Modulatory Effects of Motor State During Paired Associative Stimulation on Motor Cortex Excitability and Motor Skill Learning.

Jacqueline A Palmer,Steven L Wolf,Michael R Borich,Alice Halter,Whitney Gray

doi:10.3389/fnhum.2019.00008

Jacqueline A Palmer, Steven L Wolf + Show 3 more

Open Access

https://doi.org/10.3389/fnhum.2019.00008

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Abstract

Repeated pairing of electrical stimulation of a peripheral nerve with transcranial magnetic stimulation (TMS) over the primary motor cortex (M1) representation for a target muscle can induce neuroplastic adaptations in the human brain related to motor learning. The extent to which the motor state during this form of paired associative stimulation (PAS) influences the degree and mechanisms of neuroplasticity or motor learning is unclear. Here, we investigated the effect of volitional muscle contraction during PAS on: (1) measures of general corticomotor excitability and intracortical circuit excitability; and (2) motor performance and learning. We assessed measures of corticomotor excitability using TMS and motor skill performance during a serial reaction time task (SRTT) at baseline and at 0, 30, 60 min post-PAS. Participants completed a SRTT retention test 1 week following the first two PAS sessions. Following the PAS intervention where the hand muscle maintained an active muscle contraction (PASACTIVE), there was lower short interval intracortical inhibition compared to PAS during a resting motor state (PASREST) and a sham PAS condition (PASCONTROL). SRTT performance improved within the session regardless of PAS condition. SRTT retention was greater following both PASACTIVE and PASREST after 1 week compared to PASCONTROL. These findings suggest that PAS may enhance motor learning retention and that motor state may be used to target different neural mechanisms of intracortical excitation and inhibition during PAS. This observation may be important to consider for the use of therapeutic noninvasive brain stimulation in neurologic patient populations.

Highlights

Triggered by a variety of internal and external environmental stimuli, neural networks have a remarkable ability to modify their structure and function to learn new behaviors (Kandel, 2001; Cooper, 2005)
The primary findings of this study reveal that the state of the motor system during a facilitatory paired associative stimulation (PAS) protocol may influence intracortical excitability
We did not observe this effect on short interval intracortical inhibition (SICI) following PASCONTROL or PAS during a resting motor state (PASREST),which is consistent with results reported by others following a facilitatory PAS protocol with the muscle at rest (Stefan et al, 2002; Sale et al, 2007; Elahi et al, 2012)

Summary

Introduction

Triggered by a variety of internal and external environmental stimuli, neural networks have a remarkable ability to modify their structure and function to learn new behaviors (Kandel, 2001; Cooper, 2005). Various types of noninvasive brain stimulation to induce positive neural plasticity in the injured brain and as a primer for rehabilitation have been studied (Player et al, 2012; Carson and Kennedy, 2013). The direction and magnitude of the induced neurophysiologic effects of PAS are: largely dependent on the interstimulus interval (Wolters et al, 2003); highly variable between individuals (Müller-Dahlhaus et al, 2008; López-Alonso et al, 2014); observed beyond the period of stimulation (Stefan et al, 2002; Player et al, 2012); and affected by the state of the motor system (rest vs muscular contraction) within and homologous to the targeted limb (Kujirai et al, 2006; Kennedy and Carson, 2008; Koch et al, 2013)

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