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Lumbar Spinal Interneuron Activity As It Relates to Rhythmic Motor Output in the Adult, Spinal, Air-Stepping Cat Chantal Mcmahon Michel Lemay, Ph.D

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Lumbar Spinal Interneuron Activity As It Relates to Rhythmic Motor Output in the Adult, Spinal, Air-Stepping Cat Chantal Mcmahon Michel Lemay, Ph.D Lumbar Spinal Interneuron Activity as it Relates to Rhythmic Motor Output in the Adult, Spinal, Air-Stepping Cat A Thesis Submitted to the Faculty of Drexel University by Chantal Marie McMahon in partial fulfillment of the requirements for the degree of Doctor of Philosophy May 30th, 2014 ii Dedications I would like to dedicate to this body of work to my parents. Your unconditional love, support and guidance have meant everything to me. Thank you. I would also like to dedicate this thesis to my grandfather and my brother. Your unending quest for answers, scientifically related and other, is inspiring. iii Acknowledgments I would like to acknowledge the hard work and dedication of my lab and advisor; Michel Lemay, Alexander Krupka, David Kowalski, Dwight Higgin, Kassi Miller, Marko Dimiskovski and Karen Ollivier-Lanvin. Thank you for being there during the late night experiments, surgeries and morning and evening care as well as answering any and all questions. My thesis committee including Joshua Jacobs, Meltem Izzetoglu, Marie-Pascale Cote and Hualou Liang for your support and guidance. It was always a pleasure meeting with you. Everyone in the Department of Neurobiology and Anatomy and the PPG, ULAR, the Biomed Graduate Student Office and the BME Graduate Student Office for being readily available to assist in and address any need. A special set of acknowledgements to Joy Hudson, Ilya Rybak, Dolly Testa and Maria Peters-Hample for always having a smile and kind word. To all of my friends over the years who made life good; Angela, Rani, Emmanuelle, Melissa, Alicia, Daniel, Alex and Kassi. Finally, I would like to acknowledge my amazing husband for his support and love. iv Table of Contents List of Tables .................................................................................................................. viii List of Figures ................................................................................................................... ix Abstract ........................................................................................................................... xiii Chapter 1: Introduction and Specific Aims.................................................................... 1 1.1 Introduction and Significance 1 1.1.1 Spinal Cord Injury and Therapeutic Relevance .................................................. 1 1.1.2 Theories of Spinal Locomotor Network Drive and Gaps in Current Knowledge ..................................................................................................................................... 2 1.2 Research Plan and Specific Aims 3 1.2.1 Specific Aim 1: Characterize spinal interneuron activity and location during locomotion ................................................................................................................... 4 1.2.2 Specific Aim 2: Characterize spinal interneuron multiunit activity during locomotion ................................................................................................................... 7 1.3 Background and Significance 9 1.3.1 Anatomy of Motor Control ................................................................................. 9 1.3.2 Characterization of Locomotion ....................................................................... 29 1.3.3 Spinal Cord Injury ............................................................................................ 39 1.3.4 Spinal Control of Locomotion .......................................................................... 45 1.3.5 Analytical Framework: Functional and Spatial Organization of Spinal Locomotor Networks ................................................................................................. 60 Chapter 2: Single Cell and Ensemble Activity of Lumbar Intermediate and Ventral Horn Interneurons in the Spinal Air-Stepping Cat ..................................................... 62 2.1 Abstract 62 2.2 Introduction 63 2.2.1 Rhythmic Activity of Spinal Interneurons during Behavior ............................ 63 2.2.2 Spatial Organization of Flexor vs Extensor Tuned Neurons ............................ 64 v 2.2.3 Population Scale Neural Analysis .................................................................... 65 2.3 Materials and Methods 66 2.3.1 Animals and Experimental Procedures ............................................................. 66 2.3.2 Surgical Procedures prior to Recording Session .............................................. 67 2.3.3 Data Acquisition ............................................................................................... 68 2.3.4 Data Processing ................................................................................................ 71 2.4 Results 82 2.4.1 Summary ........................................................................................................... 82 2.4.2 EMG Stepping Results ..................................................................................... 84 2.4.3 Single Unit Results ........................................................................................... 86 2.4.4 Spinal Interneuron Community Detection Ensembles ..................................... 87 2.4.5 Preferred Phase of Firing Spinal Interneuron Ensembles ................................. 89 2.4.6 Neural Modality Comparison ........................................................................... 91 2.4.7 Anatomical Spatial Layout of Spinal Interneurons Based on Activity during Stepping ..................................................................................................................... 95 2.5 Discussion 96 2.5.1 Summary ........................................................................................................... 96 2.5.2 Neural Populations Tuned to Flexion and Extension Phases of Air-Stepping . 97 2.5.3 Network Functional Classifications.................................................................. 98 2.5.4 Spatial Distributions of Stepping Related Neurons .......................................... 99 2.5.5 Biological Relevance of Mathematical Spike Time Clustering Algorithm .... 100 Chapter 3: Power spectral analysis of lumbar multiunit activity during locomotion ......................................................................................................................................... 120 3.1 Abstract 120 3.2 Introduction and Rationale 121 3.2.1 Spectral Analysis of Multiunit Signals ........................................................... 121 vi 3.2.2 Localization of Rhythm Generating Centers .................................................. 122 3.2.3 Models of Stepping Control: 2-level Central Pattern Generator .................... 123 3.2.4 Rostrocaudal Activation Patterns along the Lumbar Spinal Cord .................. 125 3.3 Materials and Methods 128 3.3.1 Multiunit Envelope Processing ....................................................................... 128 3.3.2 Comparisons of the Multiunit Power Spectral Density per Lumbar Segment 129 3.3.3 Trial Selection Criteria for Flexion and Extension Phase MUA Power Comparisons ............................................................................................................ 131 3.3.4 Comparisons of Flexion and Extension Phase Multiunit Power Spectral Density ................................................................................................................................. 131 3.3.5 Multiunit Coherence and Phase Analysis for Detection of Progression in Rostrocaudal Activation .......................................................................................... 132 3.4 Results 133 3.4.1 Summary ......................................................................................................... 133 3.4.2 Comparisons of the Multiunit Relative Spectral Power between Lumbar Segments .................................................................................................................. 134 3.4.3 Comparisons between Flexion and Extension Phase Multiunit Spectral Power ................................................................................................................................. 136 3.4.4 Multiunit Coherence between Segments ........................................................ 137 3.5 Discussion 139 3.5.1 Summary ......................................................................................................... 139 3.5.2 Spectral Power of Spinal Interneuron Multiunit Activity .............................. 140 3.5.3 Spinal Interneurons and the Central Pattern Generator .................................. 146 Chapter 4: Discussion ................................................................................................... 160 4.1 Summary of Findings and Interpretations 160 4.1.1 Specific Aim 1: Characterize spinal interneuron activity and location during locomotion ............................................................................................................... 160 vii 4.1.2 Specific Aim 2: Characterize spinal interneuron multiunit activity during locomotion ............................................................................................................... 162 4.2 Model Limitations 165 4.3 Future Directions 167 References ...................................................................................................................... 169 Appendix I: Neuron Tracking Via Variational Bayesian Mixture Model ............... 197 Overview: 197 Data Organization and Database Layout: 197 Step
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