V. Dietz

Gating and reversal of reflexes in ankle muscles during human walking

SummaryPhase-dependent reflex modulation was studied by recording the electromyographic (EMG) responses in ankle flexors (Tibialis Anterior, TA) and extensors (Gastrocnemius Medialis, GM and Soleus, SOL) to a 20 ms train of electrical pulses, applied to the tibial or sural nerve at the ankle, in human volunteers walking on a treadmill at 4 km/h. For low intensity stimuli (i.e. 1.6 times perception threshold), given during the swing phase, the most common response was a suppression of the TA activity with a latency of 67 to 118 ms. With high intensity of stimulation (i.e. 2.8 × T), a facilitatory response appeared in TA with a latency of 74 ms. This latter response was largest during the middle of the swing phase, when it was correlated with exaggerated ankle dorsiflexion. The TA reflex amplitude was not a simple function of the level of spontaneous ongoing activity. During stance, TA responses were small or absent and accompanied by a suppression of the GM activity with a latency ranging from 62 to 101 ms. A few subjects showed an early facilitatory, instead of a suppressive, GM response (88 to 136 ms latency). They showed a phase-dependent reflex reversal from a dominant TA response during swing to a facilitatory GM response with an equivalent latency during stance. The GM facilitation occurred exclusively during the early stance phase and habituated more than the TA responses. It is concluded that phase-dependent gating of reflexes occurs in ankle muscles of man, but only when vigorous extensor reflexes are present. More commonly, a phase-dependent modulation is seen, both of facilitatory and suppressive responses.

Regulation of bipedal stance: dependency on “load” receptors

SummaryAccording to recent observations, influence of body load has to be taken into account for the neuronal control of upright stance in addition to the systems known to be involved in this regulation (e.g. afferent input from vestibular canals, visual and muscle stretch receptors). The modulation of compensatory leg muscle electromyographic (EMG) responses observed during horizontal body posture indicates the existence of a receptor system which responds to loading of the body against the supporting platform. This receptor should be located within the extensor muscles because a compensatory EMG response and a loading effect on this response was only present following translational, but not rotational impulses. As the EMG responses were identical to those obtained during upright stance, it is argued that these load receptors activate postural reflexes. According to recent observations in the spinal cat, this afferent input probably arises from Golgi tendon organs and represents a newly discovered function of these receptors in the regulation of stance and gait.

Corrective reactions to stumbling in man: neuronal co-ordination of bilateral leg muscle activity during gait.

Electromyogram (e.m.g.) responses of lower leg muscles, and corresponding movements were studied following a perturbation of the limb during walking, produced by either (a) a randomly timed, short acceleration or decelerating impulse applied to the treadmill, or (b) a unilateral triceps surae contraction induced by tibial nerve stimulation. Bilateral e.m.g. responses following the perturbation were specific for the mode of perturbation and depended on the phase of the gait cycle in which the perturbation occurred. Treadmill deceleration evoked a bilateral tibialis anterior activation; acceleration evoked an ipsilateral gastrocnemius and contralateral tibialis anterior activation (latency in either condition and on both sides was 65‐75 ms, duration about 150 ms). Tibial nerve stimulation at the beginning of a stance phase, was followed by an ipsilateral tibialis anterior activation; during the swing phase it was followed by an ipsilateral tibialis anterior and contralateral gastrocnemius activation (latency about 90 ms, duration about 100 ms). These patterns differed from the response seen after a unilateral displacement during static standing, which evoked a bilateral tibialis anterior activation. These early responses were in most cases followed by late ipsilateral responses, but the e.m.g. pattern of the next step cycle was usually unchanged, or affected only at its onset. The e.m.g. responses were unaltered by ischaemic nerve blockade of group I afferents, by training effects or by pre‐warning of the onset of perturbation (randomly or self‐induced). Despite the different e.m.g. responses following a perturbation during gait, the same basic functional mechanism was obviously at work: the early ipsilateral response achieved a repositioning of the displaced foot and leg, while the early contralateral and late ipsilateral responses provided compensation for body displacement. It is suggested that the e.m.g. responses may be mediated predominantly by peripheral information from group II and group III afferents, which modulate the basic motor pattern of spinal interneuronal circuits underlying the respective motor task.

