Phase-Dependent Inhibition of H-Reflexes During Walking in Humans Is Independent of Reduction in Knee Angular Velocity

M. Garrett, T. Kerr, and B. Caulfield

University College Dublin School of Physiotherapy, Mater Hospital, Dublin 7, Ireland


    ABSTRACT
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ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES

Garrett, M., T. Kerr, and B. Caulfield. Phase-Dependent Inhibition of H-Reflexes During Walking in Humans Is Independent of Reduction in Knee Angular Velocity. J. Neurophysiol. 82: 747-753, 1999. The purpose of this investigation was to investigate whether reduction in impulses arising from stretch of the quadriceps by restricting rapid knee flexion in early swing would affect inhibition of the H-reflex during swing. The contribution of afferent input arising from knee angular velocity to phase-dependent modulation of short-latency responses in the soleus was studied by simultaneously measuring joint velocity and soleus H-reflex responses at midstance and midswing phases of treadmill walking in 15 normal subjects. Stimulus strength was varied so that both maximal M and H waves were identified in each subject at midswing and midstance with the knee unrestricted (UK) and with knee movement restricted (RK), using a full leg bivalved cast to immobilize the knee joint. All subjects exhibited short-latency reflex responses in the soleus muscle. The H/M ratio at midswing was significantly reduced compared with midstance under both UK and RK walking conditions (P < 0.0001). When compared with UK walking, knee joint angular velocity during RK walking was significantly reduced at midswing (P < 0.001) and midstance (P < 0.005) compared with UK. There were, however, no significant differences in H/M ratios at midswing and midstance between UK and RK walking tests. Inhibition of the H-reflex in the soleus muscle during swing was not affected by significant reduction in knee angular velocity. These results indicate that the sensory input from changes in angular velocity at the knee does not lay the inhibitory foundation of phase-related reflex modulation in the ankle extensors during walking as suggested by Brooke and colleagues.


    INTRODUCTION
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INTRODUCTION
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The spinal stretch reflex is the fastest response of the mammalian CNS to muscle stretch. The amplitude of the spinal stretch reflex response or its electrical analogue, the H-reflex, elicited by stimulation of the group Ia afferents from soleus, depends on the phase of stimulation within the step cycle in small mammals (Akazawa et al. 1982) and in man (Capaday and Stein 1986; Crenna and Frigo 1987; Garrett et al. 1981). The effect of phase-dependent modulation can be seen by comparing the H-reflexes elicited in the soleus at midswing and midstance. A constant stimulus input at midswing results in a substantially reduced motor output compared with stance (Garrett et al. 1981; Garrett and Caulfield 1996).

The exact balance of central and peripheral influences acting on the neural mechanisms underlying phasic modulation of reflexes in the conscious and freely moving man has yet to be determined. In recent years Brooke and his colleagues have presented evidence that would appear to support control of walking by means of afferent input from the mechanoreceptors of the leg extensors (Brooke et al. 1995, 1997; Cheng et al. 1995). This group (Misiaszek et al. 1995) has recently demonstrated that afferent activity during passive non-weight-bearing locomotor-like rotation of the shank at the knee in the intact anesthetized dog has an inhibitory effect on the H-reflex of the toe extensor. The joint, cutaneous, and muscle receptors around the knee joint were systematically and separately deactivated. Depression of the H-reflex during passive locomotor-like rotation of the knee persisted until the intramuscular receptors were eliminated. Further removal of the remaining receptor groups from joint and skin did not result in restoration of reflex inhibitory modulation. From this they concluded that the occurrence of movement as detected by muscle stretch is the foundation on which all other sources of modulation are overlaid in humans as well as quadrupeds. This hypothesis has very profound implications for understanding the control of reflexes during walking and the reflex abnormalities that occur when injury impairs that control.

