The relationship between cerebral and cerebellar activity changes from preparation to motor execution

Circuits connecting the cerebral cortex and cerebellum are essential for sensorimotor control. How do the primary sensorimotor cortical activity and cerebellar activity affect each other during voluntary movement? Whereas the specific anatomical connections have been elucidated in great detail, the neural dynamics that drive sensorimotor behaviour are still unclear. We recorded from primary sensorimotor cortices and cerebellum during whisking in mice and intermittently optogenetically manipulated their activity. Here we unveil that the direction of signals between the cerebral cortex and the cerebellum varies depending on the phase (i.e., planning, execution) of innate voluntary movement. Before movement onset, the neuronal activity of the primary motor cortex (M1) and somatosensory (S1) correlated with Purkinje cell activity of the crus regions, with a lag consistent with the cerebellum receiving copy of motor command. After the movement onset, the lag of the correlation inverted suggesting a dominant vector signalling from the cerebellum to the cerebrum. With optogenetic neocortical stimulation of S1 or M1, we identified a restricted region of lateral crus regions integrating neuronal activity of the cortico-ponto-cerebellar and cortico-olivary pathways. Activation of this pathway drives whisker movement, the amplitude and the velocity of which are modulated by a cerebro-cerebellar feedback mechanism. Our findings reveal the circuit mechanism for cerebro-cerebellar motor control inferred by previous anatomical and computational studies.