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

Abstract

Malone LA, Bastian AJ, Torres-Oviedo G. How does the motor system correct for errors in time and space during locomotor adaptation? J Neurophysiol 108: 672-683, 2012. First published April 18, 2012 doi:10.1152/jn.00391.2011.-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. human locomotion; kinematics; motor control; motor learning; walking IN OUR EVERYDAY LIVES we experience a variety of perturbations to movement and quickly learn to correct for predictable errors-we adjust walking for icy surfaces or hand movements for an unfamiliar computer mouse. We refer to this shorttimescale motor learning process as motor adaptation. Motor adaptation is defined here as an error-driven process that allows us to adjust stored movement calibrations used to make predictions of movement outcomes. So rather than constantly correcting our movements upon sustained perturbations, motor adaptation enables us to adjust sensorimotor mappings of well-learned movements when there are changes in the environment or the body (Bastian 2008;Krakauer 2009). Motor adaptation is studied by exposing subjects to novel situations (i.e., adaptation periods), where movements are initially perturbed and errors abruptly increase (Fig. 1A). To minimize these errors, movements (i.e., motor outputs) are actively modified from a preperturbation (i.e., pa...

Learning the spatial features of a locomotor task is slowed after stroke

“…Previous studies have found that spatial and temporal variables respond differently to split-belt walking and that their response is dissociable and is retained differently with repeated exposure to split-belt walking (Malone et al 2011(Malone et al , 2012Malone and Bastian 2010). Therefore both spatial (step length) and temporal (limb phasing) variables were evaluated in this study.…”

“…A number of recent studies have shown that in neurologically intact subjects spatial and temporal variables adapt at different rates and respond differently to conscious control and manipulations in practice structure during split-belt treadmill walking (Malone et al 2011(Malone et al , 2012Malone and Bastian 2010). Neurologically intact subjects walking on the split-belt treadmill adapt limb phase at a rate twice that of step length (Malone and Bastian 2010).…”

“…Neurologically intact subjects walking on the split-belt treadmill adapt limb phase at a rate twice that of step length (Malone and Bastian 2010). Moreover, temporal parameter adaptation has been shown to be much more difficult to manipulate through conscious efforts compared with spatial parameter adaptation (Malone et al 2011(Malone et al , 2012Malone and Bastian 2010). In a recent study, after various types of exposure to split-belt walking on day 1 readaptation of both step length and limb phasing was examined on day 2, to determine the effect of different practice structures on learning in neurologically intact subjects.…”

Motor learning in childhood reveals distinct mechanisms for memory retention and re-learning

“…Extended training on day 1 did not facilitate faster re-learning of phasing on day 2. Previous work has also found a dissociation between the spatial and temporal components of split-belt walking adaptation in adults (Malone et al 2012) and children (Musselman et al 2011;Vasudevan et al 2011;Patrick et al 2014), suggesting different neural substrates and/or processes for spatial and temporal adaptation. Clearly the process responsible for spatial adaptation is responsive to over-training whereas the process for temporal adaptation is not.…”

Understanding Spatial and Temporal Gait Asymmetries in Individuals Post Stroke

“…This statement is supported by empirical data that showed significant but modest correlations between step length ratio and swing time ratio (r = 0.47) and between step length ratio and stance time ratio (r = 0.58) [14]. Recent studies on locomotor adaptation during split-belt treadmill also showed that temporal parameters (phase shift) could be adapted independently of the spatial parameters (center of oscillation shift) [50][51][52]. These studies support the hypothesis that separated mechanisms are responsible for temporal and spatial gait parameters.…”