Lars O. D. Christensen

Major role for sensory feedback in soleus EMG activity in the stance phase of walking in man

1 Sensory feedback plays a major role in the regulation of the spinal neural locomotor circuitry in cats. The present study investigated whether sensory feedback also plays an important role during walking in 20 healthy human subjects, by arresting or unloading the ankle extensors 6 deg for 210 ms in the stance phase of gait. 2 During the stance phase of walking, unloading of the ankle extensors significantly (P < 0·05) reduced the soleus activity by 50 % in early and mid‐stance at an average onset latency of 64 ms. 3 The onset and amplitude of the decrease in soleus activity produced by the unloading were unchanged when the common peroneal nerve, which innervates the ankle dorsiflexors, was reversibly blocked by local injection of lidocaine (n= 3). This demonstrated that the effect could not be caused by a peripherally mediated reciprocal inhibition from afferents in the antagonist nerves. 4 The onset and amplitude of the decrease in soleus activity produced by the unloading were also unchanged when ischaemia was induced in the leg by inflating a cuff placed around the thigh. At the same time, the group Ia‐mediated short latency stretch reflex was completely abolished. This demonstrated that group Ia afferents were probably not responsible for the decrease of soleus activity produced by the unloading. 5 The findings demonstrate that afferent feedback from ankle extensors is of significant importance for the activation of these muscles in the stance phase of human walking. Group II and/or group Ib afferents are suggested to constitute an important part of this sensory feedback.

Evidence that a transcortical pathway contributes to stretch reflexes in the tibialis anterior muscle in man

1 In human subjects, stretch applied to ankle dorsiflexors elicited three bursts of reflex activity in the tibialis anterior (TA) muscle (labelled M1, M2 and M3) at mean onset latencies of 44, 69 and 95 ms, respectively. The possibility that the later of these reflex bursts is mediated by a transcortical pathway was investigated. 2 The stretch evoked a cerebral potential recorded from the somatosensory cortex at a mean onset latency of 47 ms in nine subjects. In the same subjects a compound motor‐evoked potential (MEP) in the TA muscle, evoked by magnetic stimulation of the motor cortex, had a mean onset latency of 32 ms. The M1 and the M2 reflexes thus had too short a latency to be caused by a transcortical pathway (minimum latency, 79 ms (47 + 32)), whereas the later part of the M2 and all of the M3 reflex had a sufficiently long latency. 3 When the transcranial magnetic stimulation was timed so that the MEP arrived in the TA muscle at the same time as the M1 or M2 reflexes, no extra increase in the potential was observed. However, when the MEP arrived at the same time as the M3 reflex a significant (P < 0.01) extra‐facilitation was observed in all twelve subjects investigated. 4 Peaks evoked by transcranial magnetic stimulation in the post‐stimulus time histogram of the discharge probability of single TA motor units (n= 28) were strongly facilitated when they occurred at the same time as the M3 response. This was not the case for the first peaks evoked by electrical transcranial stimulation in any of nine units investigated. 5 We suggest that these findings are explained by an increased cortical excitability following TA stretch and that this supports the hypothesis that the M3 response in the TA muscle is ‐ at least partly ‐ mediated by a transcortical reflex.

Cerebral activation during bicycle movements in man

Abstract. The cerebral activation during bicycle movements was investigated by oxygen-15-labelled H2O positron emission tomography (PET) in seven healthy human subjects. Compared to rest active bicycling significantly activated sites bilaterally in the primary sensory cortex, primary motor cortex (M1) and supplementary motor cortex (SMA) as well as the anterior part of cerebellum. Comparing passive bicycling movements with rest, an almost equal activation was observed. Subtracting passive from active bicycle movements, significant activation was only observed in the leg area of the primary motor cortex and the precuneus, but not in the primary sensory cortex (S1). The M1 activation was positively correlated (α=0.75–0.85, t=6.4, P<10–5) with the rate of the active bicycle movements. Imagination of bicycle movements compared to rest activated bilaterally sites in the SMA. It is suggested that the higher motor centres, including the primary and supplementary motor cortices as well as the cerebellum, take an active part in the generation and control of rhythmic motor tasks such as bicycling.

