Individual differences in proprioception predict the extent of implicit sensorimotor adaptation

Abstract

Recent studies have revealed an upper bound in motor adaptation, beyond which other learning systems may be recruited. The factors determining this upper bound are poorly understood. The multisensory integration hypothesis states that this limit arises from opposing responses to visual and proprioceptive feedback. As individuals adapt to a visual perturbation, they experience an increasing proprioceptive error in the opposite direction, and the upper bound is the point where these two error signals reach an equilibrium. Assuming that visual and proprioceptive feedback are weighted according to their variability, there should be a correlation between proprioceptive variability and the limits of adaptation. Alternatively, the proprioceptive realignment hypothesis states that the upper bound arises when the (biased) sensed hand position realigns with the target. When a visuo-proprioceptive discrepancy is introduced, the sensed hand position is biased towards the visual cursor and the adaptive system nullifies this discrepancy by driving the hand away from the target. This hypothesis predicts a correlation between the size of the proprioceptive shift and the upper bound of adaptation. We tested these two hypotheses by considering natural variation in proprioception and motor adaptation across individuals. We observed a modest, yet reliable correlation between the upper bound of adaptation with both proprioceptive measures (variability and shift). While these results do not favor one hypothesis over the other, they underscore the critical role of proprioception in sensorimotor adaptation, and moreover, motivate a novel perspective on how these proprioceptive constraints drive implicit changes in motor behavior. SIGNIFICANCE STATEMENTWhile the sensorimotor system uses sensory feedback to remain properly calibrated, this learning process is constrained, limited in the maximum degree of plasticity. The factors determining this limit remain elusive. Guided by two hypotheses concerning how visual and proprioceptive information are integrated, we show that individual differences in the upper bound of adaptation in response to a visual perturbation can be predicted by the bias and variability in proprioception. These results underscore the critical, but often neglected role of proprioception in human motor learning.