Pattern of reflex responses in lower limb muscles to a resistance in walking man

Reflex responses in the lower limbs were investigated using electromyographic and kinematic techniques in man walking on a treadmill. A momentary resistance was applied to one leg at three selected points in the step cycle. The responses to such stimuli, as well as the locomotor activity, were picked up electromyographically and displayed on a four channel oscilloscope. Four superficial muscles viz: gluteus medius, vastus lateralis, rectus femoris and tibialis anterior were studied in both ipsilateral and contralateral legs. In general it was found that the ipsilateral leg muscles produced a response throughout the step cycle regardless of whether the muscle was active or silent at the time the reflex occurred. In contrast, contralateral leg muscles showed a different pattern of response which depended on where the resistance was applied in the step cycle. The long reflex latency, of the order of 80 ms, was a consistent feature of the responses and suggests the possible involvement of supra-spinal pathways. The latencies for a particular muscle were identical on the ipsi- and contralateral sides. The durations of the swing and stance phases of the step cycle were also recorded but showed no change due to application of the resistance. In general, the results indicate that the body has the inherent ability to reinforce the ongoing locomotor muscle activity in response to external stimuli in order to maintain upright balanced walking.     

Gait acts as a gate for reflexes from the foot

During human gait, electrical stimulation of the foot elicits facilitatory P2 (medium latency) responses in TA (tibialis anterior) at the onset of the swing phase, while the same stimuli cause suppressive responses at the end of swing phase, along with facilitatory responses in antagonists. This phenomenon is called phase-dependent reflex reversal. The suppressive responses can be evoked from a variety of skin sites in the leg and from stimulation of some muscles such as rectus femoris (RF). This paper reviews the data on reflex reversal and adds new data on this topic, using a split-belt paradigm. So far, the reflex reversal in TA could only be studied for the onset and end phases of the step cycle, simply because suppression can only be demonstrated when there is background activity. Normally there are only 2 TA bursts in the step cycle, whereas TA is normally silent during most of the stance phase. To know what happens in the stance phase, one needs to have a means to evoke some background activity during the stance phase. For this purpose, new experiments were carried out in which subjects were asked to walk on a treadmill with a split-belt. When the subject was walking with unequal leg speeds, the walking pattern was adapted to a gait pattern resembling limping. The TA then remained active throughout most of the stance phase of the slow-moving leg, which was used as the primary support. This activity was a result of coactivation of agonistic and antagonistic leg muscles in the supporting leg, and represented one of the ways to stabilize the body. Electrical stimulation was given to a cutaneous nerve (sural) at the ankle at twice the perception threshold. Nine of the 12 subjects showed increased TA activity during stance phase while walking on split-belts, and 5 of them showed pronounced suppressions during the first part of stance when stimuli were given on the slow side. It was concluded that a TA suppressive pathway remains open throughout most of the stance phase in the majority of subjects. The suggestion was made that the TA suppression increases loading of the ankle plantar flexors during the loading phase of stance.     

On the reflex coactivation of ankle flexor and extensor muscles induced by a sudden drop of support surface during walking in humans.

Recent studies have revealed that the stretch reflex responses of both ankle flexor and extensor muscles are coaugmented in the early stance phase of human walking, suggesting that these coaugmented reflex responses contribute to secure foot stabilization around the heel strike. To test whether the reflex responses mediated by the stretch reflex pathway are actually induced in both the ankle flexor and extensor muscles when the supportive surface is suddenly destabilized, we investigated the electromyographic (EMG) responses induced after a sudden drop of the supportive surface at the early stance phase of human walking. While subjects walked on a walkway, the specially designed movable supportive surface was unexpectedly dropped 10 mm during the early stance phase. The results showed that short-latency reflex EMG responses after the impact of the drop (<50 ms) were consistently observed in both the ankle flexor and extensor muscles in the perturbed leg. Of particular interest was that a distinct response appeared in the tibialis anterior muscle, although this muscle showed little background EMG activity during the stance phase. These results indicated that the reflex activities in the ankle muscles certainly acted when the supportive surface was unexpectedly destabilized just after the heel strike during walking. These reflex responses were most probably mediated by the facilitated stretch reflex pathways of the ankle muscles at the early stance phase and were suggested to be relevant to secure stabilization around the ankle joint during human walking.     

