Cortico-cerebellar coordination facilitates neuroprosthetic learning

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 task-related neuronal assemblies in cortical and subcortical regions that are 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 activation. During neuroprosthetic learning, actuator movements are causally linked to primary motor cortex (M1) neurons, i.e., "direct" neurons, that drive the decoder and whose firing is required to successfully perform the task. However, it is unknown how task-related 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 this activity developed a preferential relationship with M1 task-related direct and indirect activity but not with M1 task unrelated activity with learning. We also performed optogenetic inhibition of cerebellar activity (in the cerebellar cortex and its deep nuclei) and found that this led to performance impairments in M1-driven 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 neuronal populations, and further, that cerebellar influence is necessary for M1-driven neuroprosthetic control.