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A First Step Towards Understanding the Role of the Cerebellum in the Control of Movements Is to Determine the Nature of the Information Forwarded to It

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A First Step Towards Understanding the Role of the Cerebellum in the Control of Movements Is to Determine the Nature of the Information Forwarded to It INPUT PROPERTIES OF FOUR POPULATIONS OF SPINOCEREBELLAR TRACT NEURONS IN THE CAT AND THE RAT THORACO-LUMBAR SPINAL CORD Sony Shakya Shrestha Thesis submitted in fulfillment for the degree of Doctor of Philosophy Institute of Neuroscience and Psychology College of Medical, Veterinary and Life Sciences University of Glasgow Glasgow, Scotland July 2012 Dedication To my most loving late Grandfather and my family Summary The cerebellum receives information from the hindlimbs through several populations of spinocerebellar tract neurons. Although the role of these neurons has been established in electrophysiological experiments, the relative contribution of afferent fibres and central neurons to their input, their organization and mechanisms of control of transmission has only been estimated approximately so far. The present study aimed to investigate the input properties of four populations of spinocerebellar tract neurons: dorsal spinocerebellar tract neurons located in Clarke´s column (ccDSCT) and in the dorsal horn (dhDSCT) and ventral spinocerebellar tract (VSCT) neurons including spinal border (SB) neurons. There were three major aims: (1) to investigate the excitatory inputs to four types of spinocerebellar tract neurons in the cat and rat thoraco-lumbar spinal cord; (2) to analyze the inhibitory inputs to four types of spinocerebellar tract neurons in the cat and rat thoraco-lumbar spinal cord; (3) to determine the origin of excitatory and inhibitory inputs to four types of spinocerebellar tract neurons in the cat and rat thoraco-lumbar spinal cord. Two series of experiments were carried out. In the first series of experiments in cats, spinocerebellar tract neurons were identified electrophysiologically and labelled intracellularly with rhodamine-dextran and Neurobiotin. In the second series of experiments in rats, cells were labelled by retrograde transport of b- subunit of Cholera toxin (CTb) from the cerebellum. In addition, to address the third aim, reticulospinal (RetS) and corticospinal (CS) terminals were identified by anterograde transport of CTb from the caudal medulla and hindlimb sensory motor cortex respectively in rats along with labelling of spinocerebellar tract neurons by retrograde injection of Fluorogold in the cerebellum. Following this, immunohistochemistry was carried out. The first aim was achieved by utilizing the difference in the immunohistochemistry of glutamatergic terminals of peripheral afferents and of central neurons with vesicular glutamate transporters, VGLUT1 or VGLUT2, respectively. All SB neurons with dominating inhibitory input from the periphery possessed very few VGLUT1 I contacts and remarkably higher numbers of VGLUT2 contacts. In VSCT neurons with excitatory primary afferent input, the number of VGLUT1 contacts was relatively high although VGLUT2 contacts likewise dominated. In contrast, DSCT neurons were associated with numerous VGLUT1 contacts; ccDSCT neurons with strong input from group I afferents had higher density of VGLUT1 contacts than dhDSCT neurons with major input from group II and cutaneous afferents. In order to fulfill the second aim, quantification of contacts formed by inhibitory axon terminals on spinocerebellar tract neurons along with excitatory terminals was carried out. Inhibitory axon terminals were characterised as either GABAergic, glycinergic or both GABAergic/glycinergic by using antibodies against vesicular GABA transporter (VGAT), glutamic acid decarboxylase (GAD) and gephyrin. Similarly, excitatory terminals were characterised by using combination of VGLUT1 and 2. The comparison revealed the presence of much higher proportions of inhibitory than excitatory contacts on SB neurons but similar proportions were found on VSCT, ccDSCT and dhDSCT neurons. In all types of cell, the majority of inhibitory terminals were glycinergic. The density of contacts was higher on somata and proximal in comparison with distal dendrites of SB and VSCT neurons but more evenly distributed in ccDSCT and dhDSCT neurons. To achieve the third aim, a series of immunohistochemical reactions was performed to characterize contacts that originate from proprioceptors, different types of interneurons and descending RetS and CS pathways. Among the four populations of spinocerebellar tract neurons, ccDSCT neurons had the highest proportion of contacts formed by VGLUT1 terminals double labeled with parvalbumin (PV) which indicated that majority of direct excitatory sensory inputs to ccDSCT neurons are derived from proprioceptors. A small proportion of excitatory and inhibitory contacts on these neurons