Reflex modulation in locusts walking on a treadwheel intracellular recordings from motoneurons

Summary In locusts (Locusta migratoria) walking on a treadwheel, afferents of tarsal hair sensilla were stimulated via chronically implanted hook electrodes (Fig. 1). Stimuli applied to the middle leg tarsus elicited avoidance reflexes (Fig. 2). In quiescent animals, the leg was lifted off the ground and the femur adducted. In walking locusts, the response was phase-dependent. During the stance phase, no reaction was observed except occasional, premature triggering of swing movements; stimuli applied near the end of the swing phase were able to elicit an additional, short leg protraction.Central nervous correlates of phase-dependent reflex modulation were observed by recording intracellularly from motoneuron somata in walking animals. As a rule, motoneurons recruited during the swing phase showed excitatory stimulus-related responses around the end of the swing movement, correlated to the triggering of additional leg protractions (Figs. 3, 4, 5). Motoneurons active during the stance phase were often inhibited by tarsal stimulation, some showed only weak responses (Figs. 8, 9, 10). Common inhibitory motoneuron 1 was excited by tarsal stimulation during all phases of the leg movement (Figs. 6, 7). In one type of flexor tibiae motoneuron, a complex response pattern was observed, involving the inversion of stimulus-related synaptic potentials from excitatory, recorded during rest, to inhibitory, observed during long-lasting stance phases (Figs. 11, 12).The results demonstrate how reflex modulation is represented on the level of synaptic input to motoneurons. They further suggest independent gain control in parallel, antagonistic pathways converging onto the same motoneuron as a mechanism for reflex reversal during locomotion.Abbreviations CI ₁ common inhibitory motoneuron (1) - EMG electromyogram - Feti fast extensor muscle of the tibia     

Triceps surae short latency stretch reflexes contribute to ankle stiffness regulation during human running

During human running, short latency stretch reflexes (SLRs) are elicited in the triceps surae muscles, but the function of these responses is still a matter of controversy. As the SLR is primarily mediated by Ia afferent nerve fibres, various methods have been used to examine SLR function by selectively blocking the Ia pathway in seated, standing and walking paradigms, but stretch reflex function has not been examined in detail during running. The purpose of this study was to examine triceps surae SLR function at different running speeds using Achilles tendon vibration to modify SLR size. Ten healthy participants ran on an instrumented treadmill at speeds between 7 and 15 km/h under 2 Achilles tendon vibration conditions: no vibration and 90 Hz vibration. Surface EMG from the triceps surae and tibialis anterior muscles, and 3D lower limb kinematics and ground reaction forces were simultaneously collected. In response to vibration, the SLR was depressed in the triceps surae muscles at all speeds. This coincided with short-lasting yielding at the ankle joint at speeds between 7 and 12 km/h, suggesting that the SLR contributes to muscle stiffness regulation by minimising ankle yielding during the early contact phase of running. Furthermore, at the fastest speed of 15 km/h, the SLR was still depressed by vibration in all muscles but yielding was no longer evident. This finding suggests that the SLR has greater functional importance at slow to intermediate running speeds than at faster speeds.     

Postural adjustments to head movements in the cat

Head movements induced by motor cortex stimulation in the cat are accompanied by variations in the vertical force exerted by each limb. These postural responses were found to show stereotyped patterns: with head dorsiflexions an increase was observed in the force exerted by the anterior limbs and a decrease at the posterior limb level. From comparison between the latencies of the force variations, the beginning of head acceleration, and EMG activity in the limb extensor muscles, it was concluded that triggering of these postural responses is not reflex, but depends on the same command as the movement itself. This early response might be a means of avoiding the downward movement of the trunk which would otherwise result from the reaction force corresponding to the upward head movement.     

