Abstract

Background: Pairing peripheral electrical stimulation (ES) and transcranial magnetic stimulation (TMS) increases corticospinal excitability when applied with a specific temporal pattern. When the two stimulation techniques are applied separately, motor imagery (MI)-related oscillatory modulation amplifies both ES-related cortical effects—sensorimotor event-related desynchronization (ERD), and TMS-induced peripheral responses—motor-evoked potentials (MEP). However, the influence of brain self-regulation on the associative pairing of these stimulation techniques is still unclear.Objective: The aim of this pilot study was to investigate the effects of MI-related ERD during associative ES and TMS on subsequent corticospinal excitability.Method: The paired application of functional electrical stimulation (FES) of the extensor digitorum communis (EDC) muscle and subsequent single-pulse TMS (110% resting motor threshold (RMT)) of the contralateral primary motor cortex (M1) was controlled by beta-band (16–22 Hz) ERD during MI of finger extension and applied within a brain-machine interface environment in six healthy subjects. Neural correlates were probed by acquiring the stimulus-response curve (SRC) of both MEP peak-to-peak amplitude and area under the curve (AUC) before and after the intervention.Result: The application of approximately 150 pairs of associative FES and TMS resulted in a significant increase of MEP amplitudes and AUC, indicating that the induced increase of corticospinal excitability was mediated by the recruitment of additional neuronal pools. MEP increases were brain state-dependent and correlated with beta-band ERD, but not with the background EDC muscle activity; this finding was independent of the FES intensity applied.Conclusion: These results could be relevant for developing closed-loop therapeutic approaches such as the application of brain state-dependent, paired associative stimulation (PAS) in the context of neurorehabilitation.

Highlights

  • Paired associative stimulation (PAS) has become a widely used method for inducing motor cortex (M1) plasticity

  • motor-evoked potentials (MEP) increases were brain state-dependent and correlated with beta-band event-related desynchronization (ERD), but not with the background extensor digitorum communis (EDC) muscle activity; this finding was independent of the functional electrical stimulation (FES) intensity applied. These results could be relevant for developing closed-loop therapeutic approaches such as the application of brain state-dependent, paired associative stimulation (PAS) in the context of neurorehabilitation

  • Pairing peripheral electrical stimulation (ES) with single pulse transcranial magnetic stimulation (TMS) of the contralateral M1 modulates corticospinal excitability in accordance with the specific temporal pattern between these two cortical inputs. Both cognitive factors such as attention (Stefan et al, 2004) and behavioral factors like voluntary muscle contraction (Stein et al, 2013) are known to influence the PAS effects, implying that this associative stimulation protocol is dependent on the brain state. This is further supported by the observation of preconditioning effects of other non-invasive stimulation techniques before a PAS protocol such as transcranial direct current stimulation, repetitive transcranial magnetic stimulation, theta burst stimulation (TBS; Popa et al, 2013) or PAS itself (Müller-Dahlhaus et al, 2015)

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Summary

Introduction

Paired associative stimulation (PAS) has become a widely used method for inducing motor cortex (M1) plasticity. Pairing peripheral electrical stimulation (ES) with single pulse transcranial magnetic stimulation (TMS) of the contralateral M1 modulates corticospinal excitability in accordance with the specific temporal pattern between these two cortical inputs (for review, see Carson and Kennedy, 2013). Both cognitive factors such as attention (Stefan et al, 2004) and behavioral factors like voluntary muscle contraction (Stein et al, 2013) are known to influence the PAS effects, implying that this associative stimulation protocol is dependent on the brain state. The influence of brain self-regulation on the associative pairing of these stimulation techniques is still unclear

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