Interlimb communication to the knee flexors during walking in humans

Abstract

A strong coordination between the two legs is important for maintaining a symmetric gait pattern and adapting to changes in the external environment. In humans as well as animals, receptors arising from the quadriceps muscle group influence the activation of ipsilateral muscles. Moreover, strong contralateral spinal connections arising from quadriceps and hamstring afferents have been shown in animal models. Therefore, the aims of the present study were to assess if such connections also exist in humans and to elucidate on the possible pathways. Contralateral reflex responses were investigated in the right leg following unexpected unilateral knee joint rotations during locomotion in either the flexion or extension direction. Strong reflex responses in the contralateral biceps femoris (cBF) muscle with a mean onset latency of 76 ± 6 ms were evoked only from ipsilateral knee extension joint rotations in the late stance phase. To investigate the contribution of a transcortical pathway to this response, transcranial magnetic and electrical stimulation were applied. Motor evoked potentials elicited by transcranial magnetic stimulation, but not transcranial electrical stimulation, were facilitated when elicited at the time of the cBF response to a greater extent than the algebraic sum of the cBF reflex and motor evoked potentials elicited separately, indicating that a transcortical pathway probably contributes to this interlimb reflex. The cBF reflex response may therefore be integrated with other sensory input, allowing for responses that are more flexible. We hypothesize that the cBF reflex response may be a preparation of the contralateral leg for early load bearing, slowing the forward progression of the body to maintain dynamic equilibrium during walking.

Figure 1. Facilitation of contralateral biceps femoris (cBF) following ipsilateral knee extension joint rotations

Mean data from one participant for either control steps (black line) or following ipsilateral knee extension joint rotations (grey line) during the late stance phase (50%) of the gait cycle (0–100%). (A) Ipsilateral knee angle; (B) mean rectified ipsilateral biceps femoris electromyography (EMG); (C) contralateral knee angle; and (D) mean rectified cBF EMG. Perturbation onset is represented by the vertical dashed line. Ipsilateral and contralateral stance phases are represented by the black bars below D. Note the period of facilitation in the cBF EMG following perturbation trials, beginning about 75 ms after perturbation onset.

Figure 2. Evidence of extra-facilitation of magnetically induced MEPs in the cBF following ipsilateral knee extension joint rotations

A, mean rectified cBF EMG for one participant following either control steps, perturbation only trials, TMS only trials, or perturbation and TMS trials. MEPs evoked by TMS were timed to coincide with the onset of the cBF reflex response. Vertical dashed lines represent perturbation onset, TMS onset and MEP/cBF reflex onset, respectively. B, group mean cBF EMG data for the 20 ms following MEP/cBF reflex onset for the four conditions for nine participants. All data were normalized to the algebraic sum of the perturbation only and TMS only conditions (horizontal dashed line in B). The asterisk denotes a significant difference of the perturbation and TMS condition compared with the algebraic sum of the perturbation only and TMS only conditions. Error bars in (B) represent SEM. cBF, contralateral biceps femoris; iEMG, integrated electromyography; MEP, motor evoked potential; pert., perturbation; TMS, transcranial magnetic stimulation.

Figure 3. Time course of extra-facilitation of magnetically induced MEPs in the cBF (A) and iBF (B) following ipsilateral knee extension joint rotations

MEPs were evoked by TMS at different timings (−30, −15, 0, +15, +30 and +250 ms) relative to the cBF reflex response onset (time 0, filled circle). A, size of the conditioned MEPs (perturbation and TMS condition) expressed as a percentage of the algebraic sum of perturbation only and TMS only conditions for each time interval in the cBF. B, size of the conditioned MEPs (perturbation and TMS condition) expressed as a percentage of the algebraic sum of perturbation only and TMS only conditions for each time interval in the iBF. The horizontal dashed lines represent 100%. Error bars represent SEM The asterisks indicate that the combined perturbation and TMS condition resulted in MEPs significantly greater (P < 0.05) than the sum of the cBF reflex response and the control MEP in the cBF only. Note that there was only a significant increase in the cBF MEPs when the MEPs were times to arrive at or immediately after the onset of the cBF response, and that there was no such increase in the MEPs evoked in the iBF at these timings. cBF, contralateral biceps femoris; iBF, ipsilateral biceps femoris; MEP, motor evoked potential; TMS, transcranial magnetic stimulation.

Figure 4. Comparison of TMS or TES induced MEPs in the cBF following ipsilateral knee extension joint rotations

Mean cBF iEMG data for the 20 ms following MEP/cBF reflex onset in three participants following either: control steps, perturbation only trials, stimulation (TMS or TES) only trials, or combined perturbation and stimulation (TMS or TES) trials. MEPs evoked by either TMS or TES were timed to coincide with the onset of the cBF reflex response. All data were normalized to the algebraic sum of the perturbation only and the stimulation (TMS or TES) only conditions (horizontal dashed line). Note that there is a clear facilitation above the algebraic sum of the perturbation only and the stimulation only conditions when M1 was magnetically stimulated, but not electrically stimulated, when either stimulation was combined with ipsilateral knee extension joint rotations (perturbation and stimulation trials). Error bars represent SEM cBF, contralateral biceps femoris; EMG, electromyography; MEP, motor evoked potential; pert., perturbation; stim., stimulation; TES, transcranial electrical stimulation; TMS, transcranial magnetic stimulation.