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Thesis.Pdf (5.344Mb) SENSORIMOTOR BEHAVIOUR IN RATS AFTER LESIONS OF DORSAL SPINAL PATHWAYS Submitted to the College of Graduate Studies and Research of the University of Saskatchewan for partial completion of the Doctor of Philosophy degree in the Department of Veterinary Biomedical Sciences at the University of Saskatchewan and pertaining to Behavioural Neuroscience by SRIKANTH G. KANAGAL © Copyright Srikanth G. Kanagal, August, 2008 All rights reserved PERMISSION TO USE In agreement with the outlines set out by the College of Graduate Studies and Research at the University of Saskatchewan, I allow the University of Saskatchewan Libraries to make this thesis available to all interested parties. Also in accordance with the College of Graduate Studies and Research, I allow this thesis to be copied “in any manner, in whole or in part, for scholarly purposes”. This thesis may not, however, be reproduced or used in any manner for financial gain with my written consent. Any scholarly use of this thesis, in part or in whole, must acknowledge both myself and the University of Saskatchewan. Any requests for copying or using this thesis, in any form or capacity, should be made to: Head of Department of Veterinary Biomedical Sciences University of Saskatchewan Saskatoon, Saskatchewan S7N 5B4 i ABSTRACT To investigate the roles of different dorsal spinal pathways in controlling movements in rats, I performed lesions of specific spinal pathways and measured the behaviour abilities of rats using different sensorimotor behavioural tests. The first experiment was designed to understand the contribution of sensory pathways traveling in the dorsal funiculus during locomotion and skilled movements using sensitive behavioural tests. I demonstrated that ascending sensory fibers play an important role during overground locomotion and contribute to skilled forelimb movements. The second experiment compared the differences in sensorimotor abilities caused by dorsal funicular lesions performed at two different levels of rat spinal cord. My results showed that the pathways present in the cervical and thoracic dorsal funiculus exert different functional effects over control of limb movement during locomotion. The third experiment investigated the compensatory potential of dorsal funicular pathways after dorsolateral funicular injuries in rats. My results showed that dorsal funicular pathways do not compensate for loss of dorsolateral pathways during the execution of locomotor tasks, though there is indirect evidence that rats with dorsolateral funicular lesions might rely more on ascending sensory pathways in the dorsolateral funiculus during skilled forelimb movements. Finally, the fourth experiment was designed to investigate the compensation from dorsolateral funicular pathways after injuries to pyramidal tract in rats. I demonstrated that pathways running in the spinal dorsolateral funiculus do provide compensatory input to spinal circuitry to maintain skilled reaching abilities after lesions of the pyramidal tract but these same pathways do not appear to compensate during either overground ii locomotion or skilled locomotion. Thus, this compensatory response is task-specific. These results highlight the fact that behavioural context determines the nature of compensation from spared pathways after spinal cord injuries. iii ACKNOWLEDGEMENTS I wish to express gratitude to my supervisor, Dr. Gillian Muir for her unwavering encouragement and unstinted support during my entire PhD program. It is on the account of scientific training that she has imparted to me, that I wish and, I can hope to continue and contribute to science. Her patience and active guidance alone has brought me this far. Being part of her lab was an absolute joy where she set an inimitable example of how to balance family with research, and made me realize what education truly means, and this to me, goes far more than what ever I have learnt about science. My many thanks to her. I thank the members of my PhD advisory committee (Drs. Baljit Singh, Ron Doucette, David Janz, Gillian Muir and Linda Hiebert) for their guidance, constructive criticisms and encouragement. Special thanks to Teresa Chu, for her inspiration and support during my initial few years. My thanks to K.S.V. Gowri, Carrol Dowdswell, Margeret Dykes and Andrea Chennettee for their technical assistance and help during my research. Thank you to Melanie Vanderloop, Sean Bennett, Cathy Dick, Laura Taylor and Nadine Poulton for their help and company. Thanks to Drs. Don Hamilton and Ron Chaplin for exposing me to wonderful joy of teaching. Special thanks to my friends for life Seena and Prabha for being, and having been, more than my family through thick and thin and through my many mood-swings. Thanks to my close friends Muraly, Kashi