Large-scale changes in cortical dynamics triggered by repetitive somatosensory electrical stimulation

April K Hishinuma,Tanuj Gulati,Mark J Burish,Karunesh Ganguly

doi:10.1186/s12984-019-0520-1

Abstract

BackgroundRepetitive somatosensory electrical stimulation (SES) of forelimb peripheral nerves is a promising therapy; studies have shown that SES can improve motor function in stroke subjects with chronic deficits. However, little is known about how SES can directly modulate neural dynamics. Past studies using SES have primarily used noninvasive methods in human subjects. Here we used electrophysiological recordings from the rodent primary motor cortex (M1) to assess how SES affects neural dynamics at the level of single neurons as well as at the level of mesoscale dynamics.MethodsWe performed acute extracellular recordings in 7 intact adult Long Evans rats under ketamine-xylazine anesthesia while they received transcutaneous SES. We recorded single unit spiking and local field potentials (LFP) in the M1 contralateral to the stimulated arm. We then compared neural firing rate, spike-field coherence (SFC), and power spectral density (PSD) before and after stimulation.ResultsFollowing SES, the firing rate of a majority of neurons changed significantly from their respective baseline values. There was, however, a diversity of responses; some neurons increased while others decreased their firing rates. Interestingly, SFC, a measure of how a neuron’s firing is coupled to mesoscale oscillatory dynamics, increased specifically in the δ-band, also known as the low frequency band (0.3- 4 Hz). This increase appeared to be driven by a change in the phase-locking of broad-spiking, putative pyramidal neurons. These changes in the low frequency range occurred without a significant change in the overall PSD.ConclusionsRepetitive SES significantly and persistently altered the local cortical dynamics of M1 neurons, changing both firing rates as well as the SFC magnitude in the δ-band. Thus, SES altered the neural firing and coupling to ongoing mesoscale dynamics. Our study provides evidence that SES can directly modulate cortical dynamics.

Highlights

Repetitive somatosensory electrical stimulation (SES) of forelimb peripheral nerves is a promising therapy; studies have shown that SES can improve motor function in stroke subjects with chronic deficits
We found that SES could independently change both the firing rate and the phase locking, i.e. the consistency of the neural firing relative to oscillatory dynamics
We found that the motor evoked response was clearly visible in the local field potentials (LFP) and showed a large deflection during the train of pulses at 10 Hz that lasted 500 ms, i.e. with a 1% duty cycle (Fig. 1c)

Summary

Introduction

Repetitive somatosensory electrical stimulation (SES) of forelimb peripheral nerves is a promising therapy; studies have shown that SES can improve motor function in stroke subjects with chronic deficits. The somatosensory system has been shown to experience relatively rapid bidirectional changes in organization as a result of repetitive manipulations of peripheral inputs. Studies have shown that increases in afferent input by stimulating peripheral pathways (i.e. repetitive somatosensory electrical stimulation or SES) can alter sensorimotor representations of the stimulated body part [9, 10]. Hishinuma et al Journal of NeuroEngineering and Rehabilitation (2019) 16:59 determined using functional imaging [11] Consistent with these results are studies demonstrating that altered patterns of physical contacts to the fingers can persistently reorganize sensory maps [12, 13]. Repetitive SES has proven to be a promising therapeutic tool for motor rehabilitation [10, 14,15,16]

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