Peripheral and Central Mechanisms of Temporal Pattern Recognition Christa Ann Baker Washington University in St
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Washington University in St. Louis Washington University Open Scholarship Arts & Sciences Electronic Theses and Dissertations Arts & Sciences Summer 8-15-2015 Peripheral and Central Mechanisms of Temporal Pattern Recognition Christa Ann Baker Washington University in St. Louis Follow this and additional works at: https://openscholarship.wustl.edu/art_sci_etds Part of the Biology Commons Recommended Citation Baker, Christa Ann, "Peripheral and Central Mechanisms of Temporal Pattern Recognition" (2015). Arts & Sciences Electronic Theses and Dissertations. 570. https://openscholarship.wustl.edu/art_sci_etds/570 This Dissertation is brought to you for free and open access by the Arts & Sciences at Washington University Open Scholarship. It has been accepted for inclusion in Arts & Sciences Electronic Theses and Dissertations by an authorized administrator of Washington University Open Scholarship. For more information, please contact [email protected]. WASHINGTON UNIVERSITY IN ST. LOUIS Division of Biology and Biomedical Sciences Neurosciences Dissertation Examination Committee: Bruce A. Carlson, Chair Dennis L. Barbour Timothy E. Holy Jeanne M. Nerbonne Barani Raman Peripheral and Central Mechanisms of Temporal Pattern Recognition by Christa Ann Baker A dissertation presented to the Graduate School of Arts & Sciences of Washington University in partial fulfillment of the requirements for the degree of Doctor of Philosophy August 2015 St. Louis, Missouri © 2015, Christa A. Baker Table of Contents List of Figures ........................................................................................................................iv List of Tables .........................................................................................................................vi List of Abbreviations .............................................................................................................vii Acknowledgements ................................................................................................................ix Abstract ..................................................................................................................................xi Chapter 1: Multiplexed temporal coding of electric communication signals in mormyrid fishes ...................................................................................................................1 Abstract ..................................................................................................................................2 Introduction ............................................................................................................................3 Electric signals in mormyrid fishes communicate sender identity and behavioral state ................................................................................................................................5 Peripheral coding of communication signals: two temporal codes, one circuit ....................12 A sensory pathway devoted to communication behavior ......................................................16 Sensory filtering and temporal sharpening ............................................................................21 Determining sender identity: a circuit for processing submillisecond spike timing differences ......................................................................................................................24 Determining the behavioral state of the sender: multiple mechanisms for temporal filtering of interspike intervals .......................................................................................30 Sensory multiplexing and the evolution of signals and species .............................................37 Future directions ....................................................................................................................39 References ..............................................................................................................................41 Chapter 2: Short-term depression, temporal summation, and onset inhibition shape interval tuning in midbrain neurons ..................................................................................57 Abstract ..................................................................................................................................58 Introduction ............................................................................................................................59 Materials and methods ...........................................................................................................61 Results ....................................................................................................................................75 Discussion ..............................................................................................................................99 References ..............................................................................................................................107 Chapter 3: Behavioral and single-neuron sensitivity to millisecond timing variations in electric communication signals .......................................................................................111 Abstract ..................................................................................................................................112 ii Introduction ............................................................................................................................113 Materials and methods ...........................................................................................................115 Results ....................................................................................................................................124 Discussion ..............................................................................................................................144 References ..............................................................................................................................150 Chapter 4: Oscillatory phase reset: a novel mechanism for peripheral sensory coding ....................................................................................................................................155 Abstract ..................................................................................................................................156 Introduction ............................................................................................................................158 Materials and methods ...........................................................................................................161 Results ....................................................................................................................................172 Discussion ..............................................................................................................................195 References ..............................................................................................................................202 Chapter 5: Conclusions and future directions ..................................................................208 Summary and significance .....................................................................................................209 Future directions ....................................................................................................................210 Conclusions ............................................................................................................................215 References ..............................................................................................................................216 iii List of Figures Chapter 1 Figure 1: Mormyrid electrocommunication consists of a fixed electric organ discharge produced at variable interpulse intervals ...............................................................6 Figure 2: Neuroanatomy of the knollenorgan electrosensory, electromotor, and corollary discharge pathways .................................................................................................8 Figure 3: Evolutionary change in the knollenorgan electrosensory system .........................11 Figure 4: Temporal multiplexing of electrocommunication signals by knollenorgans ........15 Figure 5: ELa and ELp microcircuitry overlaid on a horizontal Nissl section through the midbrain of Brienomyrus brachyistius ...................................................................................18 Figure 6: Friedman-Hopkins model for small cell duration tuning ......................................27 Figure 7: Multiplexed temporal codes are converted into distributed population codes in ELa/ELp .................................................................................................................................29 Figure 8: IPI tuning of ELp neurons in response to electrosensory stimulation in vivo .......31 Figure 9: Multiple synaptic mechanisms can establish IPI tuning .......................................34 Figure 10: Convergence of high- and low-pass tuning can establish diverse temporal filters ......................................................................................................................................38 Chapter 2 Figure 1: ELp neurons vary in their tuning to stimulus interval ...........................................76 Figure 2: Excitatory