Brief Temporal Perturbations in Somatosensory Reafference Disrupt Perceptual and Neural Attenuation and Increase Supplementary Motor Area-Cerebellar Connectivity

Abstract

Intrinsic delays in sensory feedback can be detrimental for motor control. As a compensation strategy, the brain predicts the sensory consequences of movement via a forward model on the basis of a copy of the motor command. Using these predictions, the brain attenuates somatosensory reafference to facilitate the processing of exafferent information. Theoretically, this predictive attenuation is disrupted by (even minimal) temporal errors between the predicted and actual reafference; however, direct evidence of such disruption is lacking as previous neuroimaging studies contrasted nondelayed reafferent input with exafferent input. Here, we combined psychophysics with functional magnetic resonance imaging to test whether subtle perturbations in the timing of somatosensory reafference disrupt its predictive processing. Twenty-eight participants (14 women) generated touches on their left index finger by tapping a sensor with their right index finger. The touches on the left index finger were delivered close to the time of contact of the two fingers or with a temporal perturbation (i.e., 153ms delay). We found that such a brief temporal perturbation disrupted the attenuation of the somatosensory reafference at both the perceptual and neural levels, leading to greater somatosensory and cerebellar responses and weaker somatosensory connectivity with the cerebellum, proportional to the perceptual changes. We interpret these effects as the failure of the forward model to predictively attenuate the perturbed somatosensory reafference. Moreover, we observed increased connectivity of the supplementary motor area with the cerebellum during the perturbations, which could indicate the communication of the temporal prediction error back to the motor centers.