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Neural Correlates of Directional Hearing Following Noise-Induced Hearing Loss in The Neural Correlates of Directional Hearing following Noise-induced Hearing Loss in the Inferior Colliculus of Dutch-Belted Rabbits A dissertation presented to the faculty of the College of Arts and Sciences of Ohio University In partial fulfillment of the requirements for the degree Doctor of Philosophy Hariprakash Haragopal August 2020 © 2020 Hariprakash Haragopal. All Rights Reserved. 2 This dissertation titled Neural Correlates of Directional Hearing following Noise-induced Hearing Loss in the Inferior Colliculus of Dutch-Belted Rabbits by HARIPRAKASH HARAGOPAL has been approved for the Department of the Biological Sciences and the College of Arts and Sciences by Mitchell L. Day Assistant Professor of the Department of the Biological Sciences Florenz Plassmann Dean, College of Arts and Sciences 3 Abstract HARAGOPAL, HARIPRAKASH, Ph.D., August 2020, Neuroscience Graduate Program Neural Correlates of Directional Hearing following Noise-induced Hearing Loss in the Inferior Colliculus of Dutch-Belted Rabbits Director of Dissertation: Mitchell L. Day Sound localization is the ability to pinpoint sound source direction in three dimensions using auditory cues. Sound localization in the horizontal plane involves two binaural cues (involving two ears), namely, difference in the time of arrival of sounds and difference in the level of sounds between the ears, known as interaural time difference (ITD) and interaural level difference (ILD), respectively. Electrical recordings of neural activity, mostly in awake Dutch-Belted rabbits, have shown that neurons in the auditory nervous system, especially the inferior colliculus, which is an obligatory area along the auditory pathway, use these binaural cues to encode sound source direction (that is, directional information) in their firing rates (that is, the number of times they fire an action potential in a second). However, not much is known about neural encoding of directional information following hearing loss. Studies on human subjects have revealed a deterioration of sound localization ability pointing to a potential degradation of neural encoding of directional information as well. Here, we probe this by measuring directional information in neural firing rates from the inferior colliculi of awake, Dutch-Belted rabbits with severe noise-induced hearing loss. To induce hearing loss, rabbits were overexposed to loud noise. Our overexposure resulted in widespread damage to sensory hair cells within the hearing organ embedded within the ears, called the cochlea, and 4 created a ~50-dB elevation in hearing thresholds (that is, minimum responsive sound levels). Neural measurements showed that neural firing rates, on average, contained less directional information with hearing loss than normal hearing, even when sounds were sufficiently loud to evoke responses from neurons. This was because many sound-driven neurons conveyed directional information via monaural (involving one ear) sound level cues. Remaining sound-driven neurons were purely ILD-sensitive and exhibited a complete lack of ITD sensitivity. Computational modeling suggested that the lack of ITD sensitivity could not be simply explained by damage to the cochlea, implying that changes in central auditory areas may underlie this deficit. 5 Dedication To my parents, To Katie, And to my mentor, Dr. Mitchell Day 6 Acknowledgments I would like to thank my committee members, Dr. Scott Hooper for suggesting edits to the document (except Chapter 3, which was already published at the time of drafting of this document) which has improved, considerably, both the readability of the document and my ability to revise textual content, Dr. Alexander Neiman for his critical review of the computational methods and suggestions that have increased the scope of interpretability of results (Chapter 5) and Dr. Li Xu for suggesting that we analyze peripheral effects of noise-induced hearing loss which has greatly improved our understanding of hearing loss in the Dutch-belted strain of rabbits (Chapter 3), and has paved the way for making educated simulation of hearing loss (Chapter 5). I would like to thank Dr. Mitchell Day, my doctoral advisor and committee chair, who not only chiseled me into a better experimentalist in the lab, but also expertly guided me in writing, while stressing the value of practicing thoroughness and checking the appropriateness of, within the bounds of daily calendar time, data acquisition, data analysis, result presentation and interpretation, modeling procedures, and for showing me how to execute systematic time-bound planning that spreads across years. COVID-19-related pandemic has not been easy on any of us, and to graduate during times like this, a lot of additional pains have to be taken when a student is devoid of the usual luxury of an in-person meeting with the advisor. I am grateful to Dr. Day for coming up with an effective communication strategy and a clear timeline for the summer, built around thoroughness of advising, and painstaking edits, which has supported my progress into completing the dissertation. 7 This project was supported by funds from NIDCD-NIH. I had really able hands helping me through the project. I would like to thank Dr. Soichi Tanda for extracting the cochleae from rabbit temporal bones, and Dr. Mark Berryman for providing confocal images of the cochleae. Thanks to the undergraduates: Holly Johnson (for counting hair cells in the cochleae), and Gareth Whaley, Noelle Stroud, Timothy Wohl, Lukas Palmer and Kinzie Bailey for acquiring neural data. I would like to thank the lab technicians, Dr. Ryan Dorkoski and Austin Pollard, for assisting in surgeries, in addition to acquiring neural data. I am grateful to Ohio University for facilitating confocal facility for imaging cochleae, and for providing rabbit housing. None of this would have been possible without the incredible help and support from my parents and Katie Knies. 8 Table of Contents Page Abstract ............................................................................................................................... 3 Dedication ........................................................................................................................... 5 Acknowledgments............................................................................................................... 6 List of Tables .................................................................................................................... 12 List of Figures ................................................................................................................... 13 List of Abbreviations......................................................................................................... 15 Chapter 1: Introduction ..................................................................................................... 17 Sound Localization: Physical, Psychophysical and Behavioral Aspects .................... 17 Neural Mechanisms Underlying Sound Localization: Circuit to Function ................ 20 Noise-induced Hearing Loss: Prevalence and Psychophysical Effects ...................... 24 Noise-induced Hearing Loss: Peripheral and Central Auditory Effects ..................... 25 Noise-induced Hearing Loss: Implications for Psychophysical and Neural Sound Localization and Leading Hypothesis of the Present Study ....................................... 28 Chapter 2: General Methods ............................................................................................. 30 Choice of Animal Model ............................................................................................ 30 Assessments of Hearing Sensitivity I: Auditory Brainstem Response ....................... 31 Assessments of Hearing Sensitivity II: Distortion Product Otoacoustic Emissions ... 34 Noise Waveform for Overexposure ............................................................................ 37 Cochlear Histology ..................................................................................................... 38 Chronic Electrode Design ........................................................................................... 40 Rabbit Preparation for Hearing Assessments and Neural Recordings ........................ 42 Generation of Virtual Acoustic Space for Closed-Field Stimulus Presentation ......... 47 Chapter 3: Results I: Paired Measurements of Cochlear Function and Hair Cell Count in Dutch-Belted Rabbits with Noise-Induced Hearing Loss ................................................. 49 Abstract ....................................................................................................................... 49 Introduction ................................................................................................................. 50 Methods....................................................................................................................... 52 Animals ................................................................................................................. 52 ABR and DPOAE Measurement .......................................................................... 52 Noise Overexposure .............................................................................................. 56 9 Immunofluorescence ............................................................................................. 57 Cochlear Hair Cell Counts .................................................................................... 58 Statistical Analysis
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