Coordinated Interlimb Compensatory Responses to Electrical Stimulation of Cutaneous Nerves in the Hand and Foot During Walking

2003 ◽  
Vol 90 (5) ◽  
pp. 2850-2861 ◽  
Author(s):  
Carlos Haridas ◽  
E. Paul Zehr

It has been shown that stimulation of cutaneous nerves innervating the hand (superficial radial, SR) and foot (superficial peroneal, SP) elicit widespread reflex responses in many muscles across the body. These interlimb reflex responses were suggested to be functionally relevant to assist in motor coordination between the arms and legs during motor tasks such as walking. The experiments described in this paper were conducted to test the hypothesis that interlimb reflexes were phase-dependently modulated and produced functional kinematic changes during locomotion. Subjects walked on a treadmill while electromyographic (EMG) activity was collected continuously from all four limbs, and kinematic recordings were made of angular changes across the ankle, knee, elbow, and shoulder joints. Cutaneous reflexes were evoked by delivering trains of electrical stimulation pseudorandomly to the SP nerve or SR nerves in separate trials. Reflexes were phase-averaged according to the time of occurrence in the step cycle, and phasic amplitudes and latencies were calculated. For both nerves, significant phase-dependent modulation (including reflex reversals) of interlimb cutaneous reflex responses was seen in most muscles studied. Both SR and SP nerve stimulation resulted in significant alteration in ankle joint kinematics. The results suggest coordinated and functionally relevant reflex pathways from the SP and SR nerves onto motoneurons innervating muscles in nonstimulated limbs during walking, thus extending observations from the cat to that of the bipedal human.

1995 ◽  
Vol 73 (5) ◽  
pp. 1947-1964 ◽  
Author(s):  
A. A. Tax ◽  
B. M. Van Wezel ◽  
V. Dietz

1. Cutaneous reflex responses were elicited during human running (8 km/h) on a treadmill by electrical stimulation of the sural nerve at the ankle. Stimulus trains (5 pulses of 1 ms at 200 Hz) at three nonnociceptive intensities, which were 1.5, 2.0, and 2.5 times perception threshold (PT), were delivered at 16 phases of the step cycle. For 11 subjects the surface electromyographic (EMG) activity of both the ipsilateral and contralateral long head of the biceps femoris (iBF and cBF, respectively), the semitendinosus (iST and cST), the rectus femoris (iRF and cRF), and the tibialis anterior (iTA and cTA) were recorded. 2. During human running nonnociceptive sural nerve stimulation appears to be sufficient to elicit large, widespread and statistically significant reflex responses, with a latency of approximately 80 ms and a duration of approximately 30 ms. These reflex responses seem to be an elementary property of human locomotion. This is indicated by the occurrence of the responses in all subjects, the consistency of most of the reflex patterns across the subjects and, apart from a small amount of habituation, the reproducibility of the responses during the course of the experiment. 3. The responses are modulated continuously throughout the step cycle such that their magnitude does not in general covary with the background locomotor activities. This is observed most clearly in iST, iTA, and cTA for which statistically significant reflex reversals are demonstrated, and in cRF and cTA for which the responses are gated during most of the step cycle. 4. The response magnitude generally increases as a function of increasing intensity, whereas the phase-dependent reflex modulation is intensity independent. 5. A functional dissociation within the ipsilateral hamstring muscles is demonstrated: the iBF and iST show an antagonistic reflex pattern (facilitatory and suppressive, respectively) during the periods of synergistic background locomotor activity in the step cycle. Contralaterally, however, the cBF and cST are reflexively activated as close synergists during these periods. 6. The reflex responses and their phase-dependent modulation are different for the homologous muscles in the two legs. Yet, some similarities are observed. These are present rather with respect to the phase of the corresponding leg than with respect to the phase of the stimulated leg. Both observations suggest that the phase-dependent reflex modulation is controlled separately in the ipsilateral and contralateral legs. 7. The response simultaneity in all investigated muscles supports the notion of a coordinated cutaneous interlimb reflex during human running.(ABSTRACT TRUNCATED AT 400 WORDS)


2004 ◽  
Vol 82 (8-9) ◽  
pp. 715-722 ◽  
Author(s):  
J Duysens ◽  
C M Bastiaanse ◽  
B C.M Smits-Engelsman ◽  
V Dietz

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.Key words: human gait, cutaneous reflexes, sural nerve, tibialis anterior, split belt, reflex reversal.