Transcranial magnetic stimulation and stretch reflexes in the tibialis anterior muscle during human walking

1 Stretch of the ankle dorsiflexors was applied at different times of the walking cycle in 17 human subjects. When the stretch was applied in the swing phase, only small and variable reflex responses were observed in the active tibialis anterior (TA) muscle. Two of the reflex responses that could be distinguished had latencies which were comparable with the early (M1) and late (M3)components of the three reflex responses (M1, M2 and M3) observed during tonic dorsiflexion in sitting subjects. In the stance phase a single very large response was consistently observed in the inactive TA muscle. The peak of this response had the same latency as the peak of M3, but in the majority of subjects the onset latency was shorter than that of M3. 2 The TA reflex response in the stance phase was abolished by ischaemia of the lower leg at the same time as the soleus H‐reflex, suggesting that large muscle afferents were involved in the generation of the response. 3 Motor‐evoked potentials (MEPs) elicited in the TA by transcranial magnetic stimulation (TMS) were strongly facilitated corresponding to the peak of the stretch response in the stance phase and the late reflex response in the swing phase. A similar facilitation was not observed corresponding to the earlier responses in the swing phase and the initial part of the response in stance. 4 Prior stretch did not facilitate MEPs evoked by transcranial electrical stimulation in the swing phase of walking. However, in the stance phase MEPs elicited by strong electrical stimulation were facilitated by prior stretch to the same extent as the MEPs evoked by TMS. 5 The large responses to stretch seen in the stance phase are consistent with the idea that stretch reflexes are mainly involved in securing the stability of the supporting leg during walking. It is suggested that a transcortical reflex pathway may be partly involved in the generation of the TA stretch responses during walking.

The effect of transcranial magnetic stimulation on the soleus H reflex during human walking

1 The effect of transcranial magnetic stimulation (TMS) on the soleus H reflex was investigated in the stance phase of walking in seventeen human subjects. For comparison, measurements were also made during quiet standing, matched tonic plantar flexion and matched dynamic plantar flexion. 2 During walking and dynamic plantar flexion subliminal (0.95 times threshold for a motor response in the soleus muscle) TMS evoked a large short‐latency facilitation (onset at conditioning‐test interval: −5 to −1 ms) of the H reflex followed by a later (onset at conditioning‐test interval: 3–16 ms) long‐lasting inhibition. In contrast, during standing and tonic plantar flexion the short‐latency facilitation was either absent or small and the late inhibition was replaced by a long‐lasting facilitation. 3 When grading the intensity of TMS it was found that the short‐latency facilitation had a lower threshold during walking than during standing and tonic plantar flexion. Regardless of the stimulus intensity the late facilitation was never seen during walking and dynamic plantar flexion and the late inhibition was not seen, except for one subject, during standing and tonic plantar flexion. 4 A similar difference in the threshold of the short‐latency facilitation between walking and standing was not observed when the magnetic stimulation was replaced by transcranial electrical stimulation. 5 The lower threshold of the short‐latency facilitation evoked by magnetic but not electrical transcranial stimulation during walking compared with standing suggests that cortical cells with direct motoneuronal connections increase their excitability in relation to human walking. The significance of the differences in the late facilitatory and inhibitory effects during the different tasks is unclear.

Evidence for transcortical reflex pathways in the lower limb of man.

The existence of transcortical reflex pathways in the control of distal arm and hand muscles in man is now widely accepted. Much more controversy exists regarding a possible contribution of such reflexes to the control of leg muscles. It is often assumed that transcortical reflex pathways play no, or only a minor, role in the control of leg muscles. Transcortical reflex pathways according to this view are reserved for the control of the distal upper limb and are seen in close relation to the evolution of the primate hand. Here we review data, which provide evidence that transcortical reflexes do exist for lower limb muscles and may play a significant role in the control of at least some of these muscles. This evidence is based on animal research, recent experiments combining transcranial magnetic stimulation with peripheral electrical and mechanical stimulation in healthy subjects and neurological patients. We propose that afferent activity from muscle and skin may play a role in the regulation of bipedal gait through transcortical pathways.

Evidence suggesting that a transcortical reflex pathway contributes to cutaneous reflexes in the tibialis anterior muscle during walking in man

Abstract Stimulation of cutaneous foot afferents has been shown to evoke a facilitation of the tibialis anterior (TA) EMG-activity at a latency of 70–95 ms in the early and middle swing phase of human walking. The present study investigated the underlying mechanism for this facilitation. In those subjects in whom it was possible to elicit a reflex during tonic dorsiflexion while seated (6 out of 17 tested), the facilitation in the TA EMG evoked by stimulation of the sural nerve (3 shocks, 3-ms interval, 2.0–2.5× perception threshold) was found to have the same latency in the swing phase of walking. The facilitation observed during tonic dorsiflexion has been suggested to be – at least partly – mediated by a transcortical pathway. To investigate whether a similar mechanism contributes to the facilitation observed during walking, magnetic stimulation of the motor cortex (1.2× motor threshold) was applied in the early swing phase at different intervals in relation to the cutaneous stimulation in 17 subjects. In 13 of the subjects, the motor potentials evoked by the magnetic stimulation (MEPs) were more facilitated by prior sural-nerve stimulation (conditioning-test intervals of 50–80 ms) than the algebraic sum of the control MEP and the cutaneous facilitation in the EMG when evoked separately. In four of these subjects, a tibialis anterior H-reflex could also be evoked during walking. In none of the subjects was an increase of the H-reflex similar to that for the MEP observed. In five experiments on four subjects, MEPs evoked by magnetic and electrical cortical stimulation were compared. In four of these experiments, only the magnetically induced MEPs were facilitated by prior stimulation of the sural nerve. We suggest that a transcortical pathway may also contribute to late cutaneous reflexes during walking.

