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

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. Received: 24 September 1997 / Accepted: 2 June 1998     

Modulation of non-monosynaptic excitation from ankle dorsiflexor afferents to quadriceps motoneurones during human walking

Modulation of non-monosynaptic excitation from ankle dorsiflexors to quadriceps (Q) motoneurones during human treadmill walking was investigated in 25 healthy human subjects. Stimulation of the common peroneal nerve (CPN) evoked a biphasic facilitation in the rectified and averaged ( n = 50) Q electromyographic (EMG) activity between 0 and 100 ms after heel strike. Prior to heel strike, the stimulation had no effect on the Q EMG. The latency of both peaks in the response was too long to be explained by a monosynaptic pathway to Q motoneurones. During voluntary tonic co-contraction of Q and tibialis anterior (TA) while standing, only the first of the two peaks was evoked by the CPN stimulation despite a background EMG activity level in the Q and TA muscles corresponding to that observed 30–60 ms after heel strike during walking. Stimulation of cutaneous nerves did not evoke a similar biphasic facilitation in the Q motoneurones, which suggests that muscular afferents mediate the response. The second peak had a higher threshold than the earlier peak. During cooling of the CPN, the latency of the second peak was more prolonged than the latency of the earlier peak. This suggests that afferents of different diameters contributed to the two peaks. It is proposed that afferents from TA assist the contraction of Q during walking via spinal interneurones to stabilize the knee joint and maintain upright posture during walking.     

Effect of sensory inputs on the soleus H-reflex amplitude during robotic passive stepping in humans

We investigated the modulation of the soleus (Sol) Hoffmann (H-) reflex excitability by peripheral sensory inputs during passive stepping using a robotic-driven gait orthosis in healthy subjects and spinal cord-injured patients. The Sol H-reflex was evoked at standing and at six phases during passive stepping in 40 and 100% body weight unloaded conditions. The Sol H-reflex excitability was significantly inhibited during passive stepping when compared with standing posture at each unloaded condition. During passive stepping, the H-reflex amplitude was significantly smaller in the early- and mid-swing phases than in the stance phase, which was similar to the modulation pattern previously reported for normal walking. No significant differences were observed in the H-reflex amplitude between the two unloaded conditions during passive stepping. The reflex depression observed at the early part of the swing phase during passive stepping might be attributed to the sensory inputs elicited by flexion of the hip and knee joints. The present study provides evidence that peripheral sensory inputs have a significant role in phase-dependent modulation of the Sol H-reflex during walking, and that the Sol H-reflex excitability might be less affected by load-related afferents during walking.     

Stimulation of the group I extensor afferents prolongs the stance phase in walking cats

Group I afferents in nerves innervating the lateral gastrocnemius-soleus (LG-Sol), plantaris (P1), and vastus lateralis/intermedius (VL/VI) muscles were stimulated during walking in decerebrate cats. The stimulus trains were triggered at a fixed delay following the onset of bursts in the medial gastrocnemius muscle. Stimulation of all three nerves with long stimulus trains (>600 ms) prolonged the extensor bursts and delayed the onset of flexor burst activity. LG-Sol nerve stimulation had the strongest effect; often delaying the onset of flexor burst activity until the stimulus train was ended. By contrast, flexor bursts were usually initiated before the end of the stimulus train to the P1 and VL/VI nerves. The minimum stimulus strength required to increase the cycle period was between 1.3×threshold and 1.6×threshold for all three nerves. Simultaneous stimulation of the P1 and VL/VI nerves produced a larger effect on the cycle period than stimulation of either nerve alone. The spatial summation of inputs from knee and ankle muscles suggests that the excitatory action of the group I afferents during the stance phase is distributed to all leg extensor muscles. Stimulation of the group I afferents in extensor nerves generally produced an increase in the amplitude of the heteronymous extensor EMG towards the end of the stance phase. This increase in amplitude occurred even though there were only weak monosynaptic connections between the stimulated afferents and the motoneurones that innervated these heteronymous muscles. This suggests that the excitation was produced via oligosynaptic projections onto the extensor motoneuronal pool. Stimulation with 300 ms trains during the early part of flexion resulted in abrupt termination of the swing phase and reinitiation of the stance phase of the step cycle. The swing phase resumed coincidently with the stimulus offset. Usually, stimulation of two extensor nerves at group I strengths was required to elicit this effect. We were unable to establish the relative contributions of input from the group 1a and group 1b afferents to prolonging the stance phase. However, we consider it likely that group Ib afferents contribute significantly, since their activation has been shown to prolong extensor burst activity in reduced spinal preparations. Thus, our results add support to the hypothesis that unloading of the hindlimb during late stance is a necessary condition for the initiation of the swing phase in walking animals.     

