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The Journals of Gerontology Series A: Biological Sciences and Medical Sciences 55:B570-B579 (2000)
© 2000 The Gerontological Society of America

Soleus Hoffmann-Reflex Modulation During Walking in Healthy Elderly and Young Adults

Gordon R. Chalmersa and Kathleen M. Knutzena

a Department of Physical Education, Health, and Recreation, Western Washington University, Bellingham

Gordon R. Chalmers, Department of Physical Education, Health, and Recreation, MS-9067, Western Washington University, Bellingham, WA 98225-9067 E-mail: chalmers{at}cc.wwu.edu.

Jay Roberts, PhD


   Abstract
Top
 Abstract
Methods
 Results
 Discussion
 References
 
Soleus Hoffmann-reflex (H-reflex) modulation during walking was examined in 7 young and 13 elderly adults. H-reflex size was measured in 16 equal time divisions (phases) of the step cycle. In both the elderly and the young groups, the H reflex was minimal at the time of heel contact, rose to a maximum shortly after midstance, decreased rapidly as toe-off neared, then was minimal during swing. There was a significant interaction between age group and step cycle phase ( p < .05). During midstance of walking, the elderly participants had a smaller H-reflex size during two of the 16 time phases of the step cycle ( p < .05), despite no significant difference in H-reflex size between the age groups while standing. The smaller H-reflex size during the stance phase of walking may reflect changes in central reflex mechanisms that may impact stretch reflex contribution to ankle extensor neural drive and ankle stiffness in elderly persons during walking.

THE size of the soleus Hoffmann (H) reflex in young adults is modulated during the step cycle. The reflex is minimal at the time of heel contact, increases to a maximum during stance, and decreases rapidly just prior to toe-off, then is minimal during swing (1) (2) (3) (4). Phase-dependent regulation of reflex transmission is an important component of motor control, allowing afferent feedback to have differing effects in different phases of the step cycle (5). The observed changes in H-reflex size facilitate weight support and ankle extension during mid- to late stance, while allowing ankle dorsiflexion during swing and while the body moves over the foot during early to midstance (1) (2) (6).

Although H-reflex size can be influenced by a number of different mechanisms, evidence indicates that the rapid changes in the size of the soleus H reflex during the step cycle are caused by modulation of presynaptic inhibition of muscle spindle Ia-afferent fibers innervating soleus {alpha}-motor neurons (7) (8) (9) (10).

In elderly persons, there is a reduction in presynaptic inhibition of soleus and quadriceps Ia-afferent terminals under resting test conditions, compared with that observed in young adults (11) (12) (13). The control of presynaptic inhibition during isometric contractions, and when comparing different postures, is also different in young and elderly adults. During isometric contractions of the soleus, which produce increasing forces, young adults decrease the amount of presynaptic inhibition of soleus Ia afferents, although elderly subjects demonstrate no change (13). When comparing elderly with young adults in a static supine position, elderly adults demonstrate less presynaptic inhibition of Ia-afferent terminals innervating soleus {alpha}-motor neurons, although in a standing posture there is no difference between the age groups (14). Similarly, young and elderly subjects differ in control of soleus H-reflex size when comparing supine and standing postures. Young subjects depress the soleus H reflex when they stand, although, on average, elderly subjects do not (15), or they increase the soleus H reflex (16).

Under most of the resting and isometric soleus contraction conditions discussed previously, elderly subjects demonstrated a difference in the amount of presynaptic inhibition of Ia-afferent terminals innervating soleus {alpha}-motor neurons, and/or a difference in soleus H-reflex size, compared with young adults. It is unknown if elderly persons modulate soleus H-reflex size during locomotion in the manner previously described for young adults. It is possible that aging-related changes in mechanisms that control H-reflex size, which produce the age-related differences observed under resting and isometric contraction conditions, may also produce age-related differences in the modulation of the H reflex during a dynamic contraction, such as that which occurs during locomotion. Because of the hypothesized role of H-reflex modulation in contributing to locomotion, aging-associated changes in H-reflex modulation may have an influence on walking ability. Accordingly, the purpose of this study was to determine if elderly individuals demonstrate a modulation of the soleus H reflex across the step cycle similar to that observed in young subjects.