1980 ◽  
Vol 44 (5) ◽  
pp. 1024-1037 ◽  
Author(s):  
J. Duysens ◽  
G. E. Loeb

1. The modulation of reflex responses in up to 10 simultaneously recorded hindlimb muscles was studied in unrestrained cats walking on a treadmill. Single electrical shocks of various strengths were applied to different skin areas of teh hindlimb at different times of the step cycle while the resulting EMG responses were sampled and analyzed. 2. Two excitatory response peaks (P1 and P2) at a latency of about 10 and 25 ms, respectively, were seen in all flexors examined (sartorius, semitendinosus, tibialis anterior, extensor digitorum longus). Stimulation of most skin areas was effective but responses were most easily obtained from stimuli applied to the foot or ankle. During the step cycle there was a marked modulation of the amplitudes of the responses, especially the P2 responses, which grew larger toward the end of stance when a maximum was reached, followed by a steady decline throughout swing. This pattern was very similar for various flexors, although these muscles differed considerably in their normal EMG activity pattern during walking. 3. Flexor responses were absent when the same stimuli were applied during the early stance phase. Instead, inhibition of the ongoing EMG activity was seen at a latency of 10 ms or less in all extensors examined (semimembranosus, quadriceps, soleus, gastrocnemius medialis, flexor digitorum longus). The inhibition was followed by a late excitatory peak (P3) at about 35-ms latency in all extensors except soleus. 4. Certain stimulation sites yielded exceptions to the above patterns. Stimulation of the skin area innervated by the sural nerve yielded larger and earlier MG excitatory responses as compared to stimulation of other skin areas. Activation of the plantar surface of the foot often failed to elicit P2 responses in the hip flexor sartorius, which showed inhibition instead. 5. In the hindlimb contralateral to the stimulus, excitatory responses occurred both in flexors and extensors at a latency of 20-25 ms. The pattern of modulation of these responses was similar to the ipsilateral modulation of P2 flexor and P3 extensor responses. Soleus failed to show a crossed response. 6. The data indicate that flexor and extensor responses differ both with respect to their latency and to their correlation with the ongoing EMG reactivity. It is concluded that these stimuli do not demonstrate reflex reversal in the strict sense in the normal walking cat but that there is modulation of transmission in a flexor excitatory and extensor inhibitory pathway, possibly by the flexor part of the spinal locomotor oscillator. In addition, there are some specialized flexor inhibitory and extensor excitatory pathways. The slow soleus muscle does not seem to be excited through these pathways.


1987 ◽  
Vol 96 (1) ◽  
pp. 11-18 ◽  
Author(s):  
Margarita Martinez-Gomez ◽  
Pablo Pacheco ◽  
Bernardo Dubrovsky

2007 ◽  
Vol 98 (3) ◽  
pp. 1102-1107 ◽  
Author(s):  
Serajul I. Khan ◽  
John A. Burne

Muscle cramp was induced in one head of the gastrocnemius muscle (GA) in eight of thirteen subjects using maximum voluntary contraction when the muscle was in the shortened position. Cramp in GA was painful, involuntary, and localized. Induction of cramp was indicated by the presence of electromyographic (EMG) activity in one head of GA while the other head remained silent. In all cramping subjects, reflex inhibition of cramp electrical activity was observed following Achilles tendon electrical stimulation and they all reported subjective relief of cramp. Thus muscle cramp can be inhibited by stimulation of tendon afferents in the cramped muscle. When the inhibition of cramp-generated EMG and voluntary EMG was compared at similar mean EMG levels, the area and timing of the two phases of inhibition (I1, I2) did not differ significantly. This strongly suggests that the same reflex pathway was the source of the inhibition in both cases. Thus the cramp-generated EMG is also likely to be driven by spinal synaptic input to the motorneurons. We have found that the muscle conditions that appear necessary to facilitate cramp, a near to maximal contraction of the shortened muscle, are also the conditions that render the inhibition generated by tendon afferents ineffective. When the strength of tendon inhibition in cramping subjects was compared with that in subjects that failed to cramp, it was found to be significantly weaker under the same experimental conditions. It is likely that reduced inhibitory feedback from tendon afferents has an important role in generating cramp.


1990 ◽  
Vol 63 (5) ◽  
pp. 1118-1127 ◽  
Author(s):  
L. Villanueva ◽  
K. D. Cliffer ◽  
L. S. Sorkin ◽  
D. Le Bars ◽  
W. D. Willis

