Role of the Cerebellum in Adaptation to Delayed Action Effects

Abstract

SummaryActions are typically associated with sensory consequences. For example, knocking at a door results in predictable sounds. These self-initiated sensory stimuli are known to elicit smaller cortical responses compared to passively presented stimuli, e.g., early auditory evoked magnetic fields known as M100 and M200 components are attenuated. Current models implicate the cerebellum in the prediction of the sensory consequences of our actions. However, causal evidence is largely missing. In this study, we introduced a constant delay (of 100 ms) between actions and action-associated sounds, and we recorded magnetoencephalography (MEG) data as participants adapted to the delay. We found an increase in the attenuation of the M100 component over time for self-generated sounds, which indicates cortical adaptation to the introduced delay. In contrast, no change in M200 attenuation was found. Interestingly, disrupting cerebellar activity via transcranial magnetic stimulation (TMS) abolished the adaptation of M100 attenuation, while the M200 attenuation reverses to an M200 enhancement. Our results provide causal evidence for the involvement of the cerebellum in adapting to delayed action effects, and thus in the prediction of the sensory consequences of our actions.

Beta‐band oscillations play an essential role in motor–auditory interactions

“…This result is consistent with previous studies and demonstrates how actions can modulate auditory processing (Cao, Thut, & Gross, ; Cao, Veniero, et al, ; Hughes, Desantis, & Waszak, ; Martikainen et al, ; Schneider & Mooney, ). The term sensory attenuation has been used for the M100 amplitude suppression for a long time (Cao, Thut, & Gross, ; Cao, Veniero, et al, ; Hughes et al, ; Wolpe et al, ). One possible function of neurons generating M100 is to call attention to the availability of stimulus information (Näätänen & Picton, ).…”

“…Our results also demonstrate functional connectivity from motor to auditory cortex in alpha range before the stimulus onset for active condition. This result extends previous observations that prestimulus changes in alpha oscillations in auditory cortex during movement preparation (Cao, Thut, & Gross, ; Cao, Veniero, et al, ; Müller, Leske, Hartmann, Szebényi, & Weisz, ; Stenner, Bauer, Haggard, Heinze, & Dolan, ) shape the processing of incoming sensory stimuli. In fact, Granger causality from motor to LAC (Figure ) suggests a spectral connectivity pattern that shifts from alpha frequencies before tone onset to beta frequencies just after tone onset.…”

“…We report significant beta power decrease in left and right auditory cortex following stimulus onset in the active condition compared to the passive condition. This replicates a similar finding in right auditory cortex in a similar task (Cao, Thut, & Gross, ; Cao, Veniero, et al, ) and suggests an interaction between motor and auditory cortex in this frequency band. Indeed, we observed two interactions.…”

“…Cao et al demonstrated a correlation between the prestimulus alpha increase in auditory cortex and the magnitude of sensory attenuation indicating a downregulation of auditory excitability when predicted self‐generated sensory input is expected (Cao, Thut, & Gross, ; Cao, Veniero, Thut, & Gross, ). In line with the above‐mentioned functional differentiation between different oscillations, gamma‐band changes in response to self‐generated stimuli seem to reflect prediction errors (Buchholz, David, Sengelmann, & Engel, ; Cao, Thut, & Gross, ; Cao, Veniero, et al, ; Flinker et al, ). These prediction errors are computed by comparing real sensory input and the sensory input that is predicted on the basis of the motor command by the internal forward model.…”

Corollary Discharge versus Efference Copy: Distinct Neural Signals in Speech Preparation Differentially Modulate Auditory Responses

“…It dissociates from specific actions that the system will engage, as we observed ubiquitous inhibition in auditory responses to all syllables. Moreover, the CD is probably independent of what motor effectors the actions would be executed by, as the auditory suppression was also observed by manual buttonpress (Bäß et al, 2008;Cao et al, 2017;Horváth et al, 2012). Furthermore, the CD is probably general inhibitory motor signals that are available across visual (Sommer & Wurtz, 2006), auditory (Poulet & Hedwig, 2006), and somatosensory (Sarah-J.…”