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Characterizing the Cortical Contributions to Working Memory-Guided Obstacle Locomotion" (2018)

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Characterizing the Cortical Contributions to Working Memory-Guided Obstacle Locomotion Western University Scholarship@Western Electronic Thesis and Dissertation Repository 9-26-2018 2:30 PM Characterizing the Cortical Contributions to Working Memory- Guided Obstacle Locomotion Carmen Wong The University of Western Ontario Supervisor Lomber, Stephen G. The University of Western Ontario Graduate Program in Neuroscience A thesis submitted in partial fulfillment of the equirr ements for the degree in Doctor of Philosophy © Carmen Wong 2018 Follow this and additional works at: https://ir.lib.uwo.ca/etd Part of the Systems Neuroscience Commons Recommended Citation Wong, Carmen, "Characterizing the Cortical Contributions to Working Memory-Guided Obstacle Locomotion" (2018). Electronic Thesis and Dissertation Repository. 5716. https://ir.lib.uwo.ca/etd/5716 This Dissertation/Thesis is brought to you for free and open access by Scholarship@Western. It has been accepted for inclusion in Electronic Thesis and Dissertation Repository by an authorized administrator of Scholarship@Western. For more information, please contact [email protected]. Abstract While walking in complex environments, the ability to acquire information about objects in our surroundings is essential for successful obstacle negotiation. Furthermore, the ease with which most animals can traverse cluttered terrain while grazing, exploring, or hunting is facilitated by the capacity to store obstacle information in working memory (WM). However, the underlying neural substrates supporting such complex behaviours are poorly understood. Therefore, the goal of this thesis is to examine the neural underpinnings of WM-guided obstacle negotiation in the walking cat. Obstacle locomotion was studied in two main paradigms, characterized by whether obstacle presence was detected via vision or touch. In both paradigms, walking was delayed following foreleg obstacle clearance. When walking resumed, elevated hindleg stepping demonstrated that animals successfully remembered the obstacle beneath them. The tactile paradigm was first examined to assess the ability of animals to remember an unexpected obstacle over which the forelegs had tripped. Such tactile input to the forelegs was capable of producing a robust, long-lasting WM of the obstacle, similar to what has been previously described using the visual paradigm. Next, to assess whether regions of the brain associated with spatial representation and movement planning contribute to these behaviours, parietal area 5 was reversibly deactivated as visual or tactile obstacle WM was tested. Such deactivations resulted in substantial WM deficits precluding successful avoidance in both paradigms. To further characterize this cortical contribution, neural activity was then recorded with multi-electrode arrays implanted in area 5. While diverse patterns of task-related modulation were observed, only a small proportion of neurons demonstrated WM-related activity. These neurons exhibited the hallmark property of sustained delay period activity associated with WM maintenance, and were able to reliably discern whether or not the animal had stepped over an obstacle prior to the delay. Therefore, only a specialized subset of area 5 neurons is capable of maintaining stable representations of obstacle information in WM. i Altogether, this work extends our understanding of WM-guided obstacle locomotion in the cat. Additionally, these findings provide insight into the neural circuitry within the posterior parietal cortex, which likely supports a variety of WM-guided behaviours. Keywords Walking, Obstacle Avoidance, Working Memory, Cat, Posterior Parietal Cortex, Area 5, Cortical Cooling, Cryoloop, Electrophysiology, Neural Activity ii Statement of Co-Authorship All data collection, analysis, and writing of the manuscripts that comprise this doctoral thesis dissertation were primarily conducted by the author of this thesis, Carmen Wong. Dr. Keir Pearson assisted with the experimental design and editing of the manuscripts for Chapters 3 and 4. Gary Wong assisted in the data collection and analysis for the manuscript for Chapter 3. Dr. Stephen Lomber provided expertise and supervision during all stages of work, including the experimental design and manuscript edits for all chapters. iii Acknowledgments This work would not have been possible without the unwavering support, encouragement, and graciousness of my supervisor, Dr. Stephen Lomber. I struggle to find ample words to articulate my gratitude and fully encapsulate how fortunate I feel to have met him as a naïve undergraduate student. His wisdom, patience, and generosity were invaluable to my development throughout graduate school. He’s one of the good ones. I also feel very fortunate that Dr. Lomber met Dr. Keir Pearson at a conference many years ago. I am thankful for the technical expertise and trust in continuing his work that Dr. Pearson has offered me throughout this process. The insights, challenges, criticisms, and reassurances that members of my advisory committee provided have also been essential to this work. I thank Dr. Brian Allman, Dr. Brian Corneil, Dr. Paul Gribble, and Dr. David Sherry for sparing their time and imparting their knowledge. To the members of the Cerebral Systems Lab throughout the years (Dr. Nicole Chabot, Pam Nixon, Gary Wong, Dr. Blake Butler, Stephen Gordon, Paisley Barnes, Melanie Kok, Dr. Daniel Stolzberg): thank you for your technical support, words of wisdom, amusing anecdotes, and sympathetic ears. To Nelson: your insistence for bad puns, dancing offbeat, racing me on runs, and supplying sushi have been constant sources of annoyance, entertainment, motivation, and comfort that have helped me retain a sense of sanity and normalcy. iv Table of Contents Abstract ................................................................................................................................ i Statement of Co-Authorship .............................................................................................. iii Acknowledgments.............................................................................................................. iv Table of Contents ................................................................................................................ v List of Figures ..................................................................................................................... x Chapter 1 ............................................................................................................................. 1 1 General Introduction ...................................................................................................... 1 1.1 Locomotor control systems in the walking cat ....................................................... 2 1.1.1 Spinal locomotor circuitry .......................................................................... 2 1.1.2 Supraspinal control of locomotion .............................................................. 6 1.2 Working memory-guided behaviours ................................................................... 11 1.2.1 Neuroanatomy of working memory .......................................................... 12 1.2.2 Delay period activity may not be required for working memory ............. 15 1.3 Working memory-guided obstacle locomotion .................................................... 16 1.4 Thesis overview .................................................................................................... 18 1.5 References ............................................................................................................. 19 Chapter 2 ........................................................................................................................... 32 2 Reversible cooling-induced deactivations to study cortical contributions to obstacle memory in the walking cat ........................................................................................... 32 2.1 Summary ............................................................................................................... 32 2.2 Abstract ................................................................................................................. 32 2.3 Introduction ........................................................................................................... 33 2.4 Protocol ................................................................................................................. 34 2.4.1 Apparatus .................................................................................................. 34 v 2.4.2 Training Procedures .................................................................................. 37 2.4.3 Behavioural Training and Testing Protocol .............................................. 38 2.4.4 Video Analyses ......................................................................................... 41 2.4.5 Cooling loop (Cryoloop) Implantation ..................................................... 42 2.4.6 Cortical Cooling Protocol ......................................................................... 42 2.4.7 Verifying the Extent of Cooling ............................................................... 49 2.5 Representative Results .......................................................................................... 49 2.6 Discussion ............................................................................................................. 52 2.7 References ............................................................................................................
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