Recruitment of extensor-carpi-radialis motor units by transcranial magnetic stimulation and radial-nerve stimulation in human subjects

Abstract The responses of 34 extensor-carpi-radialis motor units to graded transcranial magnetic stimulation (TMS) and electrical stimulation of the radial nerve were investigated in six human subjects. Simultaneously with the recording of the single motor-unit discharges, motor-evoked potentials (MEPs) and H-reflexes evoked by the two types of stimulation were recorded by surface electrodes and expressed as a percentage of the maximal motor response (Mmax). Ten motor units were activated in the H-reflex when it was less than 5% of Mmax, but not in the MEP even when it was 15% of Mmax. The opposite was observed for three motor units. Eleven motor units were recruited by both stimuli, but with significantly different recruitment thresholds. Only ten motor units had a threshold similar to TMS and radial nerve stimulation. From these observations, we suggest that caution should be taken when making conclusions regarding motor cortical excitability based on changes in the size of MEPs, even when it is ensured that there are no similar changes in background EMG-activity or H-reflexes.

Cerebral functional anatomy of voluntary contractions of ankle muscles in man

1 Cerebral activation elicited by right‐sided voluntary ankle muscle contraction was investigated by positron emission tomography measurements of regional cerebral blood flow. Two studies with eight subjects in each were carried out. Tonic isometric plantar and dorsiflexion and co‐contraction of the antagonist muscles were investigated in study 1. Tonic contraction was compared with dynamic ramp‐and‐hold contractions in study 2. 2 All types of contraction elicited activation of the left primary motor cortex (M1). The distance between the M1 peak activation locations for tonic isometric dorsi‐ and plantar flexion was 17 mm. Co‐contraction elicited activation of a larger area of M1 mainly located inbetween but partially overlapping the M1 areas activated during isolated dorsi‐/plantar flexion. 3 A voxel‐by‐voxel correlation analysis corrected for subject covariance showed for dorsiflexion a significant correlation between tibialis anterior EMG level and cerebral blood flow activation in the cerebellum and the M1 of the medial frontal cortex. For plantar flexion a significant correlation was found between soleus EMG and cerebral activation in the left medial S1 and M1, left thalamus and right cerebellum. 4 The activation during dynamic isotonic and isometric dorsi‐ and plantar flexion was significantly more extensive than during tonic contractions. In addition to M1, activation was seen in the contralateral supplementary motor area and bilaterally in the premotor and parietal cortices. Isotonic and isometric contractions did not differ except in a small area in the primary somatosensory cortex. 5 One possible explanation of the different cerebral activation during co‐contraction compared to that during plantar/dorsiflexion is that slightly different populations of cortical neurones are involved. The more extensive activation during dynamic compared with tonic contractions may reflect a larger cortical drive necessary to initiate and accelerate movements.

Chapter 23 Synchronization of lower limb motor units in spastic patients

Publisher Summary Synergistic motor units usually show a short duration central peak in the cross-correlogram, indicating an increased probability of synchronous firing, which is caused partly by a common synaptic drive to the motoneurones from branches of last-order neurones. It has been suggested that the short duration peak and 18–35 Hz coherence depends on activity in the corticospinal tract. One argument is the finding that neurological patients with lesions of the central motor pathways show a decreased incidence of cross-correlogram short duration peaks and coherence in the 18–35 Hz band. Broad peaks are assumed not to be caused by a common input from branches of last-order neurones, but rather by synchronized discharges from populations of spinal neurones released from descending control by the effects of the lesion. To control the validity of the use of surface recordings, the same analysis on electromyography (EMG) needle recordings obtained using the same experimental protocol as for the surface recordings is performed. Researchers have investigated the association among multiunit spike occurrences in the surface EMGs recorded from two different locations on the same leg muscle. Because the use of a trigger level ensures that only the multiunit spikes with the largest amplitudes are included in the analysis, it is unlikely that cross-talk would contribute significantly. It is obvious that the cross-correlation and coherence analysis of the multiunit surface EMG is a useful method for investigation of functional inputs to the spinal motoneurones during different motor tasks.