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Spike Timing in Pyramidal Cells of the Dorsal Cochlear Nucleus

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Spike Timing in Pyramidal Cells of the Dorsal Cochlear Nucleus Spike Timing in Pyramidal Cells of the Dorsal Cochlear Nucleus Sarah Elizabeth Street A dissertation submitted to the faculty of the University of North Carolina at Chapel Hill in partial fulfillment of the requirements for the degree of Doctor of Philosophy in the Department of Cell and Molecular Physiology Chapel Hill 2007 Approved by: Paul B. Manis Robert Sealock Robert Rosenberg Paul Tiesinga Benjamin Philpot Abstract Sarah Street: Spike Timing in Pyramidal Cells of the Dorsal Cochlear Nucleus (Under the direction of Paul B. Manis) The cochlear nucleus is the termination point for all axons of the auditory nerve. In addition to input from the auditory nerve, the dorsal cochlear nucleus (DCN) receives input from other sensory systems. The principal neurons of the DCN, the pyramidal cells, process information from both the auditory and non-auditory inputs and relay this information to the inferior colliculus. While it is known that pyramidal cells can use spike timing to encode some auditory information such as frequency modulation, these neurons are usually described in terms of average rate. This study examines the spike timing characteristics of DCN pyramidal cells. We first investigated the spike timing characteristics of pyramidal cells by presenting the cells with Gaussian distributed white noise currents. In response to such stimuli, pyramidal cells fired trains of action potentials with precisely timed spikes. In addition, when an inhibitory event, such as an IPSP was added at the midpoint of the stimulus, the spike times became more precise after the IPSP than they were without the inhibitory event. Intrinsic conductances can shape the output of neurons. One important conductance is a transient outward current known as an A-current. A-currents arise from potassium channels such as Kv1.4, Kv3.4 and the entire Kv4 family. It has been hypothesized that an A-current leads to the build-up response pattern in pyramidal cells, which is characterized by a long latency to the first spike. Using heteropodatoxin-2, a specific blocker of Kv4 channels, ii we determined that Kv4 channels are responsible for the long delay to the first spike after a hyperpolarizing pre-pulse. To confirm this result, we also subtracted a model of the A- current using dynamic clamp and observed the same effect. Finally, the identity of this potassium current was determined using in situ hybridization and immunofluoresence. Pyramidal cells were labeled by injecting a retrograde dye into the inferior colliculus. Labeled pyramidal cells expressed Kv4.3 but not Kv4.2 potassium channels. From these results we concluded that Kv4.3 is essential for the characteristic response patterns observed in DCN pyramidal cells. iii Acknowledgements I am indebted to many wonderful people who helped me throughout this undertaking. First, I am grateful to my parents, Joseph and Marjorie Street, who have been supportive and encouraging throughout my life in all of my pursuits and goals. They have been especially supportive of all of my educational goals and have always made it possible for me to have every opportunity for success. In addition, I must acknowledge and thank my dissertation advisor, Paul B. Manis for his guiding influence, support, and help at all times throughout this project. He has been a friend, a mentor and an exceptional scientific example. My dissertation committee chaired by Robert Sealock and consisting of Robert Rosenberg, Paul Tiesinga and Benjamin Philpot have provided many helpful suggestions and motivating examples that have helped me to bring this work to fruition. I also count each of them among the best teachers I have ever had in my life. I would like to thank David K. Ryugo at the John Hopkins University for providing the tissue samples used in the immuohistochemistry experiments. Mark J. Zylka provided helpful guidance and reagents with the molecular biology needed to construct the probes used for the in situ hybridization experiments. In addition to his help with the in situ work, I would also like to extend a heartfelt thank you to my friend and colleague, Janet Hart, at Duke University for helping me construct the plasmid used to make the Kv4.2 in situ hybridization probe. iv I would like to thank Lyanne Schlicter at the University of Toronto, for providing me with a full length Kv4.2 clone that was used to construct the probe used in the in situ hybridization studies. Ann Stuart has been my graduate school mother and has helped me in ways too numerous to mention here. Whether letting me live in her house or proofreading my papers, she has been a genuine friend and teacher from the time I started graduate school at UNC. Finally, I must acknowledge that if it were not for my great group of friends in Chapel Hill, including Anne Clayton, Amy Lowman, Alisa Muelleck, Alison Neeley, Abby Parcell, and Lisa Jones-Christensen, this process would have not been the enjoyable one that it has been. They have been the best social-support network a woman could ever ask for. A special thanks goes to Alison for formatting my dissertation. v Table of Contents List of Figures ........................................................................................................................................................viii List of Abbreviations............................................................................................................................................... x Chapter 1: Introduction ............................................................................................................................................. 1 1.1 Overview ................................................................................................................................................ 1 1.1.1 Spike Timing in the Auditory System ................................................................................. 3 1.2 DCN Anatomy........................................................................................................................................ 4 1.2.1 Circuitry and Cell Types....................................................................................................... 8 1.3 DCN Physiology.................................................................................................................................. 12 1.3.1 Neuronal Responses to Sound............................................................................................ 12 1.3.2 Intrinsic Conductances of Pyramidal Cells ....................................................................... 19 1.3.3 Other DCN Neurons............................................................................................................ 20 1.3.4 DCN Plasticity..................................................................................................................... 21 1.4 DCN Function ..................................................................................................................................... 22 1.4.1 Amplitude Modulation Encoding....................................................................................... 22 1.4.2 Sound Localization.............................................................................................................. 23 1.4.3 Multisensory Integration..................................................................................................... 27 1.4.4 Tinnitus ................................................................................................................................ 27 1.5 Spike Timing and the Neural Code .................................................................................................... 29 1.6 Transient Potassium Currents............................................................................................................ 31 1.6.1 Molecular characteristics of Transient Potassium Channels ............................................ 31 1.7 Kv4 channel expression patterns........................................................................................................ 34 1.7.1 Kv4 Channel Modulation ................................................................................................... 36 1.7.2 Kv4 channels and neuronal function.................................................................................. 39 1.8 Summary .............................................................................................................................................. 42 Chapter 2: Action potential timing precision in dorsal cochlear nucleus pyramidal cells............................ 43 2.1 Introduction ......................................................................................................................................... 43 2.2 Materials and Methods ....................................................................................................................... 45 2.3 Results .................................................................................................................................................. 50 2.3.1 Responses of Pyramidal Cells to a White Noise Current Injection ................................. 50 2.3.2 Sensitivity of SAC to Spectral Structure of the Noise Input ............................................ 61 2.3.3 Dependence of CI on Firing Rate....................................................................................... 61 2.3.4 Spike Triggered Averages .................................................................................................
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