and Prasad for their patient hearing and support. Thank you to Raj and Janardhan for helping me to understand and navigate through life and science and also for exposing me to scientific obsession, I am enjoying it. Thank you to iv Chandrashekar, my friend-in-need. Thanks to Tara, Lakshminarayana Reddy, Kiran, Naveen, Manju, Keshav, Shankar, Nag, Viji and Raghu for your words of encouragement, laughs, time and company. Thanks to my master’s supervisor Dr. K. Narayana for showing me the path of research and for his persistent encouragement and support. Thanks to Diane Matovich, Joane Payne, Sandra Rose, Sheila Carron for their secretarial support. Thanks to Cathy, Darr and Jim for providing humor and making my stay a memorable one. Lastly and most importantly, I would like to thank my family- Anna, Amma, Sharath Attha, Mama, Raghu and Lakshmi for their patience, unconditional love, support and encouragement. Anna and Amma, I am here because of your sacrifices, I love you very much. I also like to thank Nagesh mama for all the moral support and encouragement despite the inconveniences I put him through. I could not have done this with out these people. v I dedicate this work to my wife Rama and daughter Adithi. It was their sacrifices, forced by my whims and fancies, which made the completion of this thesis possible. Thank you Rama, for supporting and encouraging me during my dark days, you filled me with enough courage and purpose that helped me to reach this goal. Thank you Adithi, for showing me that there is a life besides research, which is beyond everything that I had known. I love you both, thank you. vi TABLE OF CONTENTS PERMISSION TO USE i ABSTRACT ii ACKNOWLEDGEMENTS iv DEDICATION vi List of abbreviations xi List of figures xii List of tables xv Chapter 1. LITERATURE REVIEW------------------------------------------------- 1 1.1 Introduction 1 1.2 Neuroanatomy of spinal cord 2 1.2.1 Introduction 2 1.2.2 Dorsal funiculus 6 1.2.2.1 Dorsal column-medial lemniscal pathway 7 1.2.2.2 Post-synaptic dorsal column pathway 7 1.2.2.3 Corticospinal tract 9 1.2.3 Dorsolateral funiculus 12 1.2.3.1 Spinocerebellar tract 13 1.2.3.2 Spinohypothalamic tract 14 1.2.3.3 Spinomesencephalic tract 15 1.2.3.4 Rubrospinal tract 15 1.2.3.5 Reticulospinal tract 20 1.2.4. Pathways running in ventrolateral and ventral funiculus 21 1.2.4.1 Coeruleospinal tract 21 1.2.4.2 Spinomesencephalic tract 22 1.2.4.3 Spinoreticular tracts 22 1.2.4.4 Spinothalamic tract 23 1.2.4.5 Vestibulospinal tracts 23 1.3 Neural control of locomotion 24 1.4 Neural control of skilled locomotion 27 1.5 Neural control of skilled reaching 30 1.6 Models commonly used to study spinal cord injury 33 1.6.1 Complete spinal cord injury models 34 1.6.2 Incomplete spinal cord injury models 34 1.6.2.1 Contusion injury 35 1.6.2.2 Compression injury 35 1.6.2.3 Laceration injury 36 1.6.2.4 Ischemic injury 36 1.6.2.5 Chemical-mediated injuries 37 1.7 Methods to assess functional recovery after partial spinal lesions in rats 38 1.7.1 End point measures 39 1.7.2 Qualitative measures 40 1.7.3 Quantitative measures 41 1.7.3.1 Quantitative kinematic analysis 41 1.7.3.2 Kinetic analysis 42 vii Chapter 2. OBJECTIVES AND HYPOTHESES--------------------------------------- 44 2.1 Rationale 44 2.2 Objectives and hypotheses of the studies 46 Chapter 3. GENERAL METHODS AND PROCEDURES 48 3.1 Subjects 48 3.2 Training 48 3.3 Surgery 49 3.3.1 Surgical preparation and pre-medication 49 3.3.2 Surgical procedure 49 3.4 Behavioural assessment 51 3.4.1 Training 51 3.4.2 Single pellet reaching- test for skilled forelimb usage 51 3.4.3 Ladder crossing- test for skilled locomotor abilities 54 3.4.4 Kinetic measurements- overground locomotion 54 3.4.4.1 Measurement of ground reaction forces 54 3.4.4.2 Measurement of stride parameters 58 3.5 Histology- microscopic evaluation of the lesion site 58 3.6 Statistical analyses 58 Chapter 4. BILATERAL DORSAL FUNICULAR LESIONS ALTER SENSORIMOTOR BEHAVIOUR IN RATS------------------------------------------- 60 4.1 Abstract 60 4.2 Introduction 61 4.3 Materials and Methods 63 4.3.1 Animals 63 4.3.2 Surgery 63 4.3.3 Behavioural assessment 63 4.3.3.1 Training 63 4.3.3.2 Skilled reaching- single pellet reaching 64 4.3.3.3 Skilled locomotion -Horizontal ladder 64 4.3.3.4 Overground locomotion 64 4.3.3.4.1 Kinematic measurement of ground reaction forces 64 4.3.3.4.2 Measurement of stride parameters 65 4.3.4 Histology 65 4.3.5 Statistical analyses 65 4.4 Results 65 4.4.1 Histology 65 4.4.2 Behavioural assessment 67 4.4.2.1 Skilled reaching- single pellet reaching 67 4.4.2.2 Skilled locomotion: horizontal ladder 70 4.4.2.3 Overground locomotion 70 4.4.2.3.1 Analysis of ground reaction forces 70 4.4.2.3.1 Step lengths and stride parameters 72 4.5 Discussion 75 4.6 Conclusions 82 viii Chapter 5.
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