Possible functional roles of phase resetting during walking

The walking rhythm is known to show phase shift or "reset" in response to external impulsive perturbations. We tried to elucidate functional roles of the phase reset possibly used for the neural control of locomotion. To this end, a system with a double pendulum as a simplified model of the locomotor control and a model of bipedal locomotion were employed and analyzed in detail. In these models, a movement corresponding to the normal steady-state walking was realized as a stable limit cycle solution of the system. Unexpected external perturbations applied to the system can push the state point of the system away from its limit cycle, either outside or inside the basin of attraction of the limit cycle. Our mathematical analyses of the models suggested functional roles of the phase reset during walking as follows. Function 1: an appropriate amount of the phase reset for a given perturbation can contribute to relocating the system's state point outside the basin of attraction of the limit cycle back to the inside. Function 2: it can also be useful to reduce the convergence time (the time necessary for the state point to return to the limit cycle). In experimental studies during walking of animals and humans, the reset of walking rhythm induced by perturbations was investigated using the phase transition curve (PTC) or the phase resetting curve (PRC) representing phase-dependent responses of the walking. We showed, for the simple double-pendulum model, the existence of the optimal phase control and the corresponding PTC that could optimally realize the aforementioned functions in response to impulsive force perturbations. Moreover, possible forms of PRC that can avoid falling against the force perturbations were predicted by the biped model, and they were compared with the experimentally observed PRC during human walking. Finally, physiological implications of the results were discussed.     

EMG modulation in anticipation of a possible trip during walking in young and older adults.

This study investigated whether changes in lower limb muscle activity occurred in anticipation of a possible perturbation in 11 young (mean age 27 years) and 11 older (mean age 68 years) adults. Altered muscle activity could affect tripping responses and consequently the ecological validity of experimental results of studies on tripping. It was hypothesized that anticipatory muscle activity would be present immediately after a trip, and decrease after several subsequent unperturbed (forewarned) walking trials. Electromyograms of lower limb muscles were measured in 3 conditions: during normal walking, during forewarned walking immediately after a trip, and during forewarned walking several trials after a trip had occurred. Small but statistically significant differences in averaged muscle activity over a stride were found among conditions. Young adults showed slightly increased activity immediately after tripping (co-contraction) in hamstrings, quadriceps and tibialis anterior muscles. This increased activity diminished after several unperturbed trials, although it did not return to the baseline activity levels during normal walking. In older adults, an increased muscle activity among conditions was only discerned in tibialis anterior and soleus muscles. This suggested that older adults prefer to avoid contact with the obstacle over joint stiffening. Yet, for both age-groups, the increases in muscle activity were very small when compared to tripping responses reported in the literature. Therefore, anticipatory effects are not expected to jeopardize the validity of experiments in which subjects are perturbed more than once.     

Different fusimotor reflexes from the ipsi- and contralateral hind limbs of the cat assessed in the same primary muscle spindle afferents

Experiments were performed in forty-five cats anaesthetized with alpha-chloralose. The aim of the study was to investigate a sample of primary muscle spindle afferents from triceps muscle with respect to their fusimotor reflex control from ipsi- as well as contralateral hind limb. Primary muscle spindle afferents of the triceps surae muscle were recorded from the mean rate of firing and the modulation of the afferent response to sinusoidal stretching of the triceps surae muscle was determined. Test measurements were made during tonic stretch of the ipsilateral PBSt, contralateral PBSt, contralateral triceps muscle or during extension of the intact contralateral hind limb. Control measurements were made with ipsi- and contralateral PBSt as well as contralateral triceps muscles relaxed and with contralateral hind limb in resting position. The occurrence and types of fusimotor effects were assessed by comparing test to control responses. The main finding of the present investigation was the great variability in type and size of the fusimotor effects evoked by different ipsi- and contralateral reflex stimuli. Both ipsi- and contralateral stimulations gave rise to predominantly dynamic, predominantly static or mixed static and dynamic fusimotor reflexes. In the same preparation, a given reflex stimulus often caused different reflex responses in different triceps surae primary spindle afferents. In the same afferent unit, different reflex stimuli usually produced fusimotor effects which differed from each other in type and/or size. In general, contralateral whole limb extension and stretch of contralateral PBSt muscles were more potent as reflex stimuli than stretch of the ipsilateral PBSt muscle. Stretch of the contralateral triceps surae muscle was, but for a few afferent units, ineffective as reflexogenic stimulus. It is concluded that the individualized receptive profiles of the primary muscle spindle afferents, which have been postulated in earlier investigations where the effects of different stimuli have been investigated on different cell populations, still seems to hold good when the stimuli are tested on the same units. The individuality of the receptive profiles of gamma-motoneurones is discussed in relation to different motor control hypotheses.     

