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Dopaminergic Modulation of Spinal Circuits for Walking in the Adult Mouse

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Dopaminergic Modulation of Spinal Circuits for Walking in the Adult Mouse University of Calgary PRISM: University of Calgary's Digital Repository Graduate Studies The Vault: Electronic Theses and Dissertations 2018-09-06 Dopaminergic modulation of spinal circuits for walking in the adult mouse Mayr, Kyle Andrew Mayr, K. A. (2018). Dopaminergic modulation of spinal circuits for walking in the adult mouse (Unpublished master's thesis). University of Calgary, Calgary, AB. doi:10.11575/PRISM/32925 http://hdl.handle.net/1880/107749 master thesis University of Calgary graduate students retain copyright ownership and moral rights for their thesis. You may use this material in any way that is permitted by the Copyright Act or through licensing that has been assigned to the document. For uses that are not allowable under copyright legislation or licensing, you are required to seek permission. Downloaded from PRISM: https://prism.ucalgary.ca UNIVERSITY OF CALGARY Dopaminergic modulation of spinal circuits for walking in the adult mouse by Kyle Andrew Mayr A THESIS SUBMITTED TO THE FACULTY OF GRADUATE STUDIES IN PARTIAL FULFILMENT OF THE REQUIREMENTS FOR THE DEGREE OF MASTER OF SCIENCE GRADUATE PROGRAM IN NEUROSCIENCE CALGARY, ALBERTA SEPTEMBER, 2018 © Kyle Mayr 2018 Abstract Walking is a stereotyped rhythmic behavior that consists of alternating contractions of flexor and extensor muscles, as well as the left and right hindlimbs. The basic rhythmic pattern underlying locomotion is generated by a central pattern generator network within the lumbar spinal cord. The role of many neurotransmitters and modulators have been studied extensively, but dopamine’s (DA) role in modulating movement at the level of the lumbar spinal cord, is still not fully understood, especially in adult mice. The decerebrate mouse preparation allows us to examine modulation of stepping behaviour in adult mice with reduced descending inputs to the spinal cord, while intrathecally manipulating the lumbar spinal cord. Locomotor activity was measured by recording weight bearing during locomotion and electromyograms (EMG) from the flexor (tibialis anterior) and extensor (gastrocnemius) muscles of the hindlimbs. Our results show that intrathecal application of DA at the lumbar spinal cord increased the duration of locomotor bouts. Intrathecal DA led to an increase in weight bearing, suggesting that DA may promote extensor biased walking. Furthermore, addition of D1-like agonists augmented weight bearing in the decerebrate animal, but not as much as DA alone. Using intact animals intrathecally injected with either DA, or DA antagonists we selectively activated or blocked DA receptor subtypes of the spinal cord. Using the open field test and ladder rung, we quantified the amount of activity, type of activity and scored the skilled steps during locomotion. Our findings show that DA decreased the amount of locomotor activity in the open field but did not have a significant effect on the ladder rung step score. Furthermore, we found that D1-like antagonists reduced locomotor activity (distance, velocity and bouts) while D2-like antagonists did not have a significant impact on open field activity, though there was an increase in errors while crossing the ladder rung. This thesis provides insight into the DAergic contribution to the modulation in adult mouse locomotion and bridges the gap from previous neonatal animal work. It shows that DA can have differential effects dependant on the state of the animal and provides a foundation for future work on DA neuromodulation. ii Preface Chapter 1. Review of the literature and the relevant information pertaining to this thesis. Chapter 2. Has been published as C. Meehan and K.A. Mayr, M. Manuel, S.T. Nakanishi, P.J. Whelan, “Decerebrate mouse model for studies of the spinal cord circuits.”. (2017) Nature protocols, vol. 12(4), issue: 4, pages: 732-747. Chapter 3. In preparation for submission as K.A. Mayr and P.J. Whelan, “Dopaminergic modulation of stepping locomotion in adult mice”. Journal of Neuroscience. Chapter 4: Is a general discussion of the material presented throughout this thesis and how it integrates with current knowledge on spinal network function. iii Acknowledgements I would like to thank Dr. Patrick Whelan for his continuous support and mentorship throughout my master’s program. He has been an invaluable resource and mentor always giving me the freedom to explore new ideas but encouraging me to see the big picture in science. Words will never be enough to explain the gratitude I have for these past few years. I would like to extend a sincere thank you to Dr. Simon Sharples for his friendship, expertise and help throughout this project and degree. You have been an invaluable resource to discuss and explore science with. Your intellect and persistence will make you an amazing PI one day. This work would not have been possible without the funding and support of multiple agencies. I extend my deepest gratitude to the HBI for the funding support and the countless programs that are offered from this institution. HBI’s countless outreach, mentorship and involvement has allowed me to develop both professionally and personally. I would like to thank the Branch out Neurological Foundation for the funding support and for the numerous outreach events that I have been involved with. I would like to thank my supportive lab and all the people that have made it so enjoyable to work in for the past few years including Adam Lognon, Shane Eaton and Dr. Charlie Kwok. You have always been an entertaining group of people, but were still there to lend an ear or a hand when needed. To Dr. Celine Jean-Xavier and Dr. Sandeep Sharma, you were great resources throughout my degree, you have both always been willing to teach me new things and provide honest feedback when necessary. To my committee, Dr. Zelma Kiss and Dr. Dave Bennett. You have helped direct my studies and focus my work. You have both been instrumental in the creation of this thesis and making me a better scientist for it. To Dr. Shalina Ousman, thank you for taking the time to read this thesis and provide comments. To Katie, you have been my rock over the past years. I can never express my gratitude for everything you do, thanks for being there for me. iv Lastly, I would like to thank my parents, Wendy and Andy Mayr, and my brother Tylor. No one has been more important and supportive than my family. You have guided me throughout my life and for this I am eternally grateful. You listened even though many times the words that escaped my mouth seemed like gibberish. Your unconditional love and support will always drive me to succeed. v Table of Contents Abstract ............................................................................................................................... ii Preface................................................................................................................................ iii Acknowledgements ............................................................................................................ iv Table of Contents ............................................................................................................... vi List of Tables .......................................................................................................................x List of Figures and Illustrations ......................................................................................... xi List of Symbols, Abbreviations and Nomenclature ......................................................... xiii CHAPTER 1 ........................................................................................................................1 1.1 Introduction ................................................................................................................1 1.1.1 The descending control of locomotion ..............................................................2 1.1.2 Central pattern generator for hindlimb locomotion ...........................................2 1.1.3 Neurotransmitters and Dopamine ......................................................................4 1.1.4 DA receptor subtypes ........................................................................................6 1.1.5 Previous work on DA and locomotion ..............................................................7 1.1.6 Decerebrate preparations ...................................................................................8 1.1.7 Motor diseases ...................................................................................................9 1.2 Importance of this research ........................................................................................9 1.3 Hypothesis ...............................................................................................................10 1.4 Aims .........................................................................................................................10 1.4.1 Aim 1: Development of a decerebrate preparation capable of producing sustained locomotor activity. ...........................................................................................10 1.4.2 Aim 2: Does intrathecal DA have an effect on locomotion in decerebrate animals on a treadmill. ..................................................................................................11 1.4.3 Aim 3: Does intrathecal DA have an effect on locomotion in the freely moving mouse ...............................................................................................................11 1.5 Figures
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