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 (M1) 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. Interestingly, we found this emergent activity only in the rats that gained expertise in the task. We found that the local and cross-area spiking activity was coordinated with LFOs in proficient rats. Finally, we also found that these neural dynamics were more prominently expressed during accurate behavior in the M1. This work furthers our understanding on emergent dynamics in the cortico-cerebellar loop that underlie learning and execution of precise skilled movement.Significance StatementMovement execution involves parallel processing across brain regions, with the motor cortex (M1) being a key hub that recruits several subcortical nodes. The cerebellar cortex is a principal receiver of M1 projections via pons, but the emergent dynamics in these regions with motor skill learning is incompletely understood. We performed simultaneous recordings of M1 and cerebellum in a reach-to-grasp task. We found low frequency activity and coordinated neural dynamics emerged within and across regions with skillful task execution. Recent interest in modulating cortico-cerebellar networks for motor-recovery post-injury/stroke make this work an important precursor to assessing whether similar low-frequency activity in cortico-cerebellar networks can serve as a biomarker of motor recovery and help optimize modulation of these networks.

Cortico-cerebellar coordination facilitates neuroprosthetic control

“…S3C; 0.18 ± 0.011 to 0.27 ± 0.016, mixed-effects model: t (38) = 5.52, P = 2.5 × 10 −6 ]. 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 , 20 ).…”

“…This coherent activity may allow for flexible use of task-relevant cells in either region. The synchrony that we observed in the 3- to 6-Hz band is consistent with other work that has showed low-frequency coherence between M1 and other motor regions during learning ( 6 , 7 ). One of the possibilities for the 3- to 6-Hz increased coherence that we observed could be a result of common neural drive to both these regions (or one of the regions driving the other).…”

“…Shuttle mounted probes were moved across days and recorded from depths of 1.5 to 4 mm. Our target regions were Simplex/Crus I and Crus II areas of the cerebellum (7,(72)(73)(74). Activity in these areas has shown modulation during upper limb motor behaviors in response to corticofugal fiber and forelimb stimulation and during forelimb reaching task.…”

“…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 is also known to alter 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 whether changes in interaction are due to reciprocal connectivity between M1 and cerebellum (8)(9)(10) or because of their roles in coordinating a common target-the upper limb.…”

“…While M1-cerebellum have been simultaneously recorded ( 2 , 7 ) in upper limb behaviors, results presented from such interactions are marred by the confound of both these regions directly controlling limb movement. This confound is overcome in the brain-machine interface (BMI) task we used, where select M1 neurons (“direct” neurons) modulate their activity to control an external disembodied actuator.…”