How does the motor system correct for errors in time and space during locomotor adaptation?

Walking is a complex behavior for which the healthy nervous system favors a smooth, symmetric pattern. However, people often adopt an asymmetric walking pattern after neural or biomechanical damage (i.e., they limp). To better understand this aberrant motor pattern and how to change it, we studied walking adaptation to a split-belt perturbation where one leg is driven to move faster than the other. Initially, healthy adult subjects take asymmetric steps on the split-belt treadmill, but within 10-15 min people adapt to reestablish walking symmetry. Which of the many walking parameters does the nervous system change to restore symmetry during this complex act (i.e., what motor mappings are adapted to restore symmetric walking in this asymmetric environment)? Here we found two parameters that met our criteria for adaptive learning: a temporal motor output consisting of the duration between heel-strikes of the two legs (i.e., "when" the feet land) and a spatial motor output related to the landing position of each foot relative to one another (i.e., "where" the feet land). We found that when subjects walk in an asymmetric environment they smoothly change their temporal and spatial motor outputs to restore temporal and spatial symmetry in the interlimb coordination of their gait. These changes in motor outputs are stored and have to be actively deadapted. Importantly, the adaptation of temporal and spatial motor outputs is dissociable since subjects were able to adapt their temporal motor output without adapting the spatial output. Taken together, our results suggest that temporal and spatial control for symmetric gait can be adapted separately, and therefore we could potentially develop interventions targeting either temporal or spatial walking deficits.

[1]  Sarah E. Criscimagna-Hemminger,et al.  Size of error affects cerebellar contributions to motor learning. , 2010, Journal of neurophysiology.

[2]  D. Armstrong,et al.  Step phase‐related excitability changes in spino‐olivocerebellar paths to the c1 and c3 zones in cat cerebellum. , 1995, The Journal of physiology.

[3]  D. Ryczko,et al.  Chapter 4--supraspinal control of locomotion: the mesencephalic locomotor region. , 2011, Progress in brain research.

[4]  D. Yanagihara,et al.  Nitric oxide plays a key role in adaptive control of locomotion in cat. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[5]  F A Mussa-Ivaldi,et al.  Adaptive representation of dynamics during learning of a motor task , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[6]  A. Bastian,et al.  Thinking about walking: effects of conscious correction versus distraction on locomotor adaptation. , 2010, Journal of neurophysiology.

[7]  Amy J Bastian,et al.  Seeing Is Believing: Effects of Visual Contextual Cues on Learning and Transfer of Locomotor Adaptation , 2010, The Journal of Neuroscience.

[8]  J. Eian,et al.  Dorsal spinocerebellar tract neurons respond to contralateral limb stepping , 2003, Experimental Brain Research.

[9]  J. Krakauer,et al.  A computational neuroanatomy for motor control , 2008, Experimental Brain Research.

[10]  Amy J Bastian,et al.  Motor Adaptation Training for Faster Relearning , 2011, The Journal of Neuroscience.

[11]  D. Reisman,et al.  Split-Belt Treadmill Adaptation Transfers to Overground Walking in Persons Poststroke , 2009, Neurorehabilitation and neural repair.

[12]  J. Halbertsma The stride cycle of the cat: the modelling of locomotion by computerized analysis of automatic recordings. , 1983, Acta physiologica Scandinavica. Supplementum.

[13]  S. Rossignol,et al.  The locomotion of the low spinal cat. II. Interlimb coordination. , 1980, Acta physiologica Scandinavica.

[14]  D M Wolpert,et al.  Multiple paired forward and inverse models for motor control , 1998, Neural Networks.

[15]  D. Reisman,et al.  Locomotor adaptation on a split-belt treadmill can improve walking symmetry post-stroke. , 2007, Brain : a journal of neurology.

[16]  John W Krakauer,et al.  Motor learning and consolidation: the case of visuomotor rotation. , 2009, Advances in experimental medicine and biology.

[17]  Okihide Hikosaka,et al.  Effects of motivational conflicts on visually elicited saccades in monkeys , 2003, Experimental Brain Research.

[18]  Julia T. Choi,et al.  Adaptation reveals independent control networks for human walking , 2007, Nature Neuroscience.

[19]  T. Drew,et al.  Contributions of the motor cortex to the control of the hindlimbs during locomotion in the cat , 2002, Brain Research Reviews.

[20]  David A McVea,et al.  Object avoidance during locomotion. , 2009, Advances in experimental medicine and biology.

[21]  T. Drew,et al.  Contribution of the motor cortex to the structure and the timing of hindlimb locomotion in the cat: a microstimulation study. , 2005, Journal of neurophysiology.

[22]  J. Krakauer,et al.  Sensory prediction errors drive cerebellum-dependent adaptation of reaching. , 2007, Journal of neurophysiology.

[23]  A. Ruina,et al.  A collisional model of the energetic cost of support work qualitatively explains leg sequencing in walking and galloping, pseudo-elastic leg behavior in running and the walk-to-run transition. , 2005, Journal of theoretical biology.

[24]  D. Zee,et al.  Ocular motor disorders associated with cerebellar lesions: pathophysiology and topical localization. , 1993, Revue neurologique.

[25]  Richard Apps,et al.  Simple spike discharge patterns of Purkinje cells in the paramedian lobule of the cerebellum during locomotion in the awake cat , 1989, Neuroscience Letters.

[26]  S. M. Morton,et al.  Cerebellar Contributions to Locomotor Adaptations during Splitbelt Treadmill Walking , 2006, The Journal of Neuroscience.

[27]  Kurt A. Thoroughman,et al.  Trial-by-trial transformation of error into sensorimotor adaptation changes with environmental dynamics. , 2007, Journal of neurophysiology.

[28]  A. Bastian Understanding sensorimotor adaptation and learning for rehabilitation , 2008, Current opinion in neurology.

[29]  T. Drew Motor cortical activity during voluntary gait modifications in the cat. I. Cells related to the forelimbs. , 1993, Journal of neurophysiology.

[30]  T. Drew,et al.  Cortical and brainstem control of locomotion. , 2004, Progress in brain research.

[31]  R. Poppele,et al.  Proprioception from a spinocerebellar perspective. , 2001, Physiological reviews.

[32]  T. Ebner,et al.  Hereditary cerebellar ataxia progressively impairs force adaptation during goal-directed arm movements. , 2004, Journal of neurophysiology.

[33]  R. Shadmehr,et al.  Interacting Adaptive Processes with Different Timescales Underlie Short-Term Motor Learning , 2006, PLoS biology.

[34]  Young-Hui Chang,et al.  An in vitro spinal cord-hindlimb preparation for studying behaviorally relevant rat locomotor function. , 2009, Journal of neurophysiology.

[35]  D. Robinson,et al.  Absence of a stretch reflex in extraocular muscles of the monkey. , 1971, Journal of neurophysiology.

[36]  Reza Shadmehr,et al.  Some Perspectives on Saccade Adaptation , 2009, Annals of the New York Academy of Sciences.

[37]  Hannah J. Block,et al.  Interlimb coordination during locomotion: what can be adapted and stored? , 2005, Journal of neurophysiology.

[38]  Amy J Bastian,et al.  Walking flexibility after hemispherectomy: split-belt treadmill adaptation and feedback control. , 2009, Brain : a journal of neurology.

[39]  John W. Krakauer,et al.  Independent learning of internal models for kinematic and dynamic control of reaching , 1999, Nature Neuroscience.

[40]  Erin V. L. Vasudevan,et al.  Younger Is Not Always Better: Development of Locomotor Adaptation from Childhood to Adulthood , 2011, The Journal of Neuroscience.