Variance in exposed perturbations impairs retention of visuomotor adaptation

• Published in: Journal of neurophysiology Vol. 118; no. 5; pp. 2745 - 2754
• Main Authors: Canaveral, Cesar Augusto, Danion, Frédéric, Berrigan, Félix, Bernier, Pierre-Michel
• Format: Journal Article
• Language: English
• Published: United States American Physiological Society 01-11-2017
• Series: Control of Movement
• Subjects: Adaptation, Physiological; Adaptation, Psychological; Adult; Analysis of Variance; Cognitive science; Female; Humans; Male; Memory; Motor Skills; Neuropsychological Tests; Neuroscience; Reaction Time; Rotation; Uncertainty; Visual Perception; Young Adult; sensorimotor adaptation; arm reaching movement; uncertainty; retention; visuomotor rotation
• ISSN: 0022-3077; 1522-1598
• DOI: 10.1152/jn.00416.2017

Sensorimotor control requires an accurate estimate of the state of the body. The brain optimizes state estimation by combining sensory signals with predictions of the sensory consequences of motor commands using a forward model. Given that both sensory signals and predictions are uncertain (i.e., noisy), the brain optimally weights the relative reliance on each source of information during adaptation. In support, it is known that uncertainty in the sensory predictions influences the rate and generalization of visuomotor adaptation. We investigated whether uncertainty in the sensory predictions affects the retention of a new visuomotor relationship. This was done by exposing three separate groups to a visuomotor rotation whose mean was common at 15° counterclockwise but whose variance around the mean differed (i.e., SD of 0°, 3.2°, or 4.5°). Retention was assessed by measuring the persistence of the adapted behavior in a no-vision phase. Results revealed that mean reach direction late in adaptation was similar across groups, suggesting it depended mainly on the mean of exposed rotations and was robust to differences in variance. However, retention differed across groups, with higher levels of variance being associated with a more rapid reversion toward nonadapted behavior. A control experiment ruled out the possibility that differences in retention were accounted for by differences in success rates. Exposure to variable rotations may have increased the uncertainty in sensory predictions, making the adapted forward model more labile and susceptible to change or decay.
The brain predicts the sensory consequences of motor commands through a forward model. These predictions are subject to uncertainty. We use visuomotor adaptation and modulate uncertainty in the sensory predictions by manipulating the variance in exposed rotations. Results reveal that variance does not influence the final extent of adaptation but selectively impairs the retention of motor memories. These results suggest that a more uncertain forward model is more susceptible to change or decay.