   Methods
Top
 Abstract
 Methods
Results
 Discussion
 References
 
Subjects
Seven young (four men, three women; age [mean ± SD], 22 ± 1.5 years; age range, 20–24 years) and 13 elderly subjects (four men, nine women; age, 73 ± 5.2 years; age range, 66–84 years), with no known neurological, muscular, or gait pathologies, participated in this study. The experiments were approved by the Ethics Committee on Human Experiments at Western Washington University, and all subjects gave their written informed consent prior to inclusion in the study. All of the elderly subjects lived independently in the community and were past participants in a weight-training program for elderly persons (n = 6) or were registered for a future session of the weight-training program (n = 7). All of the elderly subjects walked without the use of aids. All subjects complied with the requirements that they refrain from exercise more strenuous than walking for 24 hours prior to testing (17) and that they not consume food, stimulants, or tobacco for 2 hours prior to testing (18). Further, all subjects reported any medications they were taking, and it was verified that none took any medications that affected the muscular or nervous systems.

Data Recording and Nerve Stimulation
H-reflex data were collected and analyzed using techniques previously described (1) (19) (20). Surface electrodes were used for stimulating and recording. All measurements were made on the right leg, with electrodes placed and not removed until completion of data collection in a room isolated from visual and auditory distractions. Heel- and toe-force sensors were placed in the right shoe to record the beginning and the end of foot contact times (21). With the subject standing, skin at the electrode sites was thoroughly cleaned, and electromyographic (EMG) recording electrodes (Ag-AgCl, 10-mm diameter) were placed on the soleus, along the midline of the dorsal aspect of the leg, with the proximal electrode 1 cm distal to medial head of the gastrocnemius and at a 3-cm interelectrode distance. A 26-cm2 metal plate ground electrode was attached to the medial gastrocnemius. To stimulate the posterior tibial nerve, a 36-cm2 metal plate anode electrode was attached to the thigh just proximal to the patella, and a cathode (Ag-AgCl, 10-mm diameter) was located in the popliteal fossa. To position the cathode, low levels of stimulation were used, and the position selected was that which allowed the largest possible submaximal H waves (the second EMG response following stimulation) to be evoked without M waves (the first EMG response following stimulation, which is due to direct stimulation of {alpha}-motor neuron axons) and where higher levels of stimulation produced M and H waves with a similar shape (20). The stimulating cathode was firmly attached with tape and an elastic bandage, taking care that subject comfort and knee use was not altered.

Muscle EMG was amplified by a bipolar differential amplifier with a common mode rejection ratio of 90 dB, and a frequency band pass of 10–1000 Hz, using a gain of up to approximately 3500 times (Grass P5, West Warwick, RI). EMG signals were digitized at greater than 2000 Hz, and the foot switch signal was digitized at greater than 500 Hz using a 12-bit data acquisition card (Micro 1401, Cambridge Electronic Designs, Cambridge, UK). Both signals were analyzed online (see experimental procedures) and stored for later analysis (see postexperiment data analysis) (Spike2 software, Cambridge Electronic Designs, Cambridge, UK). Stimulus-timing pulses were digitized concurrently. Stimuli pulses (1 ms pulse duration) were provided by a Grass S48 stimulator with an SIU5 stimulus isolation unit (Grass, West Warwick, RI). During measurement of the H-reflex recruitment curve, while the subject stood quietly, a stimulus frequency of 0.2 Hz was used (20). During measurement of the H reflex, while the subject walked, the stimulus frequency was continuously and slowly manually adjusted between 0.5 and 2 Hz so that the data collected in each of the 16 step cycle phases (step cycle phases defined later) was a combination of frequencies between the limits allowed (1). Stimulation at 0.5–2 Hz, required to allow sufficient data sampling before fatigue occurs in elderly subjects during the continuous walking, will cause depression of the H reflex. This depression, however, is greatly reduced by muscle activity during the walking (22). Further, the effect of the faster stimuli rates will be reduced in the final average within a single-step cycle phase by the randomization of the intervals and the averaging of the individual responses obtained from the range of rates utilized within each of the 16 step cycle phases (1).