Lavoie and Capaday (1996) reported a lack of correlation between soleus H-reflex modulation and simultaneous joint movement throughout the step cycle, indicating that Brooke's hypothesis needs to be examined further. The present investigation, on responses of soleus muscle to soleus nerve stimulation during both unrestricted knee (UK) and restricted knee (RK) walking, investigated the contribution of knee movement to the inhibition of the soleus H-reflex observed in the conscious and freely moving man. The critical data on which this proposition was tested were those obtained during swing because, at this part of the walking cycle, the knee extensor is subject to rapid stretch and the reflex is inhibited. Reflex responses at midstance were recorded to confirm modulation. Reafferent control of modulation of phase-dependent short-latency reflexes at the ankle by input from muscle mechanoreceptors acting about the knee during walking was therefore tested at midswing during two periods of treadmill walking in normal subjects. In the first period, the knee was moving freely. In the second period, knee movement was greatly restricted by a cast encasing the leg. If the occurrence of movement, as detected by muscle stretch receptors from the knee extensor, was the foundation on which all other sources of modulation are overlaid in humans as well as quadrupeds, then a reduction in afferent traffic from the knee extensor muscle stretch receptors would result in reduction of modulation. The conditions at the knee joint at this point of the gait cycle approximate to those obtaining in the investigation of canine H-reflexes (Misiaszek et al. 1995) in that the leg is non-weight-bearing, the knee movements are produced by passive forces and the knee and ankle extensor muscles are classically silent (Perry 1992; Winter 1991). The major advance in the design of the present study is that the H-reflex was investigated in walking subjects with simultaneous measurement of knee joint movement while the knee was moving freely and while restricted by bracing. The null hypothesis was that reduction in impulses arising from stretch of the quadriceps by restricting rapid knee flexion of early swing would not affect inhibition of the H-reflex during swing.


    METHODS
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ABSTRACT
INTRODUCTION
METHODS
RESULTS
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Subject population

Fifteen normal subjects (8 male, 7 female), between 19 and 34 yr old, recruited from a population of undergraduate and postgraduate students were tested for both UK and RK treadmill walking. All subjects gave informed consent and had no known history of neurological or motor disorder. The experimental procedures were approved by the Mater Misericordiae Hospital Ethics Committee.

H-reflex evoking techniques and knee kinematics

Comparison of muscle response to electrical stimulus was the basis of this investigation. Stimulation of the tibial nerve activates the gastrocnemius muscle as well as the soleus. Hugon (1973a) pointed out that comparability of H responses is reduced when EMG response to stimulus is obtained from both muscles. The H-reflex in the gastrocnemius is more readily elicited in the active than in the silent muscle, thus affecting comparison of response during swing with that obtained during stance. The method used in this investigation was directed at eliciting the H-reflex from the soleus alone. H-reflexes were obtained from soleus muscle by direct stimulation of the nerve to soleus. The nerve to soleus was identified in the popliteal fossa by application of 0.5-ms-square response pulses delivered by the negative pole of a constant current stimulator (Digitimer stimulator model DS7). The cathodal electrode was applied at 1-cm intervals along the popliteal crease from the medial border of the popliteal fossa to avoid stimulation of the tibial and common peroneal nerves. Elicitation of an H response without an M response identified the optimal position to stimulate the nerve to soleus (Hugon 1973a). This stimulus site provided repeatable wave forms at midswing and midstance, indicating that responses were obtained from the same motoneurons throughout the test. Maximal M and H responses obtained during the different experimental conditions were monitored and checked for similarity in configuration. Similarity of responses throughout each experimental session indicated that in each experimental condition the EMG responses recorded were from the same motor units.

The hand-held stimulating electrode was then replaced by a spring-loaded saline pad electrode, supported in a plastic housing 1 cm diam, which was secured to the posterior aspect of the subject's knee using thick elastic. The track of the bands on the skin was protected with padded adhesive gauze. The 50-cm2 anode was positioned on the posterior of the subject's thigh, 100 mm proximal to the cathode. An earth pad (100 cm2) was attached to the contralateral thigh to eliminate noise. Prior testing demonstrated that this placement achieved reduction of the stimulus artifact comparable with that observed with placement between the stimulating and recording electrodes while decreasing instrumentation on the test leg.

