Implicit motor adaptation and perceived hand position without proprioception: A kinesthetic error may be derived from efferent signals

Abstract

Our ability to produce successful goal-directed actions involves multiple learning processes. Among these, implicit adaptation is of utmost importance, keeping our sensorimotor system well-calibrated in response to changes in the body and environment. Implicit adaptation is assumed to be driven by a sensory prediction error, the difference between the predicted and actual sensory consequences of a movement. Whereas most models of implicit adaptation have focused on how visual information defines the sensory prediction error, we have recently proposed that this error signal is kinesthetic, the difference between the desired and perceived hand position, with adaptation serving to align these two signals and restore optimal motor performance (Tsay et al., 2022). Here, we examined implicit adaptation and kinesthetic perception in rare individuals who lack proprioceptive signals from the upper limbs. We used a visuomotor rotation task designed to isolate implicit adaptation while simultaneously probing the participants’ perceived hand position. Consistent with prior work, control participants exhibited robust implicit adaptation and the signature of kinesthetic re-alignment, an initial bias in perceived hand position towards the visual cursor and a gradual shift back to the movement goal. Strikingly, the time course of both implicit adaptation and kinesthetic re-alignment was preserved in the deafferented group, suggesting that proprioceptive afferents are not necessary for implicit adaptation and kinesthetic re-alignment. We propose that a kinesthetic prediction error derived from efferent motor signals is sufficient to drive implicit adaptation and to re-algin a biased percept of hand position with the movement goal.