Experimental Procedure
The subject was instructed to stand on the treadmill belt, which was not moving, and to relax muscles in upper body. Starting at a low voltage that failed to elicit any H reflex or M waves, shock intensity was increased in increments of 3 V (nominal), up to the point where the M wave failed to increase further. A minimum of five stimuli were delivered at each stimulus intensity. The peak-to-peak height of the M and H waves following each stimulus were measured, averaged for repeated stimuli at the same strength, and an H-reflex recruitment curve was plotted ( Fig. 1). The stimulus voltage that produced the maximum H-reflex amplitude when standing was selected as the starting stimulus strength (1) (2), and the corresponding M-wave amplitude was defined as the criterion target M-wave amplitude for the data collection while the subject was walking. With both hands placed lightly on the support bar at the front of the treadmill, subjects determined their preferred walking speed that they felt they could maintain continuously for up to 1.5 hours, practiced walking until comfortable, and then data collection commenced. Soleus EMG and foot-switch data were collected for 2 minutes with no nerve stimulation. While the subject walked with nerve stimulation, online data analysis identified each heel strike (21), divided each step cycle into 16 equal time intervals (step cycle phases), and measured the peak-to-peak amplitude of each M wave and H reflex. If the M-wave amplitude was within 25% of the target M-wave size, the stimulus was assigned to the one of the 16 step cycle phases that included the time of the stimulus. The 25% tolerance value is comparable with that used in previous studies (8), and pilot studies indicated that it results in an M-wave variance similar, or smaller, to that previously accepted (e.g., 1,7,8). Typically, at a given stimulus strength only a few of the step cycle phases would accumulate a significant number of criterion-passing stimuli. In other phases of the step cycle, leg movement changed the distance between the electrode and the nerve, causing an excessively large or small effective stimulus strength, and resultant M-wave size. Based on the results observed, the stimulus strength was adjusted several times to allow data to be collected in all phases of the step cycle.



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  		Figure 1. Soleus H-reflex recruitment curve, obtained while one representative elderly subject stood, showing mean H-reflex and M-wave amplitudes for five or more stimuli at each stimulus intensity. The stimulus intensity used initially for nerve stimulation while the subject walked was the stimulation that produced the maximum H-reflex amplitude during standing. The maximum M-wave amplitude was used to normalize the H-reflex size and electromyographic activity measured during walking.

 
Postexperiment Data Analysis
For each subject, the ratio of the maximum H-reflex wave amplitude to the maximum M-wave amplitude (standing Hmax/Mmax, expressed as a percentage) was determined from the H-reflex recruitment curve obtained while the subject was standing ( Fig. 1). Using data collected while a subject walked with no nerve stimulation, heel-strike and toe-off times were determined (21), and corresponding EMG data, unperturbed by stimuli, were rectified, low-pass filtered at 100 Hz, then averaged with respect to each heel strike. The amplitude of the ensemble average EMG was then averaged over the sixth and seventh phases of the step cycle for each subject. These phases were selected because, when comparing the H-reflex size of the young and elderly groups during the step cycle, there was a significant difference between the groups in these phases (see Results section). To allow comparison of EMG signals between subjects, the mean EMG level for the sixth and seventh phases was normalized for each subject and expressed as a percentage, by dividing by the amplitude of the maximum M wave observed in the subject during quiet standing. The soleus M-wave maximum indicates the total soleus muscle activation possible by direct nerve stimulation. Normalized mean EMG amplitude over phases 6 and 7, stance duration, step cycle duration, walking speed, and standing Hmax/Mmax for each subject were then averaged for the subjects within an age group.

