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I in VIVO VISUALIZATION of NEURAL PATHWAYS in the RAT IN VIVO VISUALIZATION OF NEURAL PATHWAYS IN THE RAT SPINAL CORD USING VIRAL TRACING A Dissertation Submitted to the Temple University Graduate Board In Partial Fulfillment of the Requirements for the Degree DOCTOR OF PHILOSOPHY OF BIOMEDICAL NEUROSCIENCE by Kathleen M. Keefe Diploma Date, August 2018 Examining Committee Members: George Smith, PhD, Advisor, Shriner’s Pediatric Research Center/Department of Neuroscience Wenhui Hu, MD, PhD, Committee Chair, Center for Metabolic Disease Research, Department of Pathology and Laboratory Medicine Barbara Krynska, MS, PhD, Shriner’s Pediatric Research Center/Department of Neuroscience Shuxin Li, MD, PhD, Shriner’s Pediatric Research Center/Department of Neuroscience Michel Lemay, PhD, External Examiner, Biomedical Engineering i © Copyright 2018 by Kathleen M. Keefe All Rights Reserved ii ABSTRACT Much of our understanding of the fascinating complexity of neuronal circuits comes from anatomical tracing studies that use dyes or fluorescent markers to highlight pathways that run through the brain and spinal cord. Viral vectors have been utilized by many previous groups as tools to highlight pathways or deliver transgenes to neuronal populations to stimulate growth after injury. In a series of studies, we explore anterograde and retrograde tracing with viral vectors to trace spinal pathways and explore their contribution to behavior in a rodent model. In a separate study, we explore the effect of stimulating intrinsic growth programs on regrowth of corticospinal tract (CST) axons after contusive injury. In the first study, we use self-complimentary adeno associated viral (scAAV) vectors to trace long descending tracts in the spinal cord. We demonstrate clear and bright labeling of cortico-, rubro- and reticulospinal pathways without the need for IH, and show that scAAV vectors transduce more efficiently than single stranded AAV (ssAAV) in neurons of both injured and uninjured animals. This study demonstrates the usefulness of these tracers in highlighting pathways descending from the brain. Retrograde tracing is also a key facet of neuroanatomical studies involving long distance projection neurons. In the next study, we highlight a lentivirus that permits highly efficient retrograde transport (HiRet) from synaptic terminals within the cervical and lumbar enlargements of the spinal cord. By injecting HiRet, we can clearly identify supraspinal and propriospinal circuits innervating MN pools relating to forelimb and hindlimb function. We observed robust labeling of propriospinal neurons, including high fidelity details of dendritic arbors and axon terminals seldom seen with chemical tracers. iii In addition, we examine changes in interneuronal circuits occurring after a thoracic contusion, highlighting populations that potentially contribute to spontaneous behavioral recovery in this lesion model. In a related study, we use a modified version of HiRet as part of a multi-vector system that synaptically silences neurons to explore the contribution of the rubrospinal tract (RST) and CST to forelimb motor behavior in an intact rat. This system employs Tetanus toxin at the neuronal synapse to prevent release of neurotransmitter via cleavage of vesicle docking proteins, effectively preventing the propagation of action potentials in those neurons. We find that shutdown of the RST has no effect on gross forelimb motor function in the intact state, and that shutdown of a small population of CST neurons in the FMC has a modest effect on grip strength. These studies demonstrate that the HiRet lentivirus is a unique tool for examining neuronal circuitry and its contribution to function. In the final study, we explore stimulation of the Phosphoinositide 3-kinase/Rac- alpha serine/threonine Protein Kinase (PI3K/AKT) growth pathway by antagonizing phosphatase and tensin homolog (PTEN), a major inhibitor, to encourage growth of CST axons after a contusive injury. We use systemic infusions of four distinct PTEN antagonist peptides (PAPs) targeted at different sites of the PTEN protein. We find robust axonal growth and sprouting caudal to a contusion in a subset of animals infused with PAPs targeted to the PTEN enzymatic pocket, including typical morphology of growing axons. Serotonergic fiber growth was unaffected by peptide infusion and did not correlate with CST fiber density. Though some variability was seen in the amount of growth within our animal groups, we find these PTEN antagonist peptides a promising and iv clinically relevant tool to encourage CST sprouting, and a potentially useful addition to therapies using combinatory strategies to enhance growth. These studies demonstrate that viral tracing is a powerful tool for mapping spinal pathways and elucidating their ability to reform spinal circuits after injury. Viral vectors can be used in both anterograde and retrograde tracing studies to highlight intricacies of neuronal cell bodies, axons and dendritic arbors with a high degree of fidelity. In the injured state, these tools can help identify pathways that contribute to spontaneous recovery of function by highlighting those that reform circuits past an injury site. In the uninjured state, these vectors can contain neuronal silencing methods that help define the contribution of specific pathways to behavior. v ACKNOWLEDGMENTS I would like to acknowledge Dr. George Smith for supporting the work outlined in this thesis and for helping me achieve my dream of earning a doctorate of philosophy. I would like to acknowledge all of the members of the Smith lab for their assistance over the years. Thank you to Yingpeng Liu for the surgical assistance and for helping me maintain my cool in the face of malfunctioning equipment. Thank you to Chidubem Eneanya, Ian Junker and Noelle Sterling for many hours of histology and microscope assistance. Thank you to Imran Sheikh for the commiseration. I would like to acknowledge the members of my thesis committee for reading this extensive work – thank you for your time and energy. I would like to acknowledge my fiancé Anthony Rubbo, who has been there to support me every step of the way, and has put up with all of the busy times. I would like to acknowledge my friends Will and Sarah for always reminding me that I was capable of doing all of this. I would like to acknowledge Shriner’s Pediatric Research Center for supporting my work and fostering a welcoming and collaborative environment during my time as a graduate student. vi TABLE OF CONTENTS ABSTRACT ..................................................................................................................... III ACKNOWLEDGMENTS .............................................................................................. VI LIST OF FIGURES ........................................................................................................ IX LIST OF ABBREVIATIONS ........................................................................................ XI CHAPTER 1. INTRODUCTION .....................................................................................1 Anatomy of the Spinal Cord ....................................................................................1 Descending Motor Pathways ...................................................................................6 Ascending Sensory Pathways ................................................................................13 Propriospinal Interneurons .....................................................................................14 Spinal Cord Injury and its Effects ..........................................................................16 Why Do Neurons Fail to Regenerate? ...................................................................25 The Rodent as a Model Organism for Spinal Cord Injury Studies ........................36 Using Viral Vectors for In Vivo Visualization and Regeneration Studies ............40 CHAPTER 2. MAPPING SPINAL PATHWAYS VIA ANTEROGRADE TRACING WITH ADENO-ASSOCIATED VIRAL VECTORS ...............................44 Introduction……… .......................................................................................…….44 Materials and Methods ...........................................................................................46 Results…………… ................................................................................................51 Discussion………… ..............................................................................................56 CHAPTER 3. MAPPING SPINAL PATHWAYS AND ELUCIDATING THEIR CONTRIBUTION TO BEHAVIOR USING RETROGRADE TRACING WITH HIRET LENTIVIRUS ....................................................................61 Introduction……… ................................................................................................61 Materials and Methods ...........................................................................................68 Results…………… ................................................................................................81 Discussion………. .................................................................................................93 CHAPTER 4. EXPLORING THE REGROWTH POTENTIAL OF SPINAL PATHWAYS AFTER INJURY ....................................................................................103 Introduction……… ..............................................................................................103 Materials and Methods .........................................................................................105 Results……………
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