Role of the Cerebellum in Adaptation to Delayed Action Effects

• Published in: Current biology Vol. 27; no. 16; pp. 2442 - 2451.e3
• Main Authors: Cao, Liyu, Veniero, Domenica, Thut, Gregor, Gross, Joachim
• Format: Journal Article
• Language: English
• Published: England Elsevier Ltd 21.08.2017; Cell Press
• Subjects: Adaptation, Physiological; Adult; Auditory Perception; cerebellum; Cerebellum - physiology; Female; forward model; Humans; Magnetoencephalography; Male; MEG; sensory attenuation; Time Factors; TMS; Transcranial Magnetic Stimulation; Visual Perception; Young Adult; TMS; forward model; sensory attenuation; cerebellum; MEG
• ISSN: 0960-9822; 1879-0445
• DOI: 10.1016/j.cub.2017.06.074

Actions 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. •Adaptation of M100 attenuation for delayed action effects was localized in cerebellum•Cerebellar stimulation abolished the adaptation of M100 attenuation•M200 attenuation reversed after cerebellar stimulation•Cerebellar low-frequency activity may be important for forward model updating Cao et al. show that the adaptation to delayed action effects disappears after an inhibitory cerebellar stimulation with TMS, highlighting the cerebellum’s role in forward model updating. The stimulation also changes cerebellar low-frequency activity and evokes responses in the frontal brain area, suggesting a processing hierarchy for prediction errors.