Individual differences in motor noise and adaptation rate are optimally related

Abstract

Individual variations in motor adaptation rate were recently shown to correlate with movement variability or \"motor noise\" in a forcefield adaptation task. However, this finding could not be replicated in a meta-analysis of visuomotor adaptation experiments. Possibly, this inconsistency stems from noise being composed of distinct components which relate to adaptation rate in different ways. Indeed, previous modeling and electrophysiological studies have suggested that motor noise can be factored into planning noise, originating from the brain, and execution noise, stemming from the periphery. Were the motor system optimally tuned to these noise sources, planning noise would correlate positively with adaptation rate and execution noise would correlate negatively with adaptation rate, a phenomenon familiar in Kalman filters. To test this prediction, we performed a visuomotor adaptation experiment in 69 subjects. Using a novel Bayesian fitting procedure, we succeeded in applying the well-established state-space model of adaptation to individual data. We found that adaptation rate correlates positively with planning noise (r=0.27; 95%HDI=[0.05 0.50]) and negatively with execution noise (r=-0.41; 95%HDI=[-0.63 -0.16]). In addition, the steady-state Kalman gain calculated from state and execution noise correlated positively with adaptation rate (r = 0.31; 95%HDI = [0.09 0.54]). These results suggest that motor adaptation is tuned to approximate optimal learning, consistent with the \"optimal control\" framework that has been used to explain motor control. Since motor adaptation is thought to be a largely cerebellar process, the results further suggest the sensitivity of the cerebellum to both planning noise and execution noise.\n\nSIGNIFICANCE STATEMENTOur study shows that the adaptation rate is optimally tuned to planning noise and execution noise across individuals. This suggests that motor adaptation is tuned to approximate optimal learning, consistent with \"optimal control\" approaches to understanding the motor system. In addition, our results imply sensitivity of the cerebellum to both planning noise and execution noise, an idea not previously considered. Finally, our Bayesian statistical approach represents a powerful, novel method for fitting the well-established state-space models that could have an influence on the methodology of the field.