For the data collected when a subject walked while receiving nerve stimulation, data for a single step cycle phase from different data collection runs at different stimuli intensities were combined. For each step cycle phase, the mean peak-to-peak amplitude of the M and H waves were determined (the within-subject average for the phase). The mean H-reflex amplitude in each phase of the step cycle was then normalized by expressing it as a percentage of the maximum M-wave amplitude observed in the subject during quiet standing (2) (4). Normalizing the H-reflex amplitude allows for comparison of reflex size between subjects because individual differences in skin impedance or electrode placement will affect the amplitude of both the M and H waves similarly (20), and the ratio indicates the fraction of the soleus motor neuron pool activated by the reflex (23). The subsequent use of the term H-reflex size in this article refers to the ratio, not the absolute size, of the H wave. The standard deviation (SD) of the mean M-wave amplitude across the step cycle phases was determined as a measure of the variability in stimulus strength across the 16 phases of the step cycle within a subject.

For the subjects within each of the age groups, the within-subject mean H-reflex size was averaged, within each of the step cycle phases. In addition, the mean M-wave size, M-wave SD across the 16 step cycle phases, and the total time spent walking were averaged for subjects within each of the groups.

Statistical Analyses
Results from both genders in each age group were combined because there are no gender differences in the H reflex (24) (25), and grouping of the genders is commonly done in locomotion studies (e.g., (26),27). Differences between the young and elderly group means for standing H-reflex size, gait, stimulation, and EMG data were determined using two-tailed independent t tests.

Differences in H-reflex size during walking were identified using a two-way, between-within (age by step cycle phase) analysis of variance (ANOVA) with the Huynh-Feldt adjustment applied (28). Demonstration of a significant interaction was followed by a one-way between-subjects ANOVA to determine age-simple main effects at specific levels of the step cycle phase (29). Because of the inequality of sample sizes in the two groups, it was verified that there was no significant difference in the variance of the two groups prior to the use of a one-way ANOVA (30). To determine if differences between the groups were practically significant, the effect size was calculated for each of the step cycle phases that were significantly different in the age-simple main effect (28).

Statistical analysis was performed using SPSS-PC version 8.0 (SPSS Inc., Chicago, IL); results are reported as mean ± SD, and p values <.05 were considered significant.


   Results
Top
 Abstract
 Methods
 Results
Discussion
 References
 
Standing Reflex Size, Gait, Stimulation, and EMG Amplitude Measures
There was no significant difference between the young and elderly subjects in standing H-reflex size, walking speed, step cycle duration, percentage of the step cycle spent in stance on the right leg, M-wave size across the step cycle phases, or the number of stimulations per phase of the step cycle used in the data analysis (Table 1 ). In contrast, the total time spent walking and the variation in the strength of the stimulus delivered in the 16 different phases of the step cycle (the latter reflected by the M-wave SD) were significantly less, and the normalized mean EMG amplitude over step cycle phases 6 and 7 were significantly greater in the elderly, compared with the young subjects (Table 1 ).


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  		Table 1. Mean Values of Reflex, Gait, Stimulation, and Electromyographic (EMG) Measures of Young and Elderly Subjects

 
Results From a Single Representative Elderly Subject
The H-reflex and M-wave results from a single elderly subject are illustrated in Fig. 2. At least 12 stimuli (mean = 29) were averaged to produce each trace, to show the mean M-wave and H-reflex amplitude within one 75-millisecond duration phase of the step cycle. EMG data in Fig. 2, and for all measurements of M- and H-wave amplitudes, were not rectified to allow for peak-to-peak amplitude measurements. The start of the step cycle (top trace) coincides with heel contact, and the end of the step cycle (bottom trace) coincides with the moment before heel contact occurs ( Fig. 2). Note that although the stimulus strength was relatively constant, as reflected by the small variation in M-wave amplitude (SD = 0.16 mV for this subject), the H-reflex size varied greatly during the step cycle. The H-reflex amplitude increased progressively during stance, reaching a peak shortly after midstance, and decreased rapidly as toe-off approached, then was negligible during most of swing, increasing slightly as the next heel contact approached.