The recording surface Ag/AgCl electrodes were placed 2 cm apart over the belly of soleus, 3 cm above the insertion of soleus to the Achilles tendon, to minimize pickup of activity from the gastrocnemius muscle (Hugon 1973a). The M and H responses were compared with those previously elicited with the hand-held electrode to confirm optimal position of the stimulating electrode in the popliteal fossa. The EMG signal was preamplified (with a gain of 500) close to the subject to minimize the effect of movement artifacts during data transfer, then digitized with an A/D interface and stored on a computer. Winter (1990) recommends upper cutoff frequencies of 5-10 kHz for computer recognition of individual motor-unit action potentials recorded by surface electrodes. The 8-kHz sampling rate allowed the H-reflex EMG signals to be clearly distinguished from the naturally occurring background EMG (see Fig. 2), which has little content below 0.5 kHz. This allowed identification of the maximal H and maximal M responses during locomotion and direct measurement of the peak-to-peak amplitude. The EMG signal was recorded for 50 ms following the delivery of the electrical stimulus to the subject.

The preferred comfortable walking speed was the median velocity selected by each subject over a period of 10 trials. Each subject then walked at this velocity for a period of at least 20 min during which single stride velocity was calculated at 5-min intervals by means of the optoelectronic movement analysis system. Constancy of single stride velocity was considered to indicate steady-state walking. This protocol had previously been demonstrated to achieve steady-state walking (Garrett et al. 1997). Every subject was instructed to look straight forward during testing because changes in head and neck position have a strong influence on the H-reflex (Hugon 1973a,b). The timing of the stimulus to the nerve to soleus was effected by feeding the foot-switch signal into a delay unit. The delay unit determined the latency between the step cycle marker (signal triggered by heel contact) and the stimulus. It was preset to deliver a stimulus at midswing or midstance. The average time of midswing and midstance was calculated on a sample of 10 randomly selected gait cycles when steady-state walking had been achieved. The resulting range of intrasubject variation for swing and stance duration during the periods of test walking, UK and RK, was typically <10 ms (Table 1). Stimuli were applied at >= 5-s intervals during a period of treadmill walking until a full H-reflex recruitment curve was obtained using the method first described by Garrett et al. (1981), based on that described by Hugon (1973a) in the seated subject. The maximal M response was determined by increasing stimulus intensity to the point where no further increase in the direct motor response was obtained and the H response was abolished. Five H-reflexes were elicited and recorded at this stimulus intensity. The stimulus intensity was then decreased by 10%, and five more H-reflexes were elicited and recorded. This procedure was repeated until no H and no M responses were present.


                              
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Table 1. Swing and stance duration and timing of H-reflex during the periods of test walking, unrestricted and restricted

Knee joint movements were recorded throughout the walking period by means of an optoelectronic motion analysis system (2-D Kinemetrix Gait Analysis System). A charged coupled device (CCD) camera with coaxial infrared arrays and daylight-cut filters monitored infrared pulses reflected from markers during walking. The markers were positioned on the skin overlying each subject's greater trochanter, the midpoint of the knee joint in the line of the shaft of leg, the lateral malleolus, on the shoe overlying the lateral prominence of calcaneus and the 5th metatarsal.

Experimental protocol

Two full-length casts (one anterior section and one posterior section) of the subject's right leg were molded. Space was left between the two cast sections to allow for placement of reflective markers. A window was cut in the posterior section to expose the popliteal fossa. The cast was then removed so that the optimal position of the stimulating electrode could be established.

During the walking trial period of typically 3.5 h, the H-reflex at midstance of unrestricted knee (UK) treadmill walking was elicited first. A full H-reflex recruitment curve was obtained, using the Hugon (1973a) stimulation protocol, adapted for walking (Garrett et al. 1981) while simultaneously recording knee joint movements and gait characteristics.

During restricted knee (RK) treadmill walking, the cast was reapplied. Application of the cast greatly restricted but did not abolish movement of the knee during walking. A complete H-reflex recruitment curve was obtained for each subject at midstance and at midswing for RK treadmill walking as described above for UK. In this way the maximal M and H responses were compared in the different conditions of midstance and midswing during UK and RK walking.

Data analysis

Peak-to-peak amplitude of the H and M responses at midswing and midstance were used to calculate the Hmax/Mmax ratio for each subject in UK and RK walking. It may be suggested that the maximal H response is elicited by a submaximal stimulus, and further activation of alpha -motoneurons may be masked by antidromic conduction of action potentials as the M response develops. This condition applies to all and so does not affect intersubject comparability. Angular displacement and angular velocity at the time of Hmax for UK and RK walking conditions were calculated per subject. Group descriptive statistics were performed for knee joint angular velocity, Hmax/Mmax ratios in the soleus and gait characteristics. A paired t-test was used to compare the effects of UK and RK walking because each of the 15 subjects was examined under both conditions. A two-sided significance level of 5% was taken. Regression analysis was used to test for relationships between joint velocity and Hmax/Mmax ratios separately in UK and RK walking.


