Neuroscience Letters, 49 (1984) 291-295
291
Elsevier Scientific Publishers Ireland Ltd.
NSL 02896
CORRECTIVE RESPONSES TO P E R T U R B A T I O N A P P L I E D D U R I N G W A L K I N G IN H U M A N S
MARC BELANGER and AFTAB E. PATLA*
Department of Kinesiology, University of Waterloo, Waterloo, Ontario, N2L 3G1 (Canada) (Received April 19th, 1984; Accepted May llth, 1984)
Key words: locomotion - flexor reflex - ipsilateral - EMG - humans
Modulation of the flexor reflex response during walking in humans following stimulation at 5 points in the step cycle was studied. At heel strike, an extensor response was observed at the ankle and the knee which would allow one to stabilize and plant the ipsilateral foot fast. Later on in the stance, there was a dorsiflexor and an extensor response at the ankle and the knee, respectively, which would result in the removal of the foot from the stimulus without collapsing at the knee. During mid-swing, a flexor reflex response was observed at the ankle and the hip joint. There was a tendency for the normal stride to be longer than the perturbed stride in mid swing and early stance while it was of shorter duration in late stance and early swing.
There has been considerable interest in studying the interaction between peripheral and central regulation of locomotion. In mammals such as cats, researchers found the flexor reflex response to be dependent on the phase of the step cycle [2, 4-8, 14, 16]. Although the flexor reflex has been studied fairly extensively in humans during static posture [3, 9, 10, 15], its dependency on the phase of locomotion has not been examined in detail. Lisin et al. [12], without providing any details, have reported some modulation of the flexor reflex response during locomotion. More recently, the responses in two thigh muscles to sural nerve stimulation demonstrated that the reflex transmission is actively gated during stepping [11]. The present study was undertaken to explore the responses to perturbation systematically. A preliminary report has been presented elsewhere [13]. While the subjects (n = 7) walked at their natural, self-paced speed on the treadmill, an electrical stimulus (train duration of 20 ms, with l0 pulses of 1 ms duration and 4-5 times threshold) was applied unexpectedly via a copper ring on the second toe and a ground electrode on the dorsum of the foot a few centimeters apart. The electrical stimulus triggered by a heel-strike signal was applied at 5 different points in the step cycle: heel strike (HS), toe off (TO), early stance (one-third of the time between HS and TO) (ES), late stance (two4hirds of the time between HS and *Author for correspondence.
0304-3940/84/$ 03.00 © 1984 Elsevier Scientific Publishers Ireland Ltd.
292 TO) (LS) and mid-swing (one-half of the time between TO and HS) (MS). Rectified and filtered (6 Hz, 4th order, zero-lag filter) myoelectric signals from the right tibialis anterior (TA), soleus (SOL), medial gastrocnemius (MG), vastus lateralis (VL), rectus femoris (RF), biceps femoris (long head) (BF) and the foot-switch signal were collected to study the response to the nociceptive stimulus. Each trial record provided a normal and a perturbed step cycle. Five trials for each condition were ensemble averaged. A normal cycle was then subtracted from a perturbed cycle from the same record to give the reflex response. An interactive program provided the latency of the response. The area under the processed signal curves for both the normal and perturbed cycles were determined for 100 ms, starting 20 ms after the onset of the stimulus in the perturbed cycle and the equivalent duration for the normal cycle. The choice of the duration over which the area was calculated eliminated the stimulus artifact. The durations of the normal and perturbed strides, stance and swing phases were determined from the foot-switch signal. Since no concurrent kinematics were recorded, the results are discussed in light of what is known about the biomechanical patterns of normal walking [17]. The area data for the 6 muscles are summarized in Fig. 1. The latency data (resolution _+ 7 ms) are included in brackets throughout the text to indicate the order of response in the muscles studied. The latency values clearly suggest the reflex origin of the response. At HS, during normal walking, high TA and low SOL and MG activites allow the foot to be gently lowered to the ground. The knee is stabilized and maintained in extension at the point of landing by cocontraction of the flexor and extensor muscles. From the latency and area data (Fig. 1) a normal flexor activity was observ ed at the ankle and the knee while the extensor response was facilitated (MG, 81 ms; SOL, 85 ms; VL, 94 ms; RF, 102 ms) when stimulation was presented at HS. Thus it appears that in response to the stimulus at HS the foot is quickly lowered to the ground and the knee is prevented from collapsing by the increased extensor activity. Early in the stance phase, the plantarflexor activity starts to increase whereas the