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Cortical and Subcortical Mechanisms for Sound Processing Jennifer Blackwell University of Pennsylvania, [email protected]

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Cortical and Subcortical Mechanisms for Sound Processing Jennifer Blackwell University of Pennsylvania, Blaje42@Gmail.Com University of Pennsylvania ScholarlyCommons Publicly Accessible Penn Dissertations 2019 Cortical And Subcortical Mechanisms For Sound Processing Jennifer Blackwell University of Pennsylvania, [email protected] Follow this and additional works at: https://repository.upenn.edu/edissertations Part of the Neuroscience and Neurobiology Commons Recommended Citation Blackwell, Jennifer, "Cortical And Subcortical Mechanisms For Sound Processing" (2019). Publicly Accessible Penn Dissertations. 3275. https://repository.upenn.edu/edissertations/3275 This paper is posted at ScholarlyCommons. https://repository.upenn.edu/edissertations/3275 For more information, please contact [email protected]. Cortical And Subcortical Mechanisms For Sound Processing Abstract The uda itory cortex is essential for encoding complex and behaviorally relevant sounds. Many questions remain concerning whether and how distinct cortical neuronal subtypes shape and encode both simple and complex sound properties. In chapter 2, we tested how neurons in the auditory cortex encode water-like sounds perceived as natural by human listeners, but that we could precisely parametrize. The ts imuli exhibit scale-invariant statistics, specifically temporal modulation within spectral bands scaled with the center frequency of the band. We used chronically implanted tetrodes to record neuronal spiking in rat primary auditory cortex during exposure to our custom stimuli at different rates and cycle-decay constants. We found that, although neurons exhibited selectivity for subsets of stimuli with specific ts atistics, over the population responses were stable. These results contribute to our understanding of how auditory cortex processes natural sound statistics. In chapter 3, we review studies examining the role of different cortical inhibitory interneurons in shaping sound responses in auditory cortex. We identify the findings that support each other and the mechanisms that remain unexplored. In chapter 4, we tested how direct feedback from auditory cortex to the inferior colliculus modulated sound responses in the inferior colliculus. We optogenetically activated or suppressed cortico-collicular feedback while recording neuronal spiking in the mouse inferior colliculus in response to pure tones and dynamic random chords. We found that feedback modulated sound responses by reducing sound selectivity by decreasing responsiveness to preferred frequencies and increasing responsiveness to less preferred frequencies. Furthermore, we tested the effects of perturbing intra-cortical inhibitory-excitatory networks on sound responses in the inferior colliculus. We optogenetically activated or suppressed parvalbumin-positive (PV) and somatostatin-positive (SOM) interneurons while recording neuronal spiking in mouse auditory cortex and inferior colliculus. We found that modulation of neither PV- nor SOM-interneurons affected sound-evoked responses in the inferior colliculus, despite significant modulation of cortical responses. Our findings imply that cortico-collicular feedback can modulate responses to simple and complex auditory stimuli independently of cortical inhibitory interneurons. These experiments elucidate the role of descending auditory feedback in shaping sound responses. Together these results implicate the importance of the auditory cortex in sound processing. Degree Type Dissertation Degree Name Doctor of Philosophy (PhD) Graduate Group Neuroscience First Advisor Maria N. Geffen Second Advisor Yale Cohen This dissertation is available at ScholarlyCommons: https://repository.upenn.edu/edissertations/3275 Subject Categories Neuroscience and Neurobiology This dissertation is available at ScholarlyCommons: https://repository.upenn.edu/edissertations/3275 CORTICAL AND SUBCORTICAL MECHANISMS FOR SOUND PROCESSING Jennifer M. Blackwell A DISSERTATION in Neuroscience Presented to the Faculties of the University of Pennsylvania in Partial Fulfillment of the Requirements for the Degree of Doctor of Philosophy 2019 Supervisor of Dissertation _________________________ Maria N. Geffen, PhD Associate Professor of Otorhinolaryngology Graduate Group Chairperson ________________________ Joshua I. Gold, PhD Professor of Neuroscience Dissertation Committee: Yale Cohen, Professor of Otorhinolaryngology Steven Eliades, Assistant Professor of Otorhinolaryngology Christopher Fang-Yen, Associate Professor of Neuroscience Daniel Polley, Associate Professor of Otolaryngology, Harvard Medical School ACKNOWLEDGMENTS There are so many people who have helped and supported me through my graduate school journey. First, I want to thank my