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INTRODUCTION
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RESULTS
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REFERENCES

Population averaging yielded a stance duration of 613 ± 58 (SD) ms for UK treadmill walking and 666 ± 85 ms for RK walking. Swing durations of 441 ± 63 ms for UK and 551 ± 68 ms for RK were recorded. The stride characteristics observed in UK walking were of the same order as the experimental data of Winter et al. (1989). There was a significant increase of 9 and 25% in stance and swing durations, respectively, during RK walking compared with UK walking. The group mean velocities observed of 1.4 ± 0.14 m/s in UK treadmill walking and 1.1 ± 0.13 m/s in RK treadmill walking showed highly significant differences (P < 0.0001). However, both velocities are within normal range (Perry 1992).

The effects of rate of stretch of the quadriceps on phasic modulation of the H-reflex during walking were the focus of this investigation. Joint angular velocity was taken as a measure of the rate of change of length of the quadriceps. Group mean values for knee angular velocity at midswing and midstance are set out for UK walking in Table 2, row 1. The time course of knee angular velocity in the gait cycle of a typical subject during UK and RK walking is shown in Fig. 1, A and B. The corresponding angular displacement is shown in Fig. 2, A and B, by stick figures of the leg at six points in the gait cycle. These are heel contact, midstance, toe-off, maximal velocity of knee flexion, midswing and end of swing. During UK walking stretch was imposed on the quadriceps by knee flexion, which began after midstance and achieved a characteristic maximal velocity of flexion of 240°/s immediately after toe-off in this subject (Fig. 1A). Knee extension began at 0.1 s post toe-off where maximal flexion of 70° was observed (Fig. 2A, stick figure 5). At this point the quadriceps presumably reached maximal length, after which their length decreased until the end of swing (Fig. 1A). At midswing, knee extension velocity of 220°/s represents a period of rapid release of stretch.


                              
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Table 2. Average Hmax/Mmax ratios in the soleus muscle and knee angular velocities during walking



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Fig. 1. Angular velocity at the knee joint for 1 gait cycle of a subject for unrestricted knee (UK) walking (A) and restricted knee (RK) walking (B). The duration of the Swing phase of walking and the points of the gait cycle at which stimuli were applied are outlined in each case. Positive values indicate knee flexion; negative values indicate knee extension.



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Fig. 2. Patterns of knee angular displacement are illustrated with stick figures for 6 points of the gait cycle of 1 subject. A: unrestricted knee walking (UK). B: restricted knee walking (RK). These are as follows: 1, heel contact; 2, midstance; 3, toe-off; 4, maximal velocity of knee flexion; 5, midswing; 6, end of swing. Corresponding electromyographic (EMG) records showing maximal direct motor and reflex responses obtained by the same subject during the relevant phase of the walking cycle are illustrated beneath.

Stimuli were applied over the nerve to soleus so that complete H-reflex recruitment curves were obtained at midswing and midstance in both UK and RK treadmill walking. Examples of typical Mmax and Hmax responses are seen for UK walking in Fig. 2A and for RK walking in Fig. 2B. Mmax responses have a latency between 5 and 11 ms; Hmax responses between 30 and 37 ms. Amplitude of each response was measured peak-to-peak from the initial negative deflection. The timing of each stimulus was within ± 10 ms of the midpoint of swing and stance in every trial (Table 1). H-reflex recruitment curves, obtained from three typical subjects, are presented for UK walking in Fig. 3A and for RK walking in Fig. 3B. No significant differences were found in the mean amplitudes of the maximal M response between midswing and midstance phases of the step cycle. This ensured that, throughout the investigation, the maximal effective stimulus strength was constant for each individual.