Modulation of stretch reflexes during imposed walking movements of the human ankle.

Our overall objectives were to examine the role of peripheral afferents from the ankle in modulating stretch reflexes during imposed walking movements and to assess the mechanical consequences of this reflex activity. Specifically we sought to define the changes in the electromyographic (EMG) and mechanical responses to a stretch as a function of the phase of the step cycle. We recorded the ankle position of a normal subject walking on a treadmill at 3 km/h and used a hydraulic actuator to impose the same movements on supine subjects generating a constant level of ankle torque. Small pulse displacements, superimposed on the simulated walking movement, evoked stretch reflexes at different phases of the cycle. Three major findings resulted: 1) soleus reflex EMG responses were influenced strongly by imposed walking movements. The response amplitude was substantially smaller than that observed during steady-state conditions and was modulated throughout the step cycle. This modulation was qualitatively similar to that observed during active walking. Because central factors were held constant during the imposed walking experiments, we conclude that peripheral mechanisms were capable of both reducing the amplitude of the reflex EMG and producing its modulation throughout the movement. 2) Pulse disturbances applied from early to midstance of the imposed walking cycle generated large reflex torques, suggesting that the stretch reflex could help to resist unexpected perturbations during this phase of walking. In contrast, pulses applied during late stance and swing phase generated little reflex torque. 3) Reflex EMG and reflex torque were modulated differently throughout the imposed walking cycle. In fact, at the time when the reflex EMG response was largest, the corresponding reflex torque was negligible. Thus movement not only changes the reflex EMG but greatly modifies the mechanical output that results.     

Suppressive musculocutaneous reflexes in tibialis anterior following upper leg stimulation at the end of the swing phase

In the cat it is known that the distribution and modulation of the so-called P2 responses are similar, irrespective of whether they are obtained with electrodes implanted in the different skin areas or in the various leg muscles. In man it is known that the specific stimulation of cutaneous afferents from different parts of the foot evokes P2 responses, the phase-dependent modulation pattern of which exhibits both location-specific and common features. Responses generally differ, but one striking feature is the occurrence of suppressive responses in the tibialis anterior (TA) of the ipsilateral (i) leg at the end of the swing phase independent of the nerve stimulated. The question arises of whether this aspecificity is limited to the foot. Can similar suppressive P2 responses in iTA be obtained when afferents outside the region of the foot are stimulated during walking? If so this would indicate that there is a very general suppression occurring of input to the TA motor neuron pool, for example through presynaptic inhibition of a corticospinal drive. To answer this type of question the motor responses following transcutaneous stimulation of the rectus femoris (RF) and the motor responses following stimulation of the femoral nerve branch innervating the skin area above the quadriceps were determined during human locomotion. Electromyographic (EMG) activity in iTA was recorded by means of surface electrodes. In all subjects (N=10), the first consistent responses following RF stimulation occurred at about 80 ms poststimulus. The amplitude of these responses showed a clear phase-dependent modulation pattern. Facilitatory responses occurred during the end stance and early swing phase and turned into suppressive responses at the end of the swing phase. To investigate whether cutaneous afferents overlying the RF determined some of the responses following transcutaneous RF stimulation, the experiments were repeated following local anesthesia of the skin under the stimulation electrodes. This did not affect the responses substantially, indicating that most of the RF stimulation results were related to activation of muscle afferents. A similar phase-dependent modulation pattern was found following stimulation of cutaneous afferents of the femoral nerve (Fn). However, this phase-dependent modulation pattern was less pronounced and less consistent over the subjects when compared to the one found following RF stimulation. Our first conclusion is that the results show that P2 reflexes can be elicited both by stimulation of cutaneous afferents in the foot and by proximal cutaneous nerve and muscle stimulation. Secondly, it can be concluded that the suppressive responses at the end of the swing phase are present for both RF stimulation and stimulation of cutaneous afferents of the foot. This result indicates that a wide variety of afferent inputs have a suppressive influence on the input drive to TA motor neurons just prior to heel strike.     