Afferent feedback in the control of human gait.

Sensory activity contributes to motor control in two fundamentally different ways. It may mediate 'error signals' following sudden external perturbations and it may contribute to the pre-programmed motoneuronal drive. Here we review data, which illustrate these two functions of sensory feedback in relation to human walking. When ankle plantarflexors are unloaded in the stance phase there is a sudden decrease in the sensory activity in muscle and tendon afferents from the active muscles. This decrease in sensory activity results in a drop in EMG activity recorded from the soleus muscle, which demonstrates that the sensory activity contributes importantly to the activation of the muscles. Data suggests that a spinal pathway from gr. II muscle afferents is responsible for this positive feedback contribution to the motoneuronal drive during walking.When cutaneous nerves from the foot are stimulated in the early swing phase of walking a late reflex response may be observed in the tibialis anterior muscle. This reflex may help to ensure that the foot is lifted effectively over an obstacle. Data suggest that this reflex response is at least partly mediated by a transcortical reflex pathway. It seems to be important that reactions to external perturbations are integrated at a supraspinal level during human walking.     

Comparison of global and joint-to-joint methods for estimating the hip joint load and the muscle forces during walking

A three-dimensional musculoskeletal model of the lower limb was developed to study the influence of biarticular muscles on the muscle force distribution and joint loads during walking. A complete walking cycle was recorded for 9 healthy subjects using the standard optoelectronic motion tracking system. Ground contact forces were also measured using a 6-axes force plate. Inverse dynamics was used to compute net joint reactions (forces and torques) in the lower limb. A static optimization method was then used to estimate muscle forces. Two different approaches were used: in the first one named global method, the biarticular muscles exerted a torque on the two joints they spanned at the same time, and in the second one called joint-by-joint method, these biarticular muscles were divided into two mono-articular muscles with geometrical (insertion, origin, via points) and physiological properties remained unchanged. The hip joint load during the gait cycle was then calculated taking into account the effect of muscle contractions. The two approaches resulted in different muscle force repartition: the biarticular muscles were favoured over any set of single-joint muscles with the same physiological function when using the global method. While the two approaches yielded only little difference in the resultant hip load, the examination of muscle power showed that biarticular muscles could produce positive work at one joint and negative work at the other, transferring energy between body segments and thus decreasing the metabolic cost of movement.     

Reflex muscle contractions can be elicited by valgus positional perturbations of the human knee

Experimental evidence on the reflex responses of thigh muscles to valgus mechanical perturbations at the human knee are presented. Random step positional deflections, ranging from 5 degrees to 12 degrees at 60 degrees /s, were applied to the fully extended knees of seven healthy subjects. Subjects were instructed to maintain a constant background co-activation ( approximately 2-11% MVC) of the quadriceps and hamstring muscles prior to and during the mechanical stimulus. We found that the reflex response to sustained valgus joint deflection in the vasti muscles had longer onset latencies (range: 83-92ms) than did the stretch reflex in the same muscles (latencies: 29-31ms). This reflex EMG response consisted typically of a peak followed by sustained muscle activity throughout the step perturbation. The sustained EMG activity was dependent on the amplitude of the perturbing stimulus, but in a nonlinear manner. The long latency of the valgus response suggests that the reflex originates in nonmuscular sensory pathways, potentially from mechanoreceptors lying in periarticular tissues such as joint ligaments and capsule. Analysis of the spatial distribution of reflex responses showed an asymmetrical pattern with preferential activation of medial vs. lateral muscles of the knee. We assess whether these asymmetric reflex contractions could promote joint stability, either by inducing generalized joint stiffening, or by preferential activation of those muscles that are best suited to resist induced ligament strain.     

