Intensity and dose of neuromuscular electrical stimulation influence sensorimotor cortical excitability

Abstract

Neuromuscular electrical stimulation (NMES) of the peripheral nervous system has been largely used in the field of neurorehabilitation to decrease muscle atrophy and to restore motor function in paralyzed patients. The rehabilitative effects of NMES rely on the direct or indirect efferent effect on muscle tone and afferent volleys that induce cortical excitation. Although different neuroimaging tools suggested the capability of NMES to regulate the excitability of sensorimotor cortex and corticospinal circuits, to date how intensity and dose of NMES can neuromodulate the brain oscillatory activity measured with electroencephalography (EEG) is yet to be clarified. In the present study, we quantify the effect of NMES parameters on brain oscillatory activity of twelve healthy participants who underwent stimulation of wrist extensors during rest while EEG was recorded. Three different NMES intensities were included: (1) low, inducing slight sensory perception, (2) medium, inducing moderate sensory perception, and (3) high, generating a functional movement. Firstly, we efficiently removed stimulation artifacts from the sensorimotor brain oscillatory activity. Secondly, we analyzed the effect of amplitude and dose on the latter. On the one hand, we observed significant NMES amplitude-dependent brain SMR modulation, demonstrating the direct effect of afferent receptors recruitment. On the other hand, our results revealed a significant NMES amplitude-based dose-effect on SMR modulation over time. While at low and medium intensities the NMES produced a significant cortical inhibitory effect in time, at high intensity a significant cortical facilitatory effect was induced. These results highlight the functionally relevant role of muscle contraction and proprioception in sensorimotor processes, which should be carefully considered for the design and development of NMES based neuromodulation.

Peripheral Electrical Stimulation Modulates Cortical Beta-Band Activity

“…However, it should be noted that this study did not include a sham condition. Insausti-Delgado et al (2021) showed that neuromuscular electrical stimulation (NMES) over the wrist extensors resulted in an event-related desynchronization of sensorimotor alpha and beta oscillations, which was influenced by stimulation intensity. During high-intensity NMES (above motor threshold) a significantly larger alpha and beta desynchronization was present than during low- and medium-intensity stimulation (below motor threshold).…”

Non-invasive brain-spine interface: continuous brain control of trans-spinal magnetic stimulation using EEG

“…We proposed the use of a median filter, since it can eliminate high-amplitude peaks in a time-series without causing signal discontinuities (which is the main problem of blanking or interpolation). Its main limitation is that it attenuates the activity at higher frequencies (exponential attenuation between 0 Hz and the 1/ws Hz, with ws being the length of the window of the median filter) (Insausti-Delgado et al, 2020). However, this frequencydependent attenuation does not have a big impact on the sensorimotor alpha oscillations (7-first time a non-invasive closed-loop system controls the stimulation in real-time and effectively deals with these artifacts.…”

“…However, the low signal to noise ratio and artifacts often limit EEG applications. This problem aggravates when EEG is concurrently used with electromagnetic stimulation because it can contaminate the EEG signals and impede the estimation of cortical activity (Insausti-Delgado et al, 2020).…”

“…The mean and standard deviation of these two buffers, concatenated together, were used as the normalization coefficients in each iteration before passing the feature vector to the classifier. -Delgado et al, 2017-Delgado et al, , 2020. We applied the median filter as a sliding window of 20 ms in one-sample steps, calculating the median value for each window.…”

EEG Monitoring Is Feasible and Reliable during Simultaneous Transcutaneous Electrical Spinal Cord Stimulation

“…As with other stimulation-based techniques—functional electrical stimulation [ 7 ], transcranial direct current stimulation [ 8 ], transcranial alternating current stimulation (tACS) [ 9 ], deep brain stimulation [ 10 ], for example—the introduction of EEG into an experiment may present a significant challenge when it comes to interpretation, owing to substantial stimulation artifacts in the recorded signal. Stimulation is often applied at intensities far exceeding the amplitudes associated with EEG.…”