Vibration-induced changes in EMG during human locomotion

The present study was set up to examine the contribution of Ia afferent input in the generation of electromyographic (EMG) activity. Subjects walked blindfolded along a walkway while tendon vibration was applied continuously to a leg muscle. The effects of vibration were measured on mean EMG activity in stance and swing phase. The results show that vibration of the quadriceps femoris (Q) at the knee and of biceps femoris (BF) at the knee enhanced the EMG activity of these muscles and this occurred mainly in the stance phase of walking. These results suggest involvement of Ia afferent input of Q and BF in EMG activation during stance. In contrast, vibration of muscles at the ankle and hip had no significant effect on burst amplitude. Additionally, the onset time of tibialis anterior was measured to look at timing of phase transitions. Only vibration of quadriceps femoris resulted in an earlier onset of tibialis anterior within the gait cycle, suggesting involvement of these Ia afferents in the triggering of phase transitions. In conclusion, the results of the present study suggest involvement of Ia afferent input in the control of muscle activity during locomotion in humans. A limited role in timing of phase transitions is proposed as well.     

Evidence for excitation of the human lower limb motoneurones by group II muscle afferents

The possibility was investigated that stimulation of high-threshold afferents in the common peroneal nerve (CPN) evokes excitation of quadriceps (Q) motoneurones in humans. Effects of conditioning stimuli at motor threshold (1×MT) and at higher intensities were compared on both the Q H-reflex and the post-stimulus time histogram (PSTH) of individual motor units. At 1×MT, CPN stimulation evokes a facilitation, which has been shown to be caused by an interneuronally mediated group I excitation. Increasing the CPN stimulus intensity above 2×MT caused this early excitation to increase and a later facilitation to appear both in the H-reflex and in the PSTH of single units. The later excitation had its threshold between 2 and 3×MT, and it appeared 4–8 ms after the group I-induced excitation. The higher threshold and the longer latency suggest that this excitation is evoked by afferents with a smaller diameter than group I afferents, and group II afferents meet this criterion.     

Reflex responses in active muscles elicited by stimulation of low-threshold afferents from the human foot.

1. Reflex responses were elicited in muscles that act at the ankle by electrical stimulation of low-threshold afferents from the foot in human subjects who were reclining supine. During steady voluntary contractions, stimulus trains (5 pulses at 300 Hz) were delivered at two intensities to the sural nerve (1.2-4.0 times sensory threshold) or to the posterior tibial nerve (1.1-3.0 times motor threshold for the intrinsic muscles of the foot). Electromyographic (EMG) recordings were made from tibialis anterior (TA), peroneus longus (PL), soleus (SOL), medial gastrocnemius (MG), and lateral gastrocnemius (LG) muscles by the use of intramuscular wire electrodes. 2. As assessed by averages of rectified EMG, stimulation of the sural or posterior tibial nerves at nonpainful levels evoked a complex oscillation with onset latencies as early as 40 ms and lasting up to 200 ms in each muscle. The most common initial responses in TA were a decrease in EMG activity at an onset latency of 54 ms for sural stimuli, and an increase at an onset latency of 49 ms for posterior tibial stimuli. The response of PL to stimulation of the two nerves began with a strong facilitation of 44 ms (sural) and 49 ms (posterior tibial). With SOL, stimulation of both nerves produced early inhibition beginning at 45 and 50 ms, respectively. With both LG and MG, sural stimuli produced an early facilitation at 52-53 ms. However, posterior tibial stimuli produced different initial responses in these two muscles: facilitation in LG at 50 ms and inhibition in MG at 51 ms. 3. Perstimulus time histograms of the discharge of 61 single motor units revealed generally similar reflex responses as in multiunit EMG. However, different reflex components were not equally apparent in the responses of different single motor units: an individual motor unit could respond slightly differently with a change in stimulus intensity or background contraction level. The multiunit EMG record represents a global average that does not necessarily depict the precise pattern of all motor units contributing to the average. 4. When subjects stood erect without support and with eyes closed, reflex patterns were seen only in active muscles, and the patterns were similar to those in the reclining posture. 5. It is concluded that afferents from mechanoreceptors in the sole of the foot have multisynaptic reflex connections with the motoneuron pools innervating the muscles that act at the ankle. When the muscles are active in standing or walking, cutaneous feedback may play a role in modulating motoneuron output and thereby contribute to stabilization of stance and gait.     