Passive bipedal walking with phasic muscle contraction

The existence of self-organizing walking patterns is often considered the result of a mechanical system interacting with the environment and a (neural) oscillating unit. The pattern generators might be thought of as an indispensable component for the existence of limit cycle behavior. This paper shows that this is not a necessity for the existence of a self-organizing bipedal walking pattern. Stable walking cycles emerge from a simple passive bipedal structure, with an energy source inevitably present to sustain the oscillation. In this work the energy source is chosen to be phasic muscle contraction. A two-dimensional model is composed of two legs and a hip mass, symbolizing the trunk. The stance leg stiffness is generated by two muscles. The hip stiffness is generated by four muscles. Muscle activation is caused by two reflex-like trigger signals, without feedback control. Human equivalent model parameters such as geometry and mass distribution were assumed. With return map analysis, the model is analyzed on periodic behavior. Stable walking cycles were found and could be manipulated during walking by varying the muscle or reflex parameters, forcing the oscillation to converge to a new attractor. Received: 5 November 1998 / Accepted in revised form: 26 March 1999     

Age-related changes of the stretch reflex excitability in human ankle muscles

The purpose of this study was to characterize the effects of aging on the stretch reflex in the ankle muscles, and in particular to compare the effects on the ankle dorsi-flexor (tibialis anterior: TA) and the plantar-flexor (soleus: SOL). Stretch reflex responses were elicited in the TA and SOL at rest and during weak voluntary contractions in 20 elderly and 23 young volunteers. The results indicated that, in the TA muscle, the elderly group had a remarkably larger long-latency reflex (LLR), whereas no aging effect was found in the short latency reflex (SLR). These results were very different from those in the SOL muscle, which showed significant aging effects in the SLR and medium latency reflex (MLR), but not in the LLR. Given the fact that the LLR of the TA stretch reflex includes the cortical pathway, it is probable that the effects of aging on the TA stretch reflex involve alterations not only at the spinal level but also at the cortical level. The present results indicate that the stretch reflexes of each of the ankle antagonistic muscles are affected differently by aging, which might have relevance to the neural properties of each muscle.     

Some mechanisms of voluntary control of walking in humans

The electrical activities of some muscles of the lower extremities have been studied by the method of presentation of an acoustic signal for a change in walking speed. It has been established that the motor response to a signal has two stages, at which (1) the ratio of muscle activities facilitating acceleration or deceleration of walking is formed and (2) the muscle activity corresponding to the new rate of locomotion is set. The latent period of the first stage of the motor response depends on the temporal relationship of the signal and the phase of muscle activity: it is minimum if the signal coincides with the phase of activity and maximum if the signal is given in the phase of bioelectric silence. It may be supposed that the voluntary control of the locomotion rate is related to at least two types of cortical effects: cyclic and acyclic. The former determine the transition from one speed of walking to another through changing human body posture characteristics (probably, they influence interneurons and motoneurons of reflex arcs); the latter, the characteristics of the new mode of the locomotor cycle by affecting the functional state of the interneurons and motoneurons of the spinal generator of stepping movements.     

Electrophysiological analysis of facial reflex in monkeys: trigemino-naso-labial reflex]

Electrical stimulation of the awake monkey's supra orbital nerve, elicits two successive reflex discharge in both naso-labialis muscles (NL). The responses have a similar high threshold. Similar responses are also elicited on electrical stimulation of the facial skin, whereas flash, click or tapping on the muscle belly are ineffective. These responses bear some resemblances to those obtained in orbicularis oculi muscles ; but the higher threshold and the different organization of the NL responses would suggest that such reflexes may serve a different function from that of the blink reflex.     