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  		Figure 2. Amplitude of the soleus M wave and H reflex in the 16 phases of the step cycle for a single representative elderly subject. Each trace is an average of responses to at least 12 stimuli within a step cycle phase. The start of the first phase of the step cycle (top trace) coincided with heel contact. Lower traces are responses in subsequently occurring 75-ms phases. Toe-off occurred during the tenth phase. Note that the H-reflex amplitude increased progressively during stance, then was absent during swing, while the stimulus strength, reflected by the M-wave size, showed only small variation. Electromyographic data in this figure, and for all measurements of M- and H-wave amplitudes, were not rectified to allow peak-to-peak amplitude measurements to be made. HC = heel contact; TO = toe-off.

 
The H-reflex and M-wave amplitudes for each step cycle phase shown in Fig. 2 are summarized in a single graph, along with the maximum M-wave amplitude observed in the subject during quiet standing ( Fig. 3). The normalized H-reflex size ( Fig. 3), obtained by dividing the absolute H-reflex amplitude in each phase by the maximum M-wave amplitude during standing (values in Fig. 3), allowed subsequent comparisons of H-reflex size between subjects. Rectified soleus EMG during the step cycle without nerve stimulation, averaged over 99 steps for the subject illustrated, was observed in this subject to covary with the H-reflex modulation ( Fig. 3).



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  		Figure 3. Amplitude of the soleus M wave, H reflex, and electromyographic (EMG) activity in the 16 phases of the step cycle for the single representative elderly subject whose data is displayed in Fig. 1 and Fig. 2. A, The soleus M-wave and H-reflex amplitudes from Fig. 2 are summarized in a single graph. The broken line shows the maximum M wave in the subject when a standing H-reflex recruitment curve was calculated prior to walking. B, The H-reflex amplitude for each phase of the step cycle is expressed as a percentage of the maximum M wave obtained during standing, using the absolute values in A. This curve, for each individual, was averaged within groups to produce Fig. 4. C, The average rectified soleus EMG activity for 99 steps when no nerve stimulation was being delivered.

 
H-Reflex Modulation in Young and Elderly Subjects
The pattern of H-reflex modulation, M-wave consistency, and soleus EMG modulation illustrated for the single elderly subject in Fig. 2 and Fig. 3 was similar to that seen in all elderly and young subjects. For each phase of the step cycle, the mean normalized H-reflex size of all subjects in a group is shown in Fig. 4 (i.e., the combination of Fig. 3 data across subjects within groups). The overall pattern of H-reflex modulation through the step cycle was similar for the young and elderly groups. There was a significant interaction between age and step cycle phase ( p < .05, power = 0.73). The H-reflex size in the elderly subjects was significantly smaller than that in the young subjects in step cycle phases 6 and 7 ( p < .05). The effect sizes for phases 6 and 7 were 0.86 and 1.00, respectively.



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  		Figure 4. Mean normalized H-reflex size for the young and elderly subjects in each of the 16 phases of the step cycle. Note the similarity in the overall shape of the curves, but the difference in reflex size in phases 6 and 7. Bars indicate 1 standard deviation from the mean. *Significant difference between young and elderly subjects within a single phase of the step cycle, p < .05.

 

   Discussion
Top
 Abstract
 Methods
 Results
 Discussion
References
 
The soleus H reflex, which bypasses the fusimotor system, is a measure of the efficacy of synaptic transmission from muscle spindle Ia-afferent terminals to soleus {alpha}-motor neurons and the intrinsic excitability of the {alpha}-motor neurons (19). Observations made on H-reflex modulation during locomotion likely indicate stretch reflex modulation because, in humans, the soleus stretch and H reflexes are modulated in a very similar pattern through the step cycle (31) (32) (33) (34). Recently, although noting that H-reflex data aid in the understanding of modulation of presynaptic inhibition of Ia afferents, caution has been suggested when extrapolating from H-reflex data to stretch reflex function because H and stretch reflexes are not equally affected by test stimuli producing presynaptic inhibition (35).

