Abstract
BackgroundCerebellar electrical stimulation has shown promise in improving motor recovery post-stroke in both rodent and human studies. Past studies have used motor evoked potentials (MEPs) to evaluate how cerebellar stimulation modulates ongoing activity in the cortex, but the underlying mechanisms are incompletely understood. Here we used invasive electrophysiological recordings from the intact and stroke-injured rodent primary motor cortex (M1) to assess how epidural cerebellar stimulation modulates neural dynamics at the level of single neurons as well as at the level of mesoscale dynamics.MethodsWe recorded single unit spiking and local field potentials (LFPs) in both the intact and acutely stroke-injured M1 contralateral to the stimulated cerebellum in adult Long-Evans rats under anesthesia. We analyzed changes in the firing rates of single units, the extent of synchronous spiking and power spectral density (PSD) changes in LFPs during and post-stimulation.ResultsOur results show that post-stimulation, the firing rates of a majority of M1 neurons changed significantly with respect to their baseline rates. These firing rate changes were diverse in character, as the firing rate of some neurons increased while others decreased. Additionally, these changes started to set in during stimulation. Furthermore, cross-correlation analysis showed a significant increase in coincident firing amongst neuronal pairs. Interestingly, this increase in synchrony was unrelated to the direction of firing rate change. We also found that neuronal ensembles derived through principal component analysis were more active post-stimulation. Lastly, these changes occurred without a significant change in the overall spectral power of LFPs post-stimulation.ConclusionsOur results show that cerebellar stimulation caused significant, long-lasting changes in the activity patterns of M1 neurons by altering firing rates, boosting neural synchrony and increasing neuronal assemblies’ activation strength. Our study provides evidence that cerebellar stimulation can directly modulate cortical dynamics. Since these results are present in the perilesional cortex, our data might also help explain the facilitatory effects of cerebellar stimulation post-stroke.
Highlights
Cerebellar electrical stimulation has shown promise in improving motor recovery post-stroke in both rodent and human studies
Cerebellar stimulation modulates neural firing in intact Motor cortex (M1) We first analyzed the effects of cerebellar stimulation on the firing rate of M1 neurons in the intact cortex (Fig. 1)
Activation strengths of M1 cell assemblies is strengthened after epidural cerebellar stimulation Having demonstrated large-scale cerebellar stimulationdependent changes in firing rate and correlated firing among neural pairs, we examined whether cerebellar stimulation boosted the activation of M1 cell assemblies over their baseline level of activation (Stimpre) in the intact brain
Summary
Cerebellar electrical stimulation has shown promise in improving motor recovery post-stroke in both rodent and human studies. Abbasi et al J NeuroEngineering Rehabil (2021) 18:89 deep cerebellar nuclei (DCN) neurons, the principal projection neurons from the cerebellum to M1, are tuned to cues leading to movement onset and duration in reaching tasks [3,4,5,6,7,8,9,10] Purkinje cells, another principal cell type in the cerebellar cortex, are correlated to limb position, velocity, distance of limb movement and muscle activity during movement. Studies have revealed a strong link between M1 neural plasticity and motor skill acquisition [19,20,21,22] Consistent with these findings, other recent work has shown that inactivation of either area leads to a loss of kinematic precision in skilled reaching tasks [10, 23]
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