Cortico-cerebellar coordination facilitates neuroprosthetic control

Abstract

Temporal coordination among neurons and development of functional neuronal assemblies is central to nervous system function and purposeful behavior. Still, there is a paucity of evidence about how functional coordination emerges in neuronal assemblies in cortical and subcortical regions that are directly related to the control of functional output. We investigated emergent neural dynamics between primary motor cortex (M1) and the contralateral cerebellar cortex as rats learned a neuroprosthetic/ brain-machine interface (BMI) task. BMIs offer a powerful tool to causally test how distributed neural networks achieve specific neural patterns. During neuroprosthetic learning, actuator movements are causally linked to primary motor cortex (M1) neurons, i.e., direct neurons, that project to the decoder and whose firing is required to successfully perform the task. However, it is unknown how such direct M1 activity interacts with cerebellar activity. We observed a striking 3-6 Hz coherence that emerged between these regions local-field potentials (LFPs) with neuroprosthetic learning which also modulated task-related spiking. We found a robust task-related indirect modulation in the cerebellum, and we found that it became synchronous with M1-direct activity with learning. We also performed optogenetic inhibition of cerebellar activity and found that this led to performance impairments in neuroprosthetic control. Together, these results demonstrate that coordinated neural dynamics emerge in cortico-cerebellar regions during neuroprosthetic learning which supports task-relevant activity in M1 direct neuronal populations, and further, that cerebellar influence is necessary for M1-driven rapid direct neural control.