Non-paretic leg movements can facilitate cortical drive to the paretic leg in individuals post stroke with severe motor impairment: Implications for motor priming

Abstract

Cross-education, a phenomenon where unilateral strength (or skill) training enhances strength (or skill) in the contralateral untrained limb, has been well studied in able-bodied individuals. Cross-education effect accompanies bilateral changes of corticomotor activity in the motor cortex (M1). Recent reports demonstrated greater cross-education effect in stroke survivors compared to healthy individuals, however, corticomotor responses to cross-education in stroke remains unclear. This study aimed to determine the effects of non-paretic leg movements on corticomotor excitability (CME) and reaction time of the paretic leg in severely impaired stroke survivors. Seventeen post stroke individuals with severe leg motor impairment (Fugl-Meyer lower extremity score less than 21 and absence of motor evoked potential in the paretic leg) performed three 20-min motor trainings using their non-paretic ankle: skill (targeted dynamic movements), strength (isometric resistance) and sham (sub-threshold electrical nerve stimulation). During training, verbal instructions were given to the participants to limit their movement to the non-paretic leg and this was confirmed with visual observation of the paretic leg. Transcranial magnetic stimulation measured CME of the contralateral pathways from the non-lesioned M1 to the non-paretic tibialis anterior (TA) muscle, ipsilateral pathways to the paretic TA and transcallosal inhibition (TCI) from the non-lesioned to lesioned M1. Paretic ankle reaction time was measured using a reaction time paradigm. All outcomes were measured before, immediately post, 30-min post and 60-min post priming. CME of the non-paretic TA increased after skill (.08 ± .10 mV) and strength (.06 ± .05 mV) training (p < .01). Ipsilateral CME of the paretic TA (.02 ± .01 mV) and TCI (.01 ± .01 s, ipsilateral silent period; more inhibition to the lesioned M1) increased after skill (p < .05) but not strength training. Reaction time of the paretic ankle improved after skill and strength training (-.11 ± .2 and -.13 ± .20 s, respectively; p < .05) and was sustained at 60 min. No changes were observed during the sham condition. Our findings may inform future studies for using non-paretic leg movements as a priming modality, especially for those who are contraindicated to other priming paradigms (e.g., brain stimulation) or unable to perform paretic leg movements. Conclusion: Non-paretic leg movements can be used as a priming modality, especially for those who are contraindicated to other priming paradigms (e.g., brain stimulation) or unable to perform paretic leg movements.

Keywords: cortical priming; cross-education; reaction time; severe stroke; transcranial magnetic stimulation.

Figure 1.

Flow diagram of study participants

Figure 2.

Intervention setup This schematic represents experimental setup for (A) skill, (B) strength, and (C) sham motor tasks using the non-paretic limb. ROM, range of motion; MVC, maximum voluntary contraction; EMG, electromyography; TENS, transcutaneous electrical nerve stimulation.

Figure 3.

Transcranial magnetic stimulation setup and baseline neurophysiological data from one severely impaired stroke participant Representative example of transcranial magnetic stimulation setup and baseline outcomes for one stroke participant (paretic Fugl Meyer Lower Extremity score = 19) is illustrated. (A) and (B) depicts the overlay of motor-evoked potentials (MEPs) from the contralateral non-paretic tibialis anterior (TA) and ipsilateral paretic TA, respectively, stimulated at 130% active motor threshold determined for the non-paretic TA. The bold trace represents average of all 30 MEPs. (C) demonstrates transcallosal inhibition quantified as the duration of the ipsilateral silent period (between the two vertical dashed lines) where rectified EMG activity (red bolded line) is below 25% of the mean rectified background EMG (black horizontal solid line) for more than 5 ms respectively. Yellow arrow below each figure represents the stimulus onset. MVC, maximum voluntary contraction; EMG, electromyography; NPTA, non-paretic tibialis anterior; PTA, paretic tibialis anterior; TCI, transcallosal inhibition.

Figure 4.

Changes in transcranial magnetic stimulation and reaction time outcomes from PRE assessment Percent changes from PRE to POST, POST 30, and POST 60 for (A) corticomotor excitability (CME) of the non-paretic tibialis anterior (TA), (B) ipsilateral CME of the paretic TA, (C) transcallosal inhibition from the non-lesioned to lesioned hemisphere, and (D) reaction time of the paretic TA. Skill task is colored as blue, strength as orange, and sham as gray. Error bars indicate standard error of mean. NPTA, non-paretic tibialis anterior; PTA, paretic tibialis anterior; TCI, transcallosal inhibition. *Significantly different (p < 0.05).