dorsiflexor activity drops. The leg pivots above the foot during normal walking. The knee extensors are activated to prevent the knee buckling and to extend the leg. Also, the hamstrings may be used as hip extensors which help to extend the knee by backward rotation of the thigh. Following stimulation, there was an enhanced dorsiflexor activity (TA, 58 ms) and a normal plantarflexor activity at the ankle. At the knee joint, early in the stance there was an enhanced flexor response (BF, 90 ms) followed by an increased extensor activity (RF, 96 ms). Thus it appears as if the foot was being removed from the stimulus by ankle dorsiflexor activity while the knee collapse was prevented by near simultaneous response in the flexors and extensors. It is also possible that the BF is used as a hip extensor in this situation and thus it would help extension of the knee by rotating the thigh backwards. During late stance, the ankle dorsiflexor activity remains low whereas the plantarflexor activity increases to provide the push-off. At the knee both the flexor and extensor activities are low during normal walking. Following stimulation there was
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Fig. 1. The area under the EMG signal curves (100 ms duration starting 20 ms after stimulus onset) for a normal and perturbed cycle for the 5 stimulation phases are shown for the 6 muscles. *Indicates that the results are statistically significant ( P < 0 . 1 0 ) . The latencies of the responses of the muscles are indicated in the main text.
an increased dorsiflexor (TA, 58 ms) activity at the ankle while there was an increase in BF activity (BF, 76 ms) followed by an increased extensor response (VL, 84 ms; RF, 104 ms) at the knee joint. Considering the resolution in the latency values (_+ 7 ms), the response is similar to the one observed in early stance. The only difference was the enhancement o f VL, a knee extensor. During normal walking, the TA activity increases whereas the plantarflexor ac-
294 tivity is silenced in order to dorsiflex the foot at or immediately following TO. The BF and RF activities begin to increase in order to flex the knee and hip respectively in preparation for the swing. When the stimulus was presented at TO, an enhanced ankle plantarflexor activity (SOL, 92 ms) followed an increase in dorsiflexor activity (TA, 81 ms). At the knee, there was an increased flexor activity (BF, 72 ms) followed by an enhanced RF response (RF, 120 ms). Thus at TO, the lift-off and subsequent swing phase appear to be facilitated by the enhanced ankle, knee and hip flexor activity. In normal locomotion, footdrop during swing is prevented by high dorsiflexor and low plantarflexor activities. The RF and VL activities bring the leg through and prepare it for landing. The hamstrings are activated later to decelerate the leg prior to HS. As a result of stimulation during midswing, there was an increased dorsiflexor activity (TA, 62 ms) followed by an increased plantarflexor activity (SOL, 85 ms) at the ankle. At the knee joint, there was a normal flexor and an enhanced RF response (RF, 100 ms). Thus during swing it appears as if the foot could be withdrawn from the stimulus by enhanced flexor activity at both the ankle and the hip. In animal studies, when the stimulus was applied during the stance phase, enhanced extensor activity was observed in the ankle and the knee joint [7]. This is similar to the response seen in humans in the early stance phase (HS). Also, the responses elicited during T O and MS are similar to the ones seen in cats during the swing phase [7]. The enhanced dorsiflexor response during late stance in humans appears to be the only major difference. This may in part be due to the higher stimulus intensity (4-5 times threshold) used as compared to the animal studies (2-3 times threshold) [2, 7, 16]. High intensity stimulus was used to discern the reflex response from the normal locomotor activity level. Although not statistically significant, the perturbed cycle was of shorter duration than the normal cycle when the stimulus was applied at HS, ES and MS. When the stimulus was applied at LS and TO, the perturbed stride was of equal length or even of slightly longer duration. This agrees with the results obtained from animal studies [1, 6]. To summarize, the response to nociceptive stimulus is modulated depending on the phase of the step cycle. The corrective response in the ipsilateral limb allows the individual to maintain stability and carry on with the ongoing task of locomotion. This work was supported by a grant from the National Science and Engineering Research Council of Canada. The authors gratefully acknowledge the assistance of Dr. J. Frank. 1 Duysens, J., Reflex control of locomotion as revealed by stimulation of cutaneous afferent in spontaneous walking premammillary cats, J. Neurophysiol., 40 (1977) 737-751. 2 Duysens, J. and Pearson, K.G., lpsilateral extensor reflexes and cat locomotion, in R.M. Herman,
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