The present results are likely applicable to movement control during overland walking because, in young adults, treadmill walking closely approximates overland locomotion based on EMG patterns, kinematic results, and self-selected speeds (36) (37). The elderly subjects examined in the present study were all healthy, living independently, and had physician clearance to start a weight-training program, or were active weight trainers. All were capable walkers, able to walk continuously on the level for the time required during the experiment (average = 32 minutes, maximum = 59 minutes) without demonstrating or reporting fatigue. Most of the elderly subjects were relatively young, based on the classification system defined by Seccombe and Ishii-Kuntz (38), nine were young-old (65–74 years), and four were old (75–84 years). The results, therefore, may not be applicable to elderly individuals who are older or less capable walkers.

Standing Reflex Size, Gait, Stimulation, and EMG Measures
The size of the H reflex during standing was the same in the young and elderly subjects, which is consistent with previous reports of little (15) or no (16) age difference in this measure. The walking speed of the subjects was slower than that generally reported for similar age groups [e.g., young adults: 0.81–1.4 m/s (39) (40) (41); elderly individuals, mean ages 68–74 years: 0.70–1.13 m/s (39) (42) (43)]. The present subjects may have selected to walk at a speed slightly slower than that generally observed on a 5- to 10-m walkway because they were instructed to select a speed that could be maintained for up to 1.5 hours without interruption. Data collection was more rapid in the elderly than in the young subjects because, in the elderly subjects, a single voltage setting often produced M waves of acceptable sizes in a greater number of adjacent step cycle phases, resulting in fewer voltage levels being needed. The reason for this difference is unknown.

The variability in the stimuli strength across the step cycle phases in the young subjects was similar to representative values previously reported for young adults when the same technique was utilized; SD = 0.24 mV in the present study, compared with 0.31 mV (1) and 0.26 mV (7). In the elderly subjects, the variation in stimuli strength across the step cycle phases was even less, being half that observed in the young subjects. The procedure used involved eliminating from data analysis stimuli outside of the tolerance range. It was, therefore, not determined if there were any differences between the groups in the full range of responses to all of the stimuli. Nervous system, gait, or other differences between the two age groups may potentially have produced differences in the responses to the stimuli applied that are masked when only the stimuli within the 25% tolerance range are examined. Any such fundamental differences between the groups could, therefore, confound the results.

The soleus ensemble average EMG profile during the step cycle had a similar shape in both young and elderly adults and was similar to that previously reported for young adults (27) (36). Soleus H-reflex modulation, although paralleling EMG modulation, is not dependent only on motor neuron excitation level. H-reflex size can vary at the same EMG level when different motor tasks are compared within or across individuals (3) (4) (7) (8) (10).

Possible Causes for a Smaller H-Reflex Size During Stance in the Elderly Subjects
Could reciprocal inhibition contribute to the smaller H reflex observed in step phases 6 and 7 in the elderly subjects? In most people, the soleus H reflex decreases approximately linearly with increasing tonic voluntary tibialis anterior (TA) contraction (44) (45). Task-dependent reciprocal inhibition is due to disynaptic Ia inhibition of soleus motor neurons, as well as other neural mechanisms including presynaptic inhibition of the Ia afferents that mediate the H reflex (44) (45) (46). During walking, however, TA activity does not appear to be important for control of the size of the soleus H reflex. In most individuals, elimination of TA activity during swing and very early stance, when the TA is normally active, has little to no affect on concurrent soleus H-reflex depression (10). Similarly, during the first two steps while walking, there is no correlation between TA EMG and the size of the soleus H reflex (47). During mid- to late stance of walking, when the H reflex was smaller in the elderly compared with young subjects, there is little to no activity in the TA (27) (48) and reciprocal inhibition pathways potentially operating during the walking act to reduce soleus EMG (48), which is contrary to the elevated EMG observed in the elderly subjects during stance. Accordingly, it appears unlikely that the smaller H reflex observed during stance in the elderly subjects was due to reciprocal inhibition.