1. Recordings were made in anesthetized monkeys from neurons in the medullary reticular formation (MRF) caudal to the obex. Responses of 19 MRF neurons to mechanical, thermal, and/or electrical stimulation were examined. MRF neurons exhibited convergence of nociceptive cutaneous inputs from widespread areas of the body and face. 2. MRF neurons exhibited low levels of background activity. Background activity increased after periods of intense cutaneous mechanical or thermal stimulation. Nearly all MRF neurons tested failed to respond to heterosensory stimuli (flashes, whistle sounds), and none responded to joint movements. 3. MRF neurons were excited by and encoded the intensity of noxious mechanical stimulation. Responses to stimuli on contralateral limbs were greater than those to stimuli on ipsilateral limbs. Responses were greater to stimuli on the forelimbs than to stimuli on the hindlimbs. 4. MRF neurons responded to noxious thermal stimulation (51 degrees C) of widespread areas of the body. Mean responses from stimulation at different locations were generally parallel to those for noxious mechanical stimulation. Responses increased with intensity of noxious thermal stimulation (45-50 degrees C). 5. MRF neurons responded with one or two peaks of activation to percutaneous electrical stimulation applied to the limbs, the face, or the tail. The differences in latency of responses to stimulating two locations along the tail suggested that activity was elicited by activation of peripheral fibers with a mean conduction velocity in the A delta range. Stimulation of the contralateral hindlimb elicited greater responses, with lower thresholds and shorter latencies, than did stimulation of the ipsilateral hindlimb. 6. Electrophysiological properties of monkey MRF neurons resembled those of neurons in the medullary subnucleus reticularis dorsalis (SRD) in the rat. Neurons in the caudal medullary reticular formation could play a role in processing nociceptive information. Convergence of nociceptive cutaneous input from widespread areas of the body suggests that MRF neurons may contribute to autonomic, affective, attentional, and/or sensory-motor processes related to pain.


1990 ◽  
Vol 148 (1) ◽  
pp. 113-128 ◽  
Author(s):  
U. W. E. MÜLLER ◽  
FRANÇOIS CLARAC

1. The effects of cyclic electrical stimulation of the dactyl sensory nerve (DN) on the walking pattern of rock lobsters were examined at the two crucial points within the step cycle: the anterior extreme position (AEP) and the posterior extreme position (PEP). 2. Stimulation during the occurrence of the PEP affected neither the movement pattern of the stimulated leg itself nor that of the ipsilateral adjacent legs. 3. Stimulation of the same intensity during the occurrence of the AEP interrupted the oscillation of the stimulated leg and affected the phase relationships of the ipsilateral adjacent legs. 4. The possibility that indirect influences were mediated by coupling to the substratum can be excluded. Neuronal connections may therefore exist between the funnel canal organs (FCO) of a single leg and the motor output of the adjacent legs. The discussion deals with whether the described channels alone are able to fulfil the requirements of a ‘coordinating mechanism’ as described in the literature.


1992 ◽  
Vol 67 (5) ◽  
pp. 1375-1384 ◽  
Author(s):  
A. M. Aniss ◽  
S. C. Gandevia ◽  
D. Burke

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.


2000 ◽  
Vol 83 (6) ◽  
pp. 3209-3216 ◽  
Author(s):  
Jean-François Perrier ◽  
Boris Lamotte D'Incamps ◽  
Nezha Kouchtir-Devanne ◽  
Léna Jami ◽  
Daniel Zytnicki

The postsynaptic potentials elicited in peroneal motoneurons by either mechanical stimulation of cutaneous areas innervated by the superficial peroneal nerve (SP) or repetitive electrical stimulation of SP were compared in anesthetized cats. After denervation of the foot sparing only the territory of SP terminal branches, reproducible mechanical stimulations were applied by pressure on the plantar surface of the toes via a plastic disk attached to a servo-length device, causing a mild compression of toes. This stimulus evoked small but consistent postsynaptic potentials in every peroneal motoneuron. Weak stimuli elicited only excitatory postsynaptic potentials (EPSPs), whereas increase in stimulation strength allowed distinction of three patterns of response. In about one half of the sample, mechanical stimulation or trains of 20/s electric pulses at strengths up to six times the threshold of the most excitable fibers in the nerve evoked only EPSPs. Responses to electrical stimulation appeared with 3–7 ms central latencies, suggesting oligosynaptic pathways. In another, smaller fraction of the sample, inhibitory postsynaptic potentials (IPSPs) appeared with an increase of stimulation strength, and the last fraction showed a mixed pattern of excitation and inhibition. In 24 of 32 motoneurons where electrical and mechanical effects could be compared, the responses were similar, and in 6 others, they changed from pure excitation on mechanical stimulation to mixed on electrical stimulation. With both kinds of stimulation, stronger stimulations were required to evoke inhibitory postsynaptic potentials (IPSPs), which appeared at longer central latencies than EPSPs, indicating longer interneuronal pathways. The similarity of responses to mechanical and electrical stimulation in a majority of peroneal motoneurons suggests that the effects of commonly used electrical stimulation are good predictors of the responses of peroneal motoneurons to natural skin stimulation. The different types of responses to cutaneous afferents from SP territory reflect a complex connectivity allowing modulations of cutaneous reflex responses in various postures and gaits.


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