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Sleep-Dependent Consolidation of Locomotor Sequence Learning and Locomotor Adaptation

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Sleep-Dependent Consolidation of Locomotor Sequence Learning and Locomotor Adaptation University of Massachusetts Amherst ScholarWorks@UMass Amherst Doctoral Dissertations Dissertations and Theses July 2019 SLEEP-DEPENDENT CONSOLIDATION OF LOCOMOTOR SEQUENCE LEARNING AND LOCOMOTOR ADAPTATION Gabriela Borin Castillo University of Massachusetts Amherst Follow this and additional works at: https://scholarworks.umass.edu/dissertations_2 Part of the Motor Control Commons Recommended Citation Borin Castillo, Gabriela, "SLEEP-DEPENDENT CONSOLIDATION OF LOCOMOTOR SEQUENCE LEARNING AND LOCOMOTOR ADAPTATION" (2019). Doctoral Dissertations. 1621. https://doi.org/10.7275/1sa6-r798 https://scholarworks.umass.edu/dissertations_2/1621 This Open Access Dissertation is brought to you for free and open access by the Dissertations and Theses at ScholarWorks@UMass Amherst. It has been accepted for inclusion in Doctoral Dissertations by an authorized administrator of ScholarWorks@UMass Amherst. For more information, please contact [email protected]. SLEEP-DEPENDENT CONSOLIDATION OF LOCOMOTOR SEQUENCE LEARNING AND LOCOMOTOR ADAPTATION A Dissertation Presented by GABRIELA BORIN CASTILLO Submitted to the Graduate School of the University of Massachusetts Amherst in partial fulfillment of the requirements for the degree of DOCTOR OF PHILOSOPHY May 2019 Department of Kinesiology © Copyright by Gabriela Borin Castillo 2019 All Rights Reserved ii SLEEP-DEPENDENT CONSOLIDATION OF LOCOMOTOR SEQUENCE LEARNING AND LOCOMOTOR ADAPTATION A Dissertation Presented by GABRIELA BORIN CASTILLO Approved as to style and content by: ______________________________________ Julia T. Choi, Chair ______________________________________ Richard E.A. Van Emmerik, Member ______________________________________ Rebecca M.C. Spencer, Member ___________________________________ Jane A. Kent, Department Chair Department of Kinesiology iii DEDICATION To my family for all of your love iv ACKNOWLEDGEMENTS I would like to express my sincere gratitude to my committee chair and graduate advisor Dr. Julia T. Choi, for her patience, motivation, and immense knowledge. Her guidance has made this a thoughtful and rewarding journey. I am also grateful to my dissertation committee members, Dr. Rebecca M.C. Spencer and Dr. Richard E.A. Van Emmerik for their insightful comments, encouragement and support. I would also like to thank all members of the UMass Locomotion Neuromechanics Laboratory, with a special acknowledgment to Jan Stenun, Daniel Gregory, Sumire Sato and Dane Napoli, for their continued support and partnership. I thank all the UMass Kinesiology faculties and students for sharing your knowledge and experience with me. Also, thanks to all members of the UMass Kinesiology Staff for their assistance during these years. Finally, I would like to thank each individual who have been a source of inspiration and encouragement and helped me all the way through this journey. v ABSTRACT SLEEP-DEPENDENT CONSOLIDATION OF MOTOR SEQUENCE LEARNING AND MOTOR ADAPTATION IN HUMAN LOCOMOTION MAY 2019 GABRIELA BORIN CASTILLO B.S., UNIVERSITY OF SÃO PAULO, BRAZIL M.S., UNIVERSITY OF SÃO PAULO, BRAZIL Ph.D., UNIVERSITY OF MASSACHUSETTS AMHERST, UNITED STATES Directed by: Julia T. Choi, Ph.D. Walking is a complex task that requires precise coordination of many muscles and joints. The nervous system must continually learn how to control gait patterns as changes occur to the body (e.g., injury and fatigue) or environment (e.g., slippery floor). Motor learning refers to processes that improve the spatial and/or temporal accuracy of a movement through motor practice. Although additional hours of practice can improve motor skill performance (online learning), time without additional practice (offline learning) can further enhance motor learning. Consolidation refers to the process by which motor (procedural) memory becomes more robust and stable after the end of a practice session. Recent studies have demonstrated that considerable consolidation may occur, either preferentially or exclusively, during sleep. This is referred to as sleep- dependent consolidation. The aim of this dissertation was to examine the role of sleep in the consolidation in two different locomotor tasks: locomotor sequence learning and locomotor adaptation. vi In the first study, participants practiced a sequence of visually cued step lengths during forward walking. Participants were subsequently tested, either with an untrained gait pattern (backward walking) using the same visual cues to probe transfer in the perceptual domain, or with the same gait pattern using different visual cues (inverted screen) to probe transfer in the motor domain. Transfer was assessed immediately (immediate transfer), and 