The size of the soleus H reflex is also influenced by limb movement while walking. Active or passive locomotor-like movement of either the knee or hip can inhibit the soleus H reflex, with the degree of inhibition increasing with the velocity of movement (49) (50). Spindle discharge from extensor muscles of the knee and hip, increasing presynaptic inhibition in the soleus H-reflex pathway, is believed to be the basis for the reflex attenuation (49) (51). Knee and hip peak angular velocity is reduced in the elderly, compared with the young adults (mean ages, 70 and 21 years), during the stance phase of walking at 1.5 m per second (T. Hortobágyi and P. DeVita, written communication, May 1999). Assuming that speed of limb movement and presynaptic inhibition are positively related in elderly persons, then slower limb movements in elderly persons, even at the same walking speed, would be expected to increase the H reflex, which is contrary to the smaller H-reflex size observed in the present study's elderly subjects. In addition, although there was no significant difference in mean walking speed between the two groups in the present study, there was a tendency for the elderly subjects to walk more slowly ( p = .06), which would be expected to further reduce limb-speed–dependent presynaptic inhibition and increase H-reflex size. Accordingly, it appears that factors other than speed of movement likely predominate to reduce the reflex size during stance in the elderly subjects.

Additional changes with aging that may contribute to the smaller H-reflex size during stance have been identified in cats. In older versus young cats, Ia-induced monosynaptic excitatory postsynaptic potentials in medial gastrocnemius {alpha}-motor neurons are less efficient in promoting motor neuron discharge because of a slower time course (52). Changes in the aged cats were attributed to a combination of altered motor neuron membrane properties and possible impairments in nerve impulse invasion into synaptic terminals and/or neurotransmitter release (52). If such changes occur in aged humans, they may contribute to a decreased reflex size that would be most obvious during stance when reflex size is at its highest level in the step cycle. Such anatomical changes, however, would be expected to also depress the H reflex during quiet standing in the elderly subjects, which was not observed.

The smaller stance phase H-reflex size in the elderly subjects was not a consequence of the stimulus rate used during walking. Some degree of H-reflex depression will occur at the rates used, but this will occur in both the young and elderly groups. Further, H-reflex depression due to a fast stimulus rate is reduced when the muscle is active (22), as it is during most of the stance phase, minimizing rate effects on H-reflex size in the phases where a significant difference was observed between the groups.

In summary, factors discussed do not adequately explain the smaller stance phase H-reflex size in the elderly subjects. Accordingly, other mechanisms that can influence H-reflex size and that can potentially change with aging must be considered. For example, aging-related changes in Renshaw cell activity or effectiveness, or changes in the availability of the neuromodulator serotonin (19), could change {alpha}-motor neuron excitability, or changes in descending control of presynaptic inhibition should be considered.

Potential Consequences of a Smaller H-Reflex Size During Stance in Elderly Persons
The effect size calculation indicated that the effect of age on reflex size was large in phases 6 and 7 (28). The smaller normalized reflex size in the elderly subjects means that the reflex activated a smaller percentage of the motor pool, compared with young adults. In contrast, during quiet standing there was no difference in H-reflex size between the two age groups, even though for each subject the same stimulus strength was used while standing and walking (within the tolerance permitted during walking). For elderly people, a smaller reflex size during stance may impair a stretch reflex contribution to ankle extensor neural drive and stiffness during walking.