originated from Calbindin/ Calretinin/ PV expressing neurons. Quantitative analysis revealed that SB and VSCT neurons have significantly higher numbers of appositions from VGLUT2 expressing RetS axon terminals than DSCT neurons. A small proportion of the RetS contacts on these neurons were VGAT positive. In contrast, DSCT neurons had higher numbers of appositions made by CS axon terminals in comparison to SB and VSCT neurons. II The present findings provide a new basis for understanding the organization and functional connectivity of four populations of spinocerebellar tract neurons and strengthen previous indications of their functional differentiation. SB and VSCT neurons principally receive inputs from spinal and supraspinal neurons although direct input from primary afferents is also stronger in VSCT neurons. DSCT neurons have major direct input from primary afferents and also to some extent from the CS pathway but monosynaptic inputs from proprioceptors dominated in ccDSCT neurons and dhDSCT neurons have mixed proprioceptive and low threshold cutaneous afferent input. III Acknowledgement Many people have directly or indirectly contributed to this work. To name them all would result in a directory worth of separate publication. Indeed, they know who they are, and they know that they share this work with me and hopefully they also know how much I am obliged to them. While my intellectual debts are manifolds, I am especially grateful to my supervisor Professor David J Maxwell, Spinal Cord Research Group, Institute of Neuroscience & Clinical Psychology, College of Medicine, Veterinary and Life Sciences, University of Glasgow for his endless support and excellent guidance throughout my research period. I express my heartfelt gratitude to my collaborator Professor Elzbieta Jankowska, Department of Physiology, University of Gothenburg, Sweden for her continuous support and guidance during my visit to her laboratory for electrophysiology experiments. I also would like to thank Dr. Ingela Hammar for her help and hospitality during my Sweden visit. Moreover, I want to thank all the people in Professor Jankowska’s group for their helpful nature. My sincere gratitude also goes to Professor Andrew J Todd, Spinal Cord Research Group, Institute of Neuroscience & Clinical Psychology, College of Medicine, Veterinary and Life Sciences, University of Glasgow for his continuous encouragement and valuable inputs to my research work. I take an immense pleasure to acknowledge Dr. Anne Bannatyne and Dr. Erika Polgar for their help and expert guidance during my research work. An endless thanks goes to Mrs. Christine Watt and Mr. Robert Kerr for their technical support and their always welcoming nature. Special thanks go to my laboratory mates especially, Huma and Nazma for their constant support during my thesis work. There are other groups of individuals whose contributions to this work cannot go unmentioned. All the staffs of Spinal Cord Research Group including Biological Services Central Research Unit, with whom I worked closely, colleagues whose cooperation made this work worthwhile, IV also deserve my heartfelt gratitude. I also want to thank all the cleaners and security people of West Medical Building for their friendly behaviour. A special acknowledgement is due to Overseas Research Studentship Award Scheme and Glasgow University Postgraduate Scholarship awarding body for funding my PhD research. I am very thankful for their support and trust. My special thanks go to Carol and Paul for being a very good friend and supporting us whenever we needed. Lastly, I cannot forget my parents and my loving husband Rajeev, whose never- ending support, trust and constant encouragement led to the accomplishment of this work. V Author’s declaration All the work in this thesis was carried out solely by the author apart from surgical procedures and electrophysiology. Professor David Maxwell contributed to this work by performing surgical procedures in rats. Professor Elzbieta Jankowska contributed to this work by performing surgical procedures and electrophysiological recordings in cats. This thesis has been composed by the author and has not been previously submitted for examination which has led to the award of a degree. The copyright of this thesis belongs to the author under the terms of the United Kingdom Copyright Acts as qualified by University of Glasgow Regulation. Due acknowledgement must always be made of the use of any material contained in, or derived from, this thesis. Signature: Date: VI Table of contents Summary I Acknowledgement IV Author’s declaration VI Table of contents VII List of Tables XI List of Figures XIII List of Abbreviations XVII Chapter 1: Introduction.......................................................................1 1.1 Elementary organization and general characteristics of the spinocerebellar tracts ......................................................................................2
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