Planning of Ballistic Movement following Stroke: Insights from the Startle Reflex

Following stroke, reaching movements are slow, segmented, and variable. It is unclear if these deficits result from a poorly constructed movement plan or an inability to voluntarily execute an appropriate plan. The acoustic startle reflex provides a means to initiate a motor plan involuntarily. In the presence of a movement plan, startling acoustic stimulus triggers non-voluntary early execution of planned movement, a phenomenon known as the startReact response. In unimpaired individuals, the startReact response is identical to a voluntarily initiated movement, except that it is elicited 30-40 ms. As the startReact response is thought to be mediated by brainstem pathways, we hypothesized that the startReact response is intact in stroke subjects. If startReact is intact, it may be possible to elicit more task-appropriate patterns of muscle activation than can be elicited voluntarily. We found that startReact responses were intact following stroke. Responses were initiated as rapidly as those in unimpaired subjects, and with muscle coordination patterns resembling those seen during unimpaired volitional movements. Results were striking for elbow flexion movements, which demonstrated no significant differences between the startReact responses elicited in our stroke and unimpaired subject groups. The results during planned extension movements were less straightforward for stroke subjects, since the startReact response exhibited task inappropriate activity in the flexors. This inappropriate activity diminished over time. This adaptation suggests that the inappropriate activity was transient in nature and not related to the underlying movement plan. We hypothesize that the task-inappropriate flexor activity during extension results from an inability to suppress the classic startle reflex, which primarily influences flexor muscles and adapts rapidly with successive stimuli. These results indicate that stroke subjects are capable of planning ballistic elbow movements, and that when these planned movements are involuntarily executed they can be as rapid and appropriate as those in unimpaired individuals.     

Aging effects on posture-related modulation of stretch reflex excitability in the ankle muscles in humans

The purpose of this study was to examine the effects of aging on posture-related changes of the stretch reflex excitability in the ankle extensor, soleus (SOL), and flexor, tibialis anterior (TA) muscles. Fourteen neurologically normal elderly (mean 68 ± 6 years) and 12 young (mean 27 ± 3 years) subjects participated. Under two postural conditions, upright standing (STD) and sitting (SIT), stretch reflex electromyographic (EMG) responses in the SOL/TA muscle were elicited by imposing rapid ankle dorsi-/plantar-flexion. Under the SIT condition, subjects were asked to keep the SOL background EMG level, which is identical to that under the STD condition. In the SOL muscle, both groups showed significant enhancement of the short-latency stretch reflex (SLR) response when the posture changed from SIT to STD. In the TA muscle, the young group showed significant enhancement of the middle- (MLR) and long-latency stretch reflex (LLR) when the posture changed from SIT to STD; no such modulation was observed in the elderly group. Since the TA stretch reflex responses under the STD condition were comparable in the young and elderly groups, the lack of posture-related modulation of the TA muscle in the elderly group might be explained by augmented stretch reflex excitability under the SIT condition. The present results suggest that the (1) SOL SLR responses are modulated both in the young and elderly subjects when the posture is changed from SIT to STD, (2) TA MLR and LLR responses are not modulated in the elderly subjects when the posture is changed from SIT to STD, while each response is same between the young and elderly in STD, and (3) the effect of aging on the posture-related stretch reflex differs in the SOL and TA muscles.     

Somatosensory cortical unit responses during avoidance conditioning to sound

Unit responses of the primary somatosensory cortical-projection area were recorded in cats with established conditioned avoidance to sound during the conditioned response. Five types of changes in unit activity were distinguished during the conditioned reflex. The responses were 400–1000 msec in duration; their time of onset coincided with that of the expected reinforcing stimulus. As a rule the change in unit activity was preceded by changes in the electromyogram of the corresponding limb muscles. Among neurons responding to the conditioning stimulus, the proportion with a short latent period of response to electrical stimulation of the skin was less than during investigation of ordinary unit responses to the same stimulus.     

Motor pattern selection by combinatorial code of interneuronal pathways

We use a modeling approach to examine ideas derived from physiological network analyses, pertaining to the switch of a motor control network between two opposite control modes. We studied the femur–tibia joint control system of the insect leg, and its switch between resistance reflex in posture control and “active reaction” in walking, both elicited by the same sensory input. The femur–tibia network was modeled by fitting the responses of model neurons to those obtained in animals. The strengths of 16 interneuronal pathways that integrate sensory input were then assigned three different values and varied independently, generating a database of more than 43 million network variants. We demonstrate that the same neural network can produce the two different behaviors, depending on the combinatorial code of interneuronal pathways. That is, a switch between behaviors, such as standing to walking, can be brought about by altering the strengths of selected sensory integration pathways. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users.