Afferent control of human stance and gait: evidence for blocking of group I afferents during gait

SummaryThe cerebral potentials (c.p.) evoked by electrical stimulation of the tibial nerve during stance and in the various phases of gait of normal subjects were compared with the c.p. and leg muscle e.m.g. responses evoked by perturbations of stance and gait. Over the whole step cycle of gait the c.p. evoked by an electrical stimulus were of smaller amplitude (3 μV and 9 μV, respectively) than that seen in the stance condition, and appeared with a longer latency (mean times to first positive peak: 63 and 43 ms, respectively). When the electrical stimulus was applied during stance after ischaemic blockade of group I afferents, the c.p. were similar to those evoked during gait. The c.p. evoked by perturbations were larger in amplitude than those produced by the electrical stimulus, but similar in latencies in both gait and stance (mean 26 μV and 40 μV; 65 ms and 42 ms, respectively) and configurations. The large gastrocnemius e.m.g. responses evoked by the stance and gait perturbations arose with a latency of 65 to 70 ms. Only in the stance condition was a smaller, shorter latency (40 ms) response seen. It is concluded that during gait the signals of group I afferents are blocked at both segmental and supraspinal levels which was tested by tibial nerve stimulation. It is suggested that the e.m.g. responses induced in the leg by gait perturbations are evoked by group II afferents and mediated via a spinal pathway. The c.p. evoked during gait most probably reflect the processing of this group II input by supraspinal motor centres for the coordination of widespread arm and trunk muscle activation, necessary to restablish body equilibrium.

Modulation, probably presynaptic in origin, of monosynaptic Ia excitation during human gait

Modulation of presynaptic inhibition of Ia afferents projecting monosynaptically to soleus motoneurones was investigated during human gait. Changes in presynaptic inhibition of Ia afferents were deduced from alterations in the amount of heteronymous soleus H-reflex facilitation evoked by a constant femoral nerve stimulation. It has been shown that this facilitation is mediated through a monosynaptic Ia pathway and that during its first 0.5 ms it is still uncontaminated by any polysynaptic effect and can be used to assess ongoing presynaptic inhibition of Ia terminals to soleus motoneurones. During gait, heteronymous facilitation was reduced with respect to its control value (rest during sitting) and modulated during the step cycle: it reached its maximum at mid-stance and decreased to near zero by the end of stance. At the same time the H-reflex amplitude was to some extent similarly modulated. It is argued that this decrease in heteronymous Ia facilitation and in H-reflex amplitude reflects an increased, ongoing presynaptic inhibition of Ia terminals projecting onto soleus motoneurones, which could be from central and/or peripheral origin. D1 inhibition, i.e. the late and long-lasting inhibition of the soleus H-reflex evoked by a train of stimuli to the common peroneal nerve, was used as another method to assess presynaptic inhibition. This D1 inhibition was decreased during gait, and it is argued that this decrease might reflect an occlusion in presynaptic pathways or increased presynaptic inhibition of pathways mediating the conditioning volley.

Stumbling reactions in man: significance of proprioceptive and pre‐programmed mechanisms.

1. Electromyogram (e.m.g.) responses of the leg musculature and the corresponding joint movements were studied following a perturbation of the limb during walking on a treadmill, produced by a randomly timed treadmill acceleration impulse, either predictable, or unpredictable in its amplitude and rate of acceleration. 2. The rate of rise of ipsilateral gastrocnemius e.m.g. response following a perturbation was dependent on the rate of treadmill acceleration. For a given acceleration rate the amplitude of the e.m.g. response and the timing of its peak was dependent on the amplitude of the impulse and the rate of rise of the gastrocnemius response was the same for impulses of both small and large amplitude. The onset latency was shorter (65 ms) for high accelerations and longer (85 ms) for lower ones. 3. The amplitude of the ipsilateral biceps femoris response was much smaller than the gastrocnemius response but was larger following unpredictable than predictable impulses. 4. The initial gastrocnemius response was followed by a tibialis anterior activation associated with a gastrocnemius depression and sometimes with a second, weak gastrocnemius activation. The gastrocnemius depression ended within a fixed time range relative to the onset of the response. The tibialis anterior activation was most pronounced when unpredictable impulses with high acceleration but a small amplitude were induced. 5. It is concluded that generation of the first gastrocnemius response is obviously under continuous control by muscle proprioceptive information and can be best described in terms of a stretch reflex response. It is suggested that, on the evidence of the diphasic or triphasic e.m.g. pattern, a close interaction occurs between a central programme and muscle proprioceptive input in order to generate the appropriate e.m.g. pattern. 6. On the basis of earlier work (Berger, Dietz & Quintern, 1984a) and on the present results it is suggested that the e.m.g. responses may be mediated mainly by muscle proprioceptive input from group II afferents. This input is modulated and processed by spinal interneuronal circuits, closely connected with spinal locomotor centres. The mode of processing depends on various factors, such as the predictability of the nature of the impulse.