Spindle afferents fire at their highest rates during passive muscle stretch in the step cycle (53). During the walking step cycle, the soleus muscle lengthens for most of the first half of the stance phase (1) (2). A large H reflex in mid- to late stance would allow Ia-afferent feedback to maximally contribute to weight support and ankle extension (plantar flexion) during this portion of the step cycle (1) (6) (7) (33). It has been estimated that the stretch reflex pathway may be responsible for 30% to 60% of soleus muscle activation during the first half of stance (34), with technical limitations preventing an equivalent estimate in the second half of stance. Similarly, Stein and Kearney (54) determined that small stretches to the ankle extensors can produce substantial torques, up to 23% of the torque observed with a maximum voluntary contraction (MVC), depending on factors such as ankle angle and background torque. Reflex-based muscle activation can become mechanically effective even within the short time of stance. The onset of the soleus stretch reflex-elicited EMG occurs at 33–40 ms poststretch in young adults (54) (55), and the subsequent electromechanical delay takes up to 200 ms (54) (55) (56). A time of 240 ms encompasses 3.2 of the 16 step cycle phases in the elderly subject represented in Fig. 3. With aging producing a 16% slowing of tibial nerve conduction velocity (57) and a 30% slowing of muscle contraction time (58), the total time from a muscle stretch to reflex generation of force in an average elderly subject would be approximately 306 ms, or four of the 16 step cycle phases. Clearly, even in elderly subjects, there would be sufficient time for ankle extensor muscle stretch in the first half of stance to assist in force production as toe-off approaches. In elderly individuals, a stretch reflex contribution to ankle extensor muscle neural drive and mechanical action in mid- to late stance may be reduced, compared with younger subjects, because of changes in common mechanisms that underlie both the stretch and H reflexes, indicated here by the smaller H-reflex size in the elderly subjects.

The reduced reflex size in elderly individuals, potentially decreasing reflex muscle activation, may influence ankle joint stiffness. Reflex-mediated stiffness can play a significant role in the ankle extensors of humans, peaking at approximately 200 ms after muscle stretch (56). The contribution of stretch reflexes to muscle stiffness, however, decreases with an increasing contraction level. Stretch reflex-mediated stiffness 200 ms poststretch comprises approximately 60% and 10% of the total ankle extensor muscle stiffness during contractions producing torques of 10 and 70 Newton meters (Nm), respectively, the latter being approximately 60% of the torque measured during a MVC (56). If the ankle extensor torque used during walking is less than 60% of that produced during an MVC, then the stretch reflex may contribute significantly (i.e., >10%) to total ankle extensor stiffness. Under such a condition, the central mechanisms that produce a smaller H reflex during stance in elderly persons may similarly impair a stretch reflex contribution to ankle stiffness. An age-related decrease in reflex contribution to ankle extensor stiffness is supported by a study in rats. Although stiffness of the ankle extensors during passive ankle dorsiflexion is the same in young and old rats, muscle stretch reflexes played a role in extensor stiffness only in the young rats (59). While walking at 1.5 m per second, elderly humans have a significantly lower ankle stiffness during stance, compared with young adults (elderly, 4.0 Nm/degree; young, 4.9 Nm/degree; T. Hortobágyi and P. DeVita, written communication, May 1999). Some of this difference between the age groups could be related to an elderly person's decreased capacity for muscle stretch reflexes to contribute to ankle extensor muscle stiffness.

A potential benefit for a reduced soleus H-reflex size during certain motor tasks has been hypothesized. The smaller H-reflex size during stance while walking, in elderly compared with young subjects, is similar to the smaller H reflex during stance when running is compared with walking (7) or beam walking is compared with treadmill walking (3) in young adults. Running and beam walking were associated with a lower gain in the H-reflex path, compared with regular walking (3) (7). Similarly, young adults decrease the gain of the soleus H reflex when shifting from sitting, to standing with support, to standing without support (60). Combined, these data in young adults illustrate that the gain of the soleus H reflex is reduced when postural instability is increased. In the elderly subjects in the present study, the smaller H-reflex size during stance phases 6 and 7, when EMG was higher, indicates a lower gain in the H-reflex pathway, compared with young walkers. This is similar to the observation that elderly subjects have a lower soleus H-reflex gain when standing, compared with young adults (16). The lower gain of the H reflex in young subjects while performing tasks with greater instability was hypothesized to prevent excessive reflex activation of soleus motor neurons and possible instability in the stretch reflex feedback loop, while allowing high levels of afferent information to continue to supraspinal areas (3) (7) (60). Motor control during the stance phase of walking in elderly individuals may be similarly optimized by a reduced soleus H reflex.


   Acknowledgments
 
The authors thank Dr. P. Bawa for comments made during preparation of the manuscript.

Received July 8, 1999

Accepted May 8, 2000


   References
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 Abstract
 Methods
 Results
 Discussion
 References
 

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