Voluntary activation of ankle muscles is accompanied by subcortical facilitation of their antagonists

Abstract

Flexion and extension movements are organized reciprocally, so that extensor motoneurones in the spinal cord are inhibited when flexor muscles are active and vice versa. During and just prior to dorsiflexion of the ankle, soleus motoneurones are thus inhibited as evidenced by a depression of the soleus H-reflex. It is therefore surprising that soleus motor evoked potentials (MEPs) elicited by transcranial magnetic stimulation (TMS) have been found not to be reduced and even facilitated during a voluntary dorsiflexion. The objective of this study was to investigate if MEPs, evoked by TMS, show a similar facilitation prior to and at the onset of contraction of muscles that are antagonists to the muscle in which the MEP is evoked and if so, examine the origin of such a facilitatory motor programme. Eleven seated subjects reacted to an auditory cue by contracting either the tibialis anterior (TA) or soleus muscle of the left ankle. TMS was applied to the hotspot of TA and soleus muscles on separate days. Stimuli were delivered prior to and at the beginning of contraction. Soleus MEPs were significantly facilitated when TMS was applied 50 ms prior to onset of plantar flexion. Surprisingly, soleus MEPs were also facilitated (although to a lesser extent) at a similar time in relation to the onset of dorsiflexion. TA MEPs were facilitated 50 ms prior to onset of dorsiflexion and neither depressed nor facilitated prior to plantar flexion. No difference was found between the facilitation of the soleus MEP and motor evoked responses to cervicomedullary stimulation prior to dorsiflexion, suggesting that the increased soleus MEPs were not caused by changes at a cortical level. This was confirmed by the observation that short-latency facilitation of the soleus H-reflex by subthreshold TMS was increased prior to plantar flexion, but not prior to dorsiflexion. These findings suggest that voluntary contraction at the ankle is accompanied by preceding facilitation of antagonists by a subcortical motor programme. This may help to ensure that the direction of movement may be changed quickly and efficiently during functional motor tasks.

Figure 1. Overview of experimental design

TMS was applied to the hotspot of TA or soleus at different time points prior to and at the onset of contraction. Single stimuli were delivered randomly prior to the first (C_warning) and second (C_go) auditory cue and at 25 ms intervals between 0 and 150 ms after C_go (Fig. 1). Control trials were also included in which the auditory cues were presented, but TMS was not applied.

Figure 2. Modulation of soleus H-reflexes and MEPs prior to plantar- and dorsiflexion

The amplitude of soleus MEPs was increased prior to both dorsiflexion and plantar flexion whereas the amplitude of the soleus H-reflex was only increased prior to plantar flexion. Prior to dorsiflexion, the soleus H-reflex was strongly depressed as has been shown by Crone & Nielsen (1989). Data from one subject.

Figure 3. Modulation of MEPs prior to dorsiflexion and plantar flexion

A, average soleus MEP size at rest, < C_warning, <C_go and at 25 ms intervals leading up to plantar flexion (▵) and dorsiflexion (•) as a percentage of MEP size at <C_go (n= 11). The black and red insets are average responses to TMS measured in soleus in one subject at <C_go (1.9% of M_max) and at 25 ms prior to dorsiflexion (4.3% of M_max), respectively. B, size of soleus MEP at 25 ms prior to dorsiflexion and plantar flexion for each subject as a percentage of MEP size at <C_go. C, like in A, but here TA MEP data are plotted. The black and red insets are average responses to TMS measured in TA in one subject in a soleus experiment at <C_go (17.8% of M_max) and at 25 ms prior to dorsiflexion (34.3% of M_max), respectively. Note the different shape of TA responses compared to the soleus responses in A. These responses were evoked by the same stimulus in the same session. D, size of TA MEP at 25 ms prior to dorsiflexion and plantar flexion for each subject as a percentage of MEP size at <C_go.

Figure 4. Modulation of MEPs and CMEPs

In three subjects, the responses to TMS and brainstem stimulation were measured at go and 25 ms prior to dorsiflexion (see Fig. 1). The average responses to TMS (left inset) and brainstem stimulation (right inset) at <C_go (black) and 25 ms prior to dorsiflexion (red) are illustrated from a single subject. The graphs below show the size of the MEP (left) and CMEP (right) responses as a percentage of M_max at <C_go and 25 ms prior to dorsiflexion. Each symbol represents one subject. Vertical lines represent s.e.m.

Figure 5. Time course of TMS conditioning of the H-reflex

A, an H-reflex was evoked at time ‘0 ms’ by stimulation of the posterior tibial nerve. A conditioning TMS pulse was applied at different times before and after the H-reflex stimulation and the size of the conditioned H-reflex response was then calculated for each conditioning–test interval. B, example of the time course of conditioned H-reflex response as a percentage of the control H-reflex response that was obtained in each subject at rest and during tonic plantar flexion and dorsiflexion. In this subject, the earliest facilitation during tonic planter flexion is observed at a conditioning–test interval of −4 ms. During tonic dorsiflexion, inhibition is seen at −2 ms. These intervals were then used for the following experiments.

Figure 6. Modulation of short-latency facilitation, short-latency inhibition and long-latency facilitation prior to contraction

The soleus H-reflex was conditioned by subthreshold TMS at go and 25 ms prior to dynamic plantar flexion (PF −25 ms) and dorsiflexion (DF −25 ms) contraction to 30% MVC. The size of the conditioned reflex is presented as a percentage of the control reflex size. A, for each subject, the conditioning–test interval eliciting the earliest facilitation in the time course (Fig. 4) was used for measuring short-latency facilitation. B, for short-latency inhibition, the earliest conditioning–test interval giving inhibition during tonic dorsiflexion was used. C, a conditioning–test interval of 10 ms was used to measure long-latency facilitation in all subjects.