advisor, Maria, for all the years of unwavering support. There were few ups and many downs during my time here and Maria was always able to stay positive and provide the space I needed to work through any difficulties I was facing. I also want to thank her for her support of my passion in teaching alongside my research. Even though the Geffen lab was always slightly too cold, the people have always been warm, supportive, and willing to help each other out in any way. I want to thank Laetitia Mwilambwe-Tshilobo, Drs. Mark Aizenberg, Ryan Natan, and Isaac Carruthers for their guidance when I first joined the lab. Our numbers have now expanded, but the lab environment continues to be friendly and collaborative. Thank you to Solymar Rolon- Martinez, Xiaomao Ding, Aaron Williams, Karmi Oxman, and Drs. Melanie Tobin and Linda Garami. I especially want to thank Chris Angeloni for always having the answers to all of my questions (Cy Twombly will always be the worst though) and Dr. Kath Wood for being, like me, willing to talk about literally anything (a kindred spirit). My fellow NGG students, Drs. Peter Dong, Preetika Gupta, Greg Artiushin, and CC Angelakos for the many years of friendship and laughter – I cannot imagine these years without you. For years of love and support, bringing me dinner when I was stuck in lab late at night, sending me terrible jokes from Reddit and many pictures of adorable animals just to brighten my day, I want to thank Dr. Andrew Moberly. Dad – thank you for being there while I was growing up and for introducing me to Terry Pratchett, who has gotten me through a lot of stressful times. Finally, I want to thank my mom, Dr. Kim Blackwell. I am lucky enough to know ii that there is nothing in the world you would not do to help me achieve my dreams, including staying up to read my textbooks just to help me with my homework, or writing out math equations on our napkins at the dinner table. Thank you for always being there to talk about my achievements and my failures whenever I need, and also to bake some crazy things when I really just needed a break. You never pushed me into one career or another, yet somehow it turns out that I followed you right into Neuroscience. iii ABSTRACT CORTICAL AND SUBCORTICAL MECHANISMS FOR SOUND PROCESSING Jennifer M. Blackwell Maria N. Geffen The auditory cortex is essential for encoding complex and behaviorally relevant sounds. Many questions remain concerning whether and how distinct cortical neuronal subtypes shape and encode both simple and complex sound properties. In chapter 2, we tested how neurons in the auditory cortex encode water-like sounds perceived as natural by human listeners, but that we could precisely parametrize. The stimuli exhibit scale- invariant statistics, specifically temporal modulation within spectral bands scaled with the center frequency of the band. We used chronically implanted tetrodes to record neuronal spiking in rat primary auditory cortex during exposure to our custom stimuli at different rates and cycle-decay constants. We found that, although neurons exhibited selectivity for subsets of stimuli with specific statistics, over the population responses were stable. These results contribute to our understanding of how auditory cortex processes natural sound statistics. In chapter 3, we review studies examining the role of different cortical inhibitory interneurons in shaping sound responses in auditory cortex. We identify the findings that support each other and the mechanisms that remain unexplored. In chapter 4, we tested how direct feedback from auditory cortex to the inferior colliculus modulated sound responses in the inferior colliculus. We optogenetically activated or suppressed cortico- collicular feedback while recording neuronal spiking in the mouse inferior colliculus in response to pure tones and dynamic random chords. We found that feedback modulated iv sound responses by reducing sound selectivity by decreasing responsiveness to preferred frequencies and increasing responsiveness to less preferred frequencies. Furthermore, we tested the effects of perturbing intra-cortical inhibitory-excitatory networks on sound responses in the inferior colliculus. We optogenetically activated or suppressed parvalbumin-positive (PV) and somatostatin-positive (SOM) interneurons while recording neuronal spiking in mouse auditory cortex and inferior colliculus. We found that modulation of neither PV- nor SOM-interneurons affected sound-evoked responses in the inferior colliculus, despite significant modulation of cortical responses. Our findings imply that cortico-collicular feedback can modulate responses to simple and complex auditory stimuli independently of cortical inhibitory interneurons. These experiments elucidate the role of descending auditory feedback in shaping sound responses. Together these results implicate the importance of the auditory cortex in sound processing.
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