Motor unit involvement in spastic paresis ☆: Relationship between leg muscle activation and histochemistry

In 4 patients with spastic hemiparesis the electromyograms (EMG) of leg muscles were recorded during walking and the gastrocnemius medialis on both sides was investigated by histochemistry and morphometry. During walking a reciprocal mode of muscle activation was preserved on the spastic side, but the EMG amplitude was reduced. In one patient the discharge behaviour of single motor units was investigated during stance. The mean discharge rate on both the spastic and the unaffected side amounted to about 5.5 Hz. Modification of this rate over a wider range by manoeuvres of the trunk was only observed on the unaffected side. Histochemistry and morphometry of the spastic muscle revealed: Increased levels of muscle fibre atrophy (especially type II); A predominance of type I fibres during later stages, when spasticity was established; Structural changes, such as the appearance of target fibres, mainly in type I fibres. These results suggest that the low level of tonic activation in spastic muscle develops tension enough during the stance phase of gait to support the body. The histopathological profile of the spastic gastrocnemius muscle is considered to be indicative of denervation, due to the combined effects of an impaired supraspinal control of the lower motoneurone and a concurrent transsynaptic muscle membrane dysfunction, muscle cell atrophy and fibre type transformation.

Characteristics of postural instability induced by ischemic blocking of leg afferents

SummaryAfter minimizing proprioceptive input from the legs by ischemia without degradation of muscle force and excluding visual stabilization by eye closure, a characteristic anterior-posterior postural sway around 1 Hz was observed in three normal subjects. This is similar to the instability seen in two tabes dorsalis patients. From the spectral analysis of head and hip movements, displacements of the center of force and of ankle angle as well as from EMG recordings of the anterior tibial and gastrocnemius muscle it is concluded that the oscillations around 1 Hz are due to the long latency and high threshold of vestibularly induced leg muscle discharges (200–300 ms) arriving in the counterbalancing phase of the trunk, which causes an overshoot in body sway.

Selective activation of human soleus or gastrocnemius in reflex responses during walking and running

SummaryPhase-dependent reflex modulation was studied by recording the electromyographic (EMG) responses in soleus (SOL) and gastrocnemius medialis (GM) to a 20 ms train of 5 electrical pulses, applied to the sural or tibial nerve at the ankle, in 14 volunteers walking or running on a treadmill. Although both the spontaneous activity and the reflex responses were usually similar for both muscles, instances were identified in which separate control was evident. During walking (4 km/h), activity in SOL started earlier in the stance phase than GM activity. Correspondingly, the amplitude of the reflex responses was larger in SOL than in GM in early stance, both ipsi- and contralateral to the side of stimulation. In some cases, the same stimulus could elicit contralaterally a suppression of GM in synchrony with a facilitation of SOL. These crossed extensor reflexes had a low threshold (1.2 × T) and a latency ranging from 72 to 105 ms. During running (8 km/h or more), responses were seen selectively in GM instead, without concomitant responses in SOL. Such responses had a latency ranging from 82 to 158 ms and they appeared during the first extension phase, at the end of the swing phase. In addition, selective GM responses, with latencies above 200 ms, were seen near the transition from stance to swing during running. These instances of separate reflex control of SOL and GM were correlated with step cycle periods during which the motoneurones of either one of these muscles received more spontaneous activation than the other. Nevertheless, it is argued that premotoneuronal gating must also be involved since the increased amplitude of the crossed SOL responses (in early stance) and of GM responses (at end swing) was not strictly linked to an elevated amount of spontaneous activity during these parts of the step cycle as compared to other parts.

Human neuronal interlimb coordination during split-belt locomotion

Human interlimb coordination and the adaptations in leg muscle activity were studied during walking on a treadmill with split belts. Four different belt speeds (0.5, 1.0, 1.5, 2.0 m/s) were offered in all possible combinations for the left and right leg. Subjects adapted automatically to a difference in belt speed within 10–20 stride cycles.This adaptation was achieved by a reorganization of the stride cycle with a relative shortening of the duration of the support and lengthening of the swing phase of the “fast” leg and, vice versa, in support and swing duration on the “slow” leg. The electromyogram EMG patterns were characterized by two basic observations: (1) onset and timing of EMG activity were influenced by biomechanical constraints. A shortening of the support phase on the faster side was related to an earlier onset and increase in gastrocnemius activity, while a coactivation pattern in the antagonistic leg muscles was predominant during a prolonged support phase on the slower side. (2) A differential modulation of the antagonistic leg muscles took place. An increase in ipsilateral belt speed in combination with a constant contralateral belt speed was associated with an almost linear increase in ipsilateral gastrocnemius and contralateral tibialis anterior EMG activity, while the contralateral gastrocnemius and ipsilateral tibialis anterior EMG activity were little affected. It is concluded that a modifiable timing within the stride cycle takes place with a coupling between ipsilateral support and contralateral swing phase. The neuronal control of this coupling is obviously based on ipsilateral modulation of leg extensor EMG by proprioceptive feedback and an appropriate central (e.g. spinal) modulation of contralateral tibialis anterior EMG activity.