RAPID SENSORIMOTOR CONTROL IS SHAPED BY TEMPORALLY PHASED CORTICAL-CEREBELLAR ENGAGEMENT

Skilled motor control necessitates selecting appropriate voluntary actions but also rapidly reacting to unexpected change. In response to such perturbations, the nervous system utilizes sensory feedback to trigger corrective motor commands at latencies that precede conscious volition. The quickest short latency response (SLR, at ≈20 ms) is followed by a compensatory long latency response (LLR, at ≈50 ms). While the SLR seems to be generated at the spinal level, the LLR engages supraspinal loops including the cerebellum and cortex, sharing several properties with voluntary goal-directed movements. To dissect cortical and cerebellar circuits involved in LLR generation, we used transgenic mice expressing channelrhodopsin-2 in PV-positive proprioceptive afferents, cortical inhibitory neurons and cerebellar Purkinje cells. Optogenetic activation of forelimb proprioceptors triggered reliable SLR and LLR components. Simultaneous optogenetic silencing of cortical and cerebellar regions associated with forelimb proprioception produced three temporally phased effects on the LLR. Surprisingly, cerebellar silencing also modified the SLR challenging the view that it depends solely on spinal control. Furthermore, dual cortico-cerebellar silencing revealed that these regions mutually modulate one another’s influence on both of these rapid motor responses. Our results reveal the existence of temporally phased cortico-cerebellar control policies that engage multiple sensorimotor loops. We propose a hierarchical control architecture: the earliest phases involve direct cortical and cerebellar modulation of spinal networks, while subsequent phases engage longer transcortical and transcerebellar processes. Our experimental framework facilitates further functional dissection of these circuits with projection-specific manipulations to define distinct contributions of cortex and cerebellum to rapid motor control.