Emergent low-frequency activity in cortico-cerebellar networks with motor skill learning

Abstract

The motor cortex controls skilled arm movement by recruiting a variety of targets in the nervous system, and it is important to understand the emergent activity in these regions as refinement of a motor skill occurs. One fundamental projection of the motor cortex is to the cerebellum. However, the emergent activity in the motor cortex and the cerebellum that appears as a dexterous motor skill is consolidated is incompletely understood. Here, we report on low-frequency oscillatory (LFO) activity that emerges in cortico-cerebellar networks with learning the reach-to-grasp motor skill. We chronically recorded the motor and the cerebellar cortices in rats which revealed the emergence of coordinated movement-related activity in the local-field potentials (LFPs) as the reaching skill consolidated. We found that the local and cross-area spiking activity was coordinated with LFOs. Finally, we also found that these neural dynamics were more prominently expressed during accurate behavior. This work furthers our understanding on emergent dynamics in the cortico-cerebellar loop that underlie learning and execution of precise skilled movement.

Cortico-cerebellar coordination facilitates neuroprosthetic control

“…2f, g; 0.16 ± 0.01 to 0.22 ± 0.013, mixed-effects model: t (44) = 4.6, P = 2.5 × 10 −5 ). This emergence of cross-region low-frequency activity is consistent with other observations of emergence of low-frequency activity during motor skill learning across reciprocally connected neural networks 7 .…”

“…Such coherent activity may allow for flexible use of task-relevant cells in either region. The synchrony that we observed in 3-6 Hz band is consistent with other work that has showed low-frequency coherence between M1 and other motor regions during learning 6, 7 .…”

“…Work that has looked at extensively trained mice on motor task has shown sustained activity in the cerebellum 42 . There is further evidence from studies of natural learning that emergent activity in cortico-cerebellar networks becomes stronger as task proficiency increases 7 .…”

“…We did not perform subject-specific implantation based on motor mapping. However, a subset of rats also performed reaching tasks and had robust activation during reaching 7 .…”

“…Two motor regions, the primary motor cortex (M1) and the cerebellum, have dense reciprocal connections, and are known to be involved in motor learning 1,2 . Studies have shown how learning alters local activity in the cerebellum or M1 [3][4][5][6] , yet learning also alters task-related cross area coordination 2,7 . Both M1 and the cerebellum have dense connections with other cortical and subcortical regions, and hence it is difficult to ascertain if changes in interaction are because of direct interactions between M1 and cerebellum [8][9][10] , or because of their roles coordinating the upper limb.…”