Brief temporal perturbations in somatosensory reafference disrupt perceptual and neural attenuation and increase supplementary motor-cerebellar connectivity

Abstract

AbstractIntrinsic 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 the somatosensory reafference to facilitate the processing of exafferent information. Theoretically, this predictive attenuation gets disrupted by (even minimal) temporal errors between the predicted and the actual reafference, but direct evidence for such disruption is lacking since previous neuroimaging studies contrasted conditions of nondelayed reafferent input with exafferent one. 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 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 at the time of the two fingers’ contact or with a 100 ms delay. We found that such brief temporal perturbations disrupted the attenuation of the somatosensory reafference both at the perceptual and neural level, leading to greater somatosensory and cerebellar responses and weaker somatosensory connectivity with the cerebellum proportionally to perceptual changes. Moreover, we observed increased connectivity of the supplementary motor area with the cerebellum during the perturbations. We interpret these effects as the failure of the forward model to predictively attenuate the delayed somatosensory reafference and the return of the prediction error to the motor centers, respectively.Significance statementOur brain receives the somatosensory feedback of our movements with delay. To counteract these delays, motor control theories postulate that the brain predicts the timing of the somatosensory consequences of our movements and attenuates sensations received at that timing. This makes a self-generated touch feel weaker than an identical external touch. However, how subtle temporal errors between the predicted and the actual somatosensory feedback perturb this predictive attenuation remains unknown. We show that such errors make the otherwise attenuated touch feel stronger, elicit stronger somatosensory responses, weaken the cerebellar connectivity with somatosensory areas, and increase it with motor areas. These findings show that motor and cerebellar areas are fundamental in forming temporal predictions about the sensory consequences of our movements.