Differential regulation of crossed cutaneous effects on the soleus H-reflex during standing and walking in humans

Although sensory inputs from the contralateral limb strongly modify the amplitude of the Hoffmann (H-) reflex in a static posture, it remains unknown how these inputs affect the excitability of the monosynaptic H-reflex during walking. Here, we investigated the effect of the electrical stimulation of a cutaneous (CUT) nerve innervating the skin on the dorsum of the contralateral foot on the excitability of the soleus H-reflex during standing and walking. The soleus H-reflex was conditioned by non-noxious electrical stimulation of the superficial peroneal nerve in the contralateral foot. Significant crossed facilitation of the soleus H-reflex was observed at conditioning-to-test intervals in a range of 100–130 ms while standing, without any change in the background soleus electromyographic (EMG) activity. In contrast, the amplitude of the soleus H-reflex was significantly suppressed by the contralateral CUT stimulation in the early-stance phase of walking. The background EMG activity of the soleus muscle was equivalent between standing and walking tasks and was unaffected by CUT stimulation alone. These findings suggest that the crossed CUT volleys can affect the presynaptic inhibition of the soleus Ia afferents and differentially modulate the excitability of the soleus H-reflex in a task-dependent manner during standing and walking.     

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

Summary Phase-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.     

Characterisation of the quadriceps stretch reflex during the transition from swing to stance phase of human walking

The main objective of this study was to characterize the stretch reflex response of the human thigh muscles to an unexpected knee flexion at the transition from stance to swing during walking. Eleven healthy subjects walked on a treadmill at their preferred speed. Reliable and constant knee flexions (6–12° amplitude, 230–350°/s velocity, 220 ms duration) were applied during the late swing and early stance phase of human walking by rotating the knee joint with a specifically designed portable stretch apparatus affixed to the left knee. Responses from rectus femoris (RF), vastus lateralis (VL), vastus medialis (VM), biceps femoris (BF), medial hamstrings (MH) and medial gastrocnemius (GM) were recorded via bipolar surface electromyograms (EMG). The onset of the response in the RF, VL and VM, remained stable and independent of the time in the step cycle when the stretch was applied. Across all subjects the response onset (mean ± SD) occurred at 23±1, 24±1 and 23±1 ms for RF, VL and VM, respectively. The duration of the initial response was 90–110 ms, at which time the EMG signal returned towards baseline levels. Three reflex response windows, labelled the short latency reflex (SLR), the medium latency reflex (MLR) and the late latency reflex response (LLR), were analysed. The medium and late reflex responses of all knee extensors increased significantly (p=0.008) as the gait cycle progressed from swing to stance. This was not related to the background EMG activity. In contrast, during standing at extensor EMG levels similar to those attained during walking the reflex responses were dependent on background EMG. During walking, LLR amplitudes expressed as a function of the background activity were on average two to three times greater than SLR and MLR reflex amplitudes. Distinct differences in SLR and LLR amplitude were observed for RF, VL and VM but not in the MLR amplitude. This may be related to the different pathways mediating the SLR, MLR and LLR components of the stretch response. As for the knee extensor antagonists, they exhibited a response to the stretch of the quadriceps at latencies short enough to be monosynaptic. This is in agreement with the suggestion by Eccles and Lundberg (1958) that there may be functional excitatory connections between the knee extensors and flexors in mammals.     