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Fig. 3. H-reflex recruitment curves for 3 subjects at midstance and midswing. A: unrestricted knee walking (UK). B: restricted knee walking (RK). Vertical bars indicate H wave amplitude obtained at 12% maximal M wave amplitude. For subject 4, 12% maximal M wave amplitude occurs at the peak of the H wave recruitment curve. For subject 8, 12% maximal M wave amplitude occurs during the downward slope of the H wave recruitment curve at midstance durint RK walking. For subject 15, 12% maximal M wave amplitude occurs during the rising slope of the H wave recruitment curve.

The pattern of modulation of soleus H-reflex excitability at midswing and midstance, UK walking, is set out in Table 2, row 3. At midswing during UK walking, highly significant inhibitory modulation occurred compared with midstance. Examples of H responses obtained in a typical subject at midswing and midstance for UK and RK walking are presented in the middle row of Fig. 2, A and B. The inhibition of the H-reflex at midswing (Fig. 2A) evidently did not depend on simultaneous mechanoreceptor activity arising from stretch of the quadriceps because the knee at this point was approaching maximal velocity of extension (Fig. 1A), which would correspond to a maximal rate of shortening of the quadriceps.

Similarly, in RK walking, inhibition of the H-reflex at midswing was not dependent on mechanoreceptor activity arising from rate of stretch of the quadriceps. Knee angular velocity was greatly reduced (P < 0.0001) at midswing during RK walking when compared with UK walking (Table 2, rows 1 and 2). During RK walking, instead of the rapid stretch of quadriceps associated with rapid knee flexion at toe-off, there was a knee flexion/extension oscillation (compare Fig. 1, A and B, velocity traces). This resulted in two periods of flexion, one before and one after toe-off. Group mean maximal knee flexion velocity was 100.13 ± 18.34°/s for the first and 42.07 ± 9.44°/s for the second. These values were significantly less (P < 0.0001) than those observed at toe-off in UK walking. However, the H and M responses obtained at midswing in RK walking (Fig. 2B) were unchanged from those obtained in UK walking (Fig. 2A). Consequently, the Hmax/Mmax ratios at midswing and midstance in UK and RK treadmill walking were virtually identical (Table 2, rows 3 and 4). No significant difference was seen. Knee joint velocity was uncorrelated with modulation of the H-reflex.


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This investigation showed that restricting knee movement during the swing phase of walking was not accompanied by loss of H-reflex attenuation. A highly significant reduction in the soleus Hmax/Mmax ratio at midswing compared with midstance during treadmill walking under both UK and RK conditions demonstrated the phasic modulation of reflexes. The results for UK walking are in agreement with previously published data on walking in freely moving man (Capaday and Stein 1986, 1987; Crenna and Frigo 1987; Garrett et al. 1981). Kinematic data observed for UK walking was similar to that reported by Winter (1991) and Perry (1992). The H-reflex modulation observed in the soleus during RK walking in this investigation was identical to that in UK walking. Kinematic measures of RK walking demonstrated clear and highly significant reductions in knee joint velocity at toe-off and midswing compared with UK walking. The reduction in mechanoreceptor input from the knee extensor arising from restricted knee movement was not associated with any change in phase-dependent modulation of the soleus H-reflex during walking with the knee moving freely. The longer lasting gain attenuation of the soleus H-reflex, ranging from 40 to 8,000 ms, arising from stretch of the quadriceps (Cheng et al. 1995) does not appear to contribute to the inhibition observed in this investigation because the highly significant decrease in knee angular velocity at toe-off in RK walking did not lead to an increase in H-reflex at midswing. These results suggest that, contrary to what is suggested in the reafference hypothesis, inhibition of the H-reflex during swing does not arise from somatosensory receptor discharge elicited by the movement itself. Blocking knee movement did not lead to to an increase in the H-reflex, either during swing or stance.

Brooke has further hypothesized that movement-induced attenuation can arise from somatosenory receptor discharge of the ipsilateral hip and ankle joints and the contralateral whole leg (Brooke et al. 1997). Bracing out the contribution from one joint source will not stop the contributions from the other sources. However, this group has identified somatosensory receptor discharge from the knee joint as more powerful than from the hip (Brooke et al. 1995). Despite this, no increase in the H-reflex was observed during the substantial and prolonged reduction of knee movement imposed in this trial. In fact, the repeatability of H-reflex phasic modulation in UK and RK walking was remarkable (Table 2). Reafferent modulation from stretching the hip extensor muscle remains a possibility (Brooke et al. 1993) but has yet to be demonstrated during walking in man.

