Motor prediction reduces beta-band power and enhances cerebellar-somatosensory connectivity before self-touch to enable its attenuation

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Abstract

Prevailing theories suggest that the brain uses an internal forward model to predict tactile input during voluntary movements, thereby reducing the intensity of the reafferent tactile sensation, a phenomenon known as self-touch attenuation. Although self-touch attenuation is a well- documented effect, it remains unclear how prediction-related neural mechanisms drive the attenuation prior to the actual self-touch input. In this study, we used magnetoencephalography (MEG) to examine the neural correlates of self-touch prediction. Participants performed a self-touch task with two control conditions. In one control, the touch was externally generated without any movement. In the other, the moving and the touched hands were spatially misaligned, thereby disrupting the sensorimotor alignment of self-touch. Self-touch evoked weaker early somatosensory activity (M50 component) than both control conditions. A psychophysics task also mirrored the pattern of neural attenuation, as the perception of self-touch was attenuated compared to the two control conditions. To isolate predictive neural mechanisms from general movement-related activity, we subtracted activity from corresponding stimulus-absent trials. To further refine the signal specific to predictive processing in self-touch, we compared self-touch with misaligned touch, the two conditions that both involved voluntary movement but differed in their prediction of self-touch. This revealed greater pre-stimulus beta-band desynchronization and increased cerebellar-to-somatosensory connectivity prior to self-touch compared to misaligned touch. Our results provide the first evidence of predictive neural activity that shapes the sensory consequences of self-touch, offering insight into the mechanisms through which predictive models modulate somatosensory processing.

Significance statement

The brain is thought to predict and attenuate the sensory consequences of self-generated actions, but neural evidence for such prediction before sensation has been limited. Using magnetoencephalography, we show that self-touch attenuation is preceded by beta-band desynchronization and increased directed connectivity from the cerebellum to the primary somatosensory cortex. These effects cannot be attributed to movement, as they were not observed in a control condition with similar motor output but without predicted self-touch consequences, suggesting they reflect predictive processing. Our study provides the first neural evidence of cerebellar influence on cortical sensory areas before self-touch. These pre-stimulus effects strongly support predictive forward models of sensorimotor control and shed new light on how the brain anticipates and modulates upcoming sensory input.

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