Excitability of the soleus H-reflex arc during walking and stepping in man

Summary In eight normal subjects, the excitability of the soleus (Sol) H-reflex was tested in parallel with Sol length changes, EMGs of leg and thigh muscles and ground contact phases, during three different pacing movements: bipedal treadmill walking, single limb treadmill walking, and single-limb stepping on one spot. A computerized procedure was used which compensated for changes in stimulus effectiveness that occurred during free motion. In the three paradigms examined, significant excitability modulations were observed with respect to a control level determined in standing weight-bearing position. During bipedal treadmill walking, excitability was decreased in the early stance, maximally enhanced in the second half of the stance, and again decreased during the end-stance and the whole swing phase, with a minimum value around the toe off period. The main modulation pattern was retained during single-limb treadmill walking. During single-limb stepping on one spot, the stance-phase increase in excitability and the swing phase depression were still present. However, in the second half of the swing phase, reflex responsiveness returned to reference level, which was maintained during the subsequent contact period. Moreover, a decrease in reflex excitability was detected around the mid-stance. The time course of the described modulations was only partly correlated with the EMG and length changes of the Sol muscle. Furthermore, in the three movements tested, during the early stance phase, the excitability of the H-reflex arc did not correspond to the one expected on the basis of the available H-reflex studies performed under static conditions. It is suggested that, at least in certain stride phases (e.g. around the early contact period), an active regulation affects the transmission in the Sol myotatic arc during the pacing movements investigated.     

Gating and reversal of reflexes in ankle muscles during human walking

Summary Phase-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.     

Earth-referenced handrail contact facilitates interlimb cutaneous reflexes during locomotion

The purpose of this study was to investigate whether the gating of interlimb cutaneous reflexes is altered by holding an earth-referenced handrail during locomotion. In the first experiment, subjects performed locomotor tasks of varying difficulty (level walking, incline walking, and stair climbing) while lightly holding an earth-referenced rail. In the second experiment, the extent of rail contact and nature of the rail stability (e.g., fixed vs. mobile rail) were varied while subjects performed incline walking. Cutaneous reflexes were evoked by delivering trains of electrical stimulation to the sural nerve at the ankle. EMG data were collected continuously from muscles in the upper and lower limbs and trunk. Results showed that modulation of reflexes across the body changed when the rail was held. Most interestingly, a facilitatory reflex in the shoulder extensor posterior deltoid emerged during swing phase only when subjects held a rail. This facilitatory reflex was largest during the more challenging tasks of incline walking and stair climbing, A similar reflex facilitation was observed in the elbow extensor triceps brachii. The observed facilitation of reflexes in triceps brachii and posterior deltoid was specifically expressed only when subjects held an earth-referenced rail. This suggests that interlimb reflexes in arm extensors may be enhanced to make use of a supportive handrail for stability during gait. Therefore, holding a rail may cause global changes in reflex thresholds across the body that may have widespread functional relevance for assisting in the maintenance of postural stability during locomotion.     

Loading during the stance phase of walking in humans increases the extensor EMG amplitude but does not change the duration of the step cycle