It might be suggested that sensory signals from spindles and tendon organs in other muscles are increased by the bracing. Appenteng and Prochazka (1984) found a substantial increase in tendon organ firing as a result of restraining tail movement in an intact and conscious cat walking on a treadmill. However, the method they employed to restrict the tail contrasted greatly with the methods of restraint used in this investigaion. In this investigation the bracing employed was applied by means of standard walking casts of the sort routinely used in orthopedic departments to allow comfortable and safe full-weightbearing locomotion in patients with undisplaced fractures of the lower limb. Care was taken to see that the pressure exerted by the cast on the skin surface was evenly distributed both over the surface and at the edges. The resulting walking pattern, fixed knee gait, is one to which young healthy adults can readily adapt and use for purposes of daily mobility. A second period of habituation for each subject achieved steady-state RK walking before testing. Velocity was reduced in RK walking but was still within the range of normal values described by Perry (1992). The available evidence suggests that bracing does not lead to increase in tendon organ output. Walking at a slower speed with an ankle splint, which limited movement, reduced or abolished muscle activity (De Serres et al. 1998). As regards the effect of afferent input arising from change in joint position, Boorman and co-workers (1992) have shown that immobilization of the ankle joint had no effect on phasic modulation of reflexes during cycling in man. However, the purpose of the present investigation was limited to examining Brooke's hypothesis that "the occurrence of movement, as detected by stretching of muscles, is the foundation on which other sources of modulation are overlaid." The possibility that discharge from peripheral receptors other than somatosensory receptors may influence H-reflex phasic modulation during walking is quite compatible with the findings of this investigation.

The results of the present investigation provide baseline data regarding the potential reflex activity of soleus motoneurons at midswing and midstance. The Hmax/Mmax ratio at midstance, for example, indicates that the potential reflex activity of the soleus motoneurons is 0.47 ± 0.11 in UK treadmill walking and 0.48 ± 12 in RK walking. The reduction in the potential reflex activity of the soleus motoneurones at midswing (0.13 ± 0.11 for UK walking and 0.14 ± 0.12 for RK walking) is also quantified. These observations may be useful in future investigations of the input-output properties of motoneuron pools during walking in man.

Possible neural mechanisms

During walking, central influences from the spine, brain stem, and cortical centers are added to the contribution of peripheral receptor discharge. The constancy of soleus H-reflex phasic modulation during both UK and RK walking seen in this investigation indicates that the strong inhibition observed in swing does not depend on rapid knee flexion. This weakens the case for somatosensory discharge providing the foundation for the soleus H-reflex modulation during human gait. Recent work by Lavoie et al. (1997) suggests that "inhibition of the soleus H-reflex during the swing phase of walking follows the classic pattern of reciprocal inhibition between antagonist muscles and is therefore, for the most part, centrally determined." The reduction in tibialis anterior activity to 10% maximal voluntary contraction (MVC) at midswing, rising to 40% MVC in early stance (Perry 1992), indicates that simple reciprocal inhibition may not entirely account for phasic modulation. The constancy of modulation despite substantial variations in peripheral input supports central control of H-reflex inhibition. Further evidence to support central control has been provided by Chen and Wolpaw (1997), who demonstrated that integrity of the dorsal column is essential for long-term conditioning of the H-reflex in freely moving rats.

In all subjects tested, the pattern of modulation during RK walking was exactly that observed during UK walking. This suggests that the H-reflex modulation observed during UK and RK walking represents a patterned change in the excitability of spinal reflexes, which is associated with the descending motor commands producing the movement. The present data can be explained by assuming a central control of locomotion that regulates monosynaptic reflexes and maintains phasic modulation independent of changes in knee extensor mechanoreceptor input.


    ACKNOWLEDGMENTS

The authors acknowledge the assistance of G. Scully and F. Grehan of the Department of Clinical Photography, Mater Hospital, Dublin 7.


    FOOTNOTES

Address for reprint requests: M. Garrett, University College Dublin School of Physiotherapy, Mater Hospital, Eccles Street, Dublin 7, Ireland.

The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

Received 9 April 1998; accepted in final form 31 March 1999.


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