12 h later (delayed transfer), following overnight sleep or a period of daytime alertness. We found minimal immediate transfer in the perceptual domain; however, the backward pattern improved by about 10% following a 12-h interval that included sleep. In contrast, the backward pattern only improved by around 1% following a 12-h interval awake. This suggest that sleep was important for delayed generalization of perceptual learning. Transfer in the motor domain was similarly improved over a 12-h interval, with or without sleep, indicating that time-dependent processes were involved in delayed transfer of motor learning. In the second study, participants performed a split-belt treadmill walking task with a 2:1 speed ratio over 15 min of training. Savings (i.e., faster re-adaptation) of the 2:1 split-belt walking pattern were assessed immediately (immediate savings), and again 12 h later (delayed savings) following an awake period (awake group), or an identical period of time that included sleep (sleep group). Participants in the sleep group showed delayed savings in step length symmetry compared with those in the awake group, suggesting that sleep was beneficial for spatial locomotor adaptation. Temporal locomotor adaptations showed immediate savings, but delayed savings were not enhanced after a 12-h awake period or 12-h period that included sleep. vii In sum, we showed that consolidation of locomotor skills involves both parallel and distinct processes for motor and perceptual learning, as well as spatial and temporal control of gait. Some of these processes appear to preferentially or exclusively operate during sleep. The nervous system’s ability to differentially respond to various training schedules should enable clinicians to tailor rehabilitation regimes for gait recovery while maximizing rehabilitation outcomes and training efficiency. These appear to be of equal or possibly greater importance than the actual amount of practice. viii TABLE OF CONTENTS Page ACKNOWLEDGEMENTS ............................................................................................ v ABSTRACT .................................................................................................................. vi LIST OF TABLES ....................................................................................................... viii LIST OF FIGURES ..................................................................................................... ixx CHAPTER 1. INTRODUCTION ...................................................................................................... 1 1.1 Background .................................................................................................. 1 1.2 Significance ................................................................................................... 6 1.3 Specific Aims ............................................................................................... 7 2. LITERATURE REVIEW .......................................................................................... 12 2.1 Human locomotion ..................................................................................... 12 2.1.1 Inter-limb coordination during walking ......................................... 13 2.1.2 Visually guided walking ................................................................ 13 2.1.3 Neural mechanisms of locomotion ................................................. 15 2.2. Motor Learning ........................................................................................... 18 2.2.1 Locomotor Sequence Learning ...................................................... 20 2.2.2 Locomotor adaptation .................................................................... 23 2.3. Consolidation of motor learning .................................................................. 28 2.3.1 Sleep-dependent consolidation ...................................................... 30 3. METHODS ............................................................................................................... 48 3.1 Overview of approach ................................................................................. 48 3.2 Participants ................................................................................................. 48 3.3 Functional assessments ............................................................................... 50 3.4 Specific Aim 1: To investigate the consolidation of locomotor sequence learning ................................................................................... 50 3.4.1 Experimental set-up ....................................................................... 50 3.4.2 Experimental design ...................................................................... 52 3.4.3 Data collection .............................................................................
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