 Prior work from mammals suggests that load experienced by extensor muscles of the hindlimbs (i.e. Duysens and Pearson 1980; Pearson and Collins 1993; Fouad and Pearson 1997) or cutaneous afferents from the plantar surface of the foot (Duysens and Pearson 1976; Guertin et al. 1995) enhances activity in extensor muscles during the stance phase, and delays the onset of flexor activity associated with the swing phase. The presumed functional significance of this phenomenon is that extensor activity of the supporting limb during walking can: (a) reinforce the supporting function in proportion to the load experienced, and (b) prolong the stance phase until unloading of the limb has occurred. Whether a similar functional role exists for load-sensitive afferents during walking in the human is unknown. In this study, the effect of adding or removing a substantial load (30% of body weight) at the centre of mass was studied in healthy adult human subjects. Loads were applied near the centre of mass to avoid the need for postural adjustments which might confound the interpretation of the results. Subjects walked on a treadmill with either: (a) a sustained increase or decrease in load, or (b) a sudden unexpected increase or decrease in load. In general, subjects responded to the changes in load by changing the amplitude of the extensor electromyographic (EMG) bursts. For example, with sudden unexpected additions in load, the average increase in amplitude was 40% for the soleus across the stance phase, and 134% for the quadriceps during the early part of the stance phase. Extensor EMGs increased with both sustained and sudden increases in load. Extensor EMG durations also increased (average increase in duration of 4% for soleus with sudden loading, and 7% for sustained loading). Cycle duration hardly changed (average increase of 0.5% with both sudden and sustained loading). These results differ from those of infants subjected to a similar perturbation during supported walking. A large change in timing (i.e. an increase in the duration of the stance phase by 30% and the step cycle by 28%) was seen in the infants, with no change in the amplitude of the EMG burst (Yang et al. 1998). These results suggest that the central nervous system can control the timing and amplitude of extensor EMG activity in response to loading independently. Maturation of the two components most likely occurs independently. In the adult, independent control of the two components may provide greater flexibility of the response. Received: 28 April 1998 / Accepted: 3 September 1998     

Voluntary control of human gait: conditioning of magnetically evoked motor responses in a precision stepping task

 The aim of this study was to investigate visuomotor control during human gait. It was assumed that visual input should modulate transcranially evoked motor potentials (EMPs) during walking. The effect of transcranial magnetic stimulation (TMS) in a visually guided precision stepping task was compared with that during normal gait. EMPs were studied in tibialis anterior (TA), gastrocnemius (GM), and abductor digiti minimi (AD) muscles during treadmill walking. In both stepping tasks, a facilitation of EMPs was observed prior to activation of the respective leg muscle. EMP facilitation proved to be modulated throughout the stride cycle when normalising EMP with respect to the underlying electromyogram (EMG). Facilitation was strongest in TA prior to the swing phase. Significant differences of EMP facilitation between the visual and control tasks were present. In the visual task, maximal facilitation of TA EMPs prior to and during the swing phase was decreased compared to the control task. Conversely, there was increased facilitation of GM EMPs during swing phase of the visual task, prior to the heel strike and prior to the plantarflexion, which was the moment when the target was hit. Thus, the effect of visual input upon EMPs in TA and GM was differential and reciprocal according to the respective functional state. The results support the hypothesis of a conditioning effect of visual or, alternatively volitional, drive on EMPs during stepping. Received: 24 June 1998 / Accepted: 4 February 1999     

Corticospinal input in human gait: modulation of magnetically evoked motor responses

 Transcranial magnetic stimulation (TMS) of the motor cortex was applied during locomotion to investigate the significance of corticospinal input upon the gait pattern. Evoked motor responses (EMR) were studied in the electromyogram (EMG) of tibialis anterior (TA), gastrocnemius (GM) and, for reference, abductor digiti minimi (AD) muscles by applying below-threshold magnetic stimuli during treadmill walking in healthy adults. Averages of 15 stimuli introduced randomly at each of 16 phases of the stride cycle were analysed. Phase-dependent amplitude modulation of EMR was present in TA and GM which did not always parallel the gait-associated modulation of the EMG activity. No variation of onset latency of the EMR was observed. The net modulatory response was calculated by comparing EMR amplitudes during gait with EMR amplitudes obtained (at corresponding background EMG activities) during tonic voluntary muscle contraction. Large net responses in both muscles occurred prior to or during phasic changes of EMG activity in the locomotor pattern. This facilitation of EMR was significantly higher in leg flexor than extensor muscles, with maxima in TA prior to and during late swing phase. A comparison of this facilitation of TA EMR prior to swing phase and prior to a phasic voluntary foot dorsiflexion revealed a similar onset but an increased amount of early facilitation in the gait condition. The modulated facilitation of EMR during locomotion could in part be explained by spinal effects which are different under dynamic and static motor conditions. However, we suggest that changes in corticospinal excitability during gait are also reflected in this facilitation. This suggestion is based on: (1) the similar onset yet dissimilar size of facilitatory effects in TA EMR prior to the swing phase of the stride cycle and during a voluntary dynamic activation, (2) the inverse variation of EMR and EMG amplitudes during this phase, and (3) the occurrence of this inversion at stimulation strengths below motor threshold (motor threshold was determined during weak tonic contraction and EMR were facilitated during gait). It is hypothesized that the facilitation is phase linked to ensure postural stability and is most effective during the phases prior to and during rhythmical activation of the leg muscles resulting in anticipatory adjustment of the locomotor pattern. Received: 17 May 1996 / Accepted: 29 November 1996     

