A rare case of deafferentation reveals an essential role of proprioception in bilateral coordination

Abstract

Loss of proprioception has been shown to produce deficits in intralimb coordination and in the ability to stabilize limb posture in the absence of visual feedback. However, the role of proprioceptive signals in the feedforward and feedback control of interlimb coordination remains unclear. To address this issue, we examined bimanual coordination in a deafferented participant (DP) with large-fiber sensory neuropathy, which resulted in the loss of proprioception and touch in both arms, and in age-matched control participants. The task required participants to move a single virtual bar with both hands to a rectangular target with horizontal orientation. The participants received visual feedback of the virtual bar, but not of the hand positions along the bar-axis. Although the task required symmetrical movement between the arms, there were significant differences in the trajectories of the dominant and non-dominant hands in the deafferented participant, and thus more final errors and impaired coordination compared to controls. Deafferentation was also associated with an asymmetric deficit in stabilizing the hand at the end of motion, where the dominant arm showed more drift than the non-dominant arm. While the findings with DP may reflect a unique adaptation to deafferentation, they suggest that 1) Bilateral coordination depends on proprioceptive feedback, and 2) Postural stability at the end of motion can be specified through feedforward mechanisms, in the absence of proprioceptive feedback, but this process appears to be asymmetric, with better stability in the non-dominant arm.