have led to a number of important insights in recent years, giving us a better understanding of the temporal organization of neuronal activity related to essential brain functions like sensory processing and cognition. Important principles and theories have emerged from these findings, including the communication through coherence hypothesis, which proposes that synchronous oscillations render neuronal communication effective, selective, and precise. The implications of such a theory may be universal for brain function, as the determinants of neuronal communication inextricably shape the neuronal representation of information in the brain. However, the study of communication through coherence is still relatively young. Since its articulation in 2005, the theory has predominantly been applied to assess cortical function and its communication with downstream targets in different sensory and behavioral conditions. The results herein are intended to bolster this hypothesis and explore new ways in which oscillations coordinate neuronal communication in distributed regions. This includes the development of new analytic tools for interpreting electrophysiological patterns, inspired by phase synchronization and spike train analysis. These tools aim to offer fast results with clear statistical and physiological interpretation. v TABLE OF CONTENTS CHAPTER 1. INTERPRETATION AND SIGNIFICANCE OF ELECTROPHYSIOLOGICAL RECORDINGS ............................................................1 Purpose .............................................................................................................................1 Historical Context ............................................................................................................1 The Microelectrode Recording ........................................................................................3 Determining Spike Times ............................................................................................3 Pre-processing the Local Field Potential (LFP) Record ..............................................5 Significance of LFP Oscillations .....................................................................................5 The Spectrum of LFP Oscillations...................................................................................6 Delta Oscillations .........................................................................................................8 Theta Oscillations ........................................................................................................8 Alpha Oscillations ........................................................................................................9 Beta Oscillations ..........................................................................................................9 Gamma Oscillations ...................................................................................................10 The Role of Oscillations in Cortical Information Processing ........................................12 Coherent Oscillations and Inter-Neuronal Transmission ...........................................12 Parallel Streams of Coherent Neuronal Communication ...........................................16 Cross-Frequency Coupling ........................................................................................16 Conclusion .....................................................................................................................16 Overview of Following Chapters ...................................................................................18 CHAPTER 2. DEVELOPMENT OF NOVEL METHODS FOR ASSESSING NEURONAL SYNCHRONY AND BRAIN FUNCTION THROUGH LFP AND SPIKE ANALYSIS ..........................................................................................................19 Purpose ...........................................................................................................................19 LFP Frequency, Phase and Amplitude Estimation ........................................................19 Oscillation Parameters in Context .................................................................................20 The Synchronization Metric r and Its Statistical Evaluation .........................................22 Parametric Statistical Tests Using the r Value ..........................................................23 Evaluation of Binned Test Sensitivity and Accuracy ................................................28 Application to LFP Phase Synchronization Analysis ................................................28 Oscillatory Changes in Spike Synchrony ......................................................................31 Creating the Spike Synchrony Function ....................................................................31 Statistical Evaluation of Rhythmic Spike Synchrony and CTC ................................34 Phase-Relationship Tuning of Spike Activity ...............................................................37 Phase-Amplitude Coupling ............................................................................................39 Conclusion .....................................................................................................................41 CHAPTER 3. SYNCHRONOUS OSCILLATIONS AND THALAMOCORTICAL TRANSMISSION IN THE MOUSE VISUAL SYSTEM ...........................................................................................................................42 Purpose ...........................................................................................................................42 Overview of Study .........................................................................................................42 vi Introduction ....................................................................................................................42 Methods .........................................................................................................................44 Animals ......................................................................................................................44
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