The role of cutaneous afferents in controlling locomotion evoked by epidural stimulation of the spinal cord in decerebrate cats

The effects of the cutaneous input on the formation of the locomotor pattern in conditions of epidural stimulation of the spinal cord in decerebrate cats were studied. Locomotor activity was induced by rhythmic stimulation of the dorsal surface of spinal cord segments L4-L5 at a frequency of 3-5 Hz. Electromyograms (EMG) recorded from the antagonist muscles quadriceps, semitendinosus, tibialis anterior, and gastrocnemius lateralis were recorded, along with the kinematics of stepping movements during locomotion on a moving treadmill and reflex responses to single stimuli. Changes in the pattern of reactions observed before and after exclusion of cutaneous receptors (infiltration of lidocaine solution at the base of the paw or irrigation of the paw pads with chlorothane solution) were assessed. This treatment led to impairment of the locomotor cycle: the paw was placed with the rear surface downward and was dragged along in the swing phase, and the duration of the stance phase decreased. Exclusion of cutaneous afferents suppressed the polysynaptic activity of the extensor muscles and the distal flexor muscle of the ipsilateral hindlimb during locomotion evoked by epidural stimulation of the spinal cord. The effects of exclusion of cutaneous afferents on the monosynaptic component of the EMG response were insignificant.     

Adaptive control for backward quadrupedal walking. II. Hindlimb muscle synergies

1. To compare the basic hindlimb synergies for backward (BWD) and forward (FWD) walking, electromyograms (EMG) were recorded from selected flexor and extensor muscles of the hip, knee, and ankle joints from four cats trained to perform both forms of walking at a moderate walking speed (0.6 m/s). For each muscle, EMG measurements included burst duration, burst latencies referenced to the time of paw contact or paw off, and integrated burst amplitudes. To relate patterns of muscle activity to various phases of the step cycle, EMG records were synchronized with kinematic data obtained by digitizing high-speed ciné film. 2. Hindlimb EMG data indicate that BWD walking in the cat was characterized by reciprocal flexor and extensor synergies similar to those for FWD walking, with flexors active during swing and extensors active during stance. Although the underlying synergies were similar, temporal parameters (burst latencies and durations) and amplitude levels for specific muscles were different for BWD and FWD walking. 3. For both directions, iliopsoas (IP) and semitendinosus (ST) were active as the hip and knee joints flexed at the onset of swing. For BWD walking, IP activity decreased early, and ST activity continued as the hip extended and the knee flexed. For FWD walking, in contrast, ST activity ceased early, and IP activity continued as the hip flexed and the knee extended. For both directions, tibialis anterior (TA) was active throughout swing as the ankle flexed and then extended. A second ST burst occurred at the end of swing for FWD walking as hip flexion and knee extension slowed for paw contact. 4. For both directions, knee extensor (vastus lateralis, VL) activity began at paw contact. Ankle extensor (lateral gastrocnemius, LG) activity began during midswing for BWD walking but just before paw contact for FWD walking. At the ankle joint, flexion during the E2 phase (yield) of stance was minimal or absent for BWD walking, and ankle extension during BWD stance was accompanied by a ramp increase in LG-EMG activity. At the knee joint, the yield was also small (or absent) for BWD walking, and increased VL-EMG amplitudes were associated with the increased range of knee extension for BWD stance. 5. Although the uniarticular hip extensor (anterior biceps femoris, ABF) was active during stance for both directions, the hip flexed during BWD stance and extended during FWD stance.(ABSTRACT TRUNCATED AT 400 WORDS)