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1 Motor Control Laboratory, Department of Exercise and Sport Science, University of North Carolina, Chapel Hill, North Carolina 27599; and 2 Motor Control Laboratory, Department of Kinesiology, and Program in Neural Science, Indiana University, Bloomington, Indiana 47405
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ABSTRACT |
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 TOP
 ABSTRACT
 INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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The purpose of this study was to
determine the ability of the elderly central nervous system to modulate
spinal reflex output to functionally decrease a spinally induced
balance perturbation. In this case, the soleus H reflex was used as the
source of perturbation. Therefore, decreasing (down training) of the
soleus H reflex was necessary to counteract this perturbation and to
better maintain postural control. In addition to assessing the effect
of this perturbation on the H reflex, static postural stability was
measured to evaluate possible functional effects. Ten healthy young
subjects (age: 27.0 ± 4.6 yr) and 10 healthy elderly subjects
(age: 71.4 ± 5.1 yr) participated in this study. Subjects
underwent balance perturbation on 2 consecutive days. On day
1 of perturbation, significant down training of the soleus H
reflex was demonstrated in both young (
20.4%) and elderly (18.7%)
subjects. On day 2 of perturbation, significant down
training of the soleus H reflex was again demonstrated in both young
(24.6%) and elderly (21.0%) subjects. Analysis of static
stability after the 2 days of balance perturbation revealed a
significant 10.1% decrease in the area of sway in elderly subjects. In
conclusion, this study demonstrated that healthy, elderly subjects
compared with young subjects were equally capable of down training the
soleus H reflex in response to a balance perturbation. Furthermore, the
improvement in static stability through balance training may provide
further evidence that balance can be retrained and rehabilitated in
subjects with decreased reflex function.
postural control; reflex modulation; aging
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INTRODUCTION |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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REFLEX CIRCUITRY PROVIDES
PATTERNS of rapid response to specific internal and external
stimuli. Maintenance of postural stability, for example, is partially
due to the response of the spinal-stretch reflex to involuntary stretch
imposed on postural muscles by gravity-induced sway (1).
This largely monosynaptic circuit allows rapid response to counteract
the effects of external stimuli. Furthermore, the stretch reflex is the
only reflex that monosynaptically provides information from the
periphery (via Ia afferents) to the 
-motoneuron. This provides a
powerful mechanism for postural control and allows for a rapid response
to postural perturbation.
With respect to aging, the integrity of the spinal-stretch reflex system has been demonstrated to significantly degrade over time (9). This degradation and its functional effect on reflex output have been examined by using H-reflex protocols. For example, when young subjects change body positions from supine to standing, a decrease in the soleus maximal H reflex (Hmax)-to-maximal motor response (Mmax) ratio (H/M) is observed (8). This decrease in H-reflex amplitude has been explained by changes in presynaptic inhibition that decrease the afferent input to the soleus motoneuron pool and allow for more efficient control (9). Koceja et al. (6) demonstrated that these changes were not observed in elderly subjects. In elderly subjects, the change in position from supine to standing was demonstrated to have no effect on H/M. Likewise, measures of presynaptic inhibition have demonstrated that elderly subjects have greater levels of afferent inhibition than young subjects (7, 8a).
Similar age-related decreases in the ability of the central nervous system (CNS) to modulate reflex output have been observed when measuring the input/output relationships or gain of the H reflex over a continuum of voluntarily initiated background electromyogram (EMG) levels. For example, Angulo-Kinzler et al. (2) observed that elderly subjects demonstrated less reflex modulation both from prone to standing as well as throughout a functional range of voluntary contraction than that observed in young subjects. Given the changes observed in presynaptic inhibition with aging, the decrease in ability to modulate reflex output may indicate a decrease in the ability of the CNS to efficiently respond to postural corrections sent by the peripheral nervous system. This could partially explain the increases in sway area and decreases in stability observed with aging. With the potential effect this inefficiency could have on the incidence of falls in the elderly, it is important to determine whether these age-related changes are a result of permanent or temporary changes within the CNS. If these age-related changes are permanent, then therapeutic interventions should focus on other mechanisms of balance. However, if they are temporary, then rehabilitation can attempt to impact the efficiency of the reflex response that serves as the first line of defense to falling. Currently, there is no evidence to provide an answer to that question; however, there is a protocol that can be used to address this issue.
Trimble and Koceja (10) assessed the effect of balance perturbation on the soleus H reflex of young subjects. This research supplemented the work of Wolpaw and O'Keefe (14) in macaques and Evatt et al. (3) in humans. Trimble and Koceja (10) used the soleus H reflex to perturb the balance of subjects maintaining balance on a platform that allowed movement in only the anterior-posterior direction and demonstrated a 26.2% decrease in the soleus H-reflex amplitude after only 49 perturbation trials. This demonstration of reflex down training is important for at least two reasons. First, it supports that the reflex is very sensitive to the balance needs of the body and can rapidly change to accommodate these functional needs. Second, the success of this methodology provides a protocol that can be used to compare the ability to down train the reflex system in other populations (e.g., elderly) and possibly in other conditions (e.g., task complexity).
The purpose of this study was to determine the differences in functional spinal down training in young and elderly subjects using a balance perturbation task to induce down training of the soleus H reflex. Furthermore, the effect of this training on a measure of static balance was assessed.
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METHODS |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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Subjects. Ten young subjects (5 men and 5 women) between the ages of 21 and 33 yr (age: 27.0 ± 4.6 yr; height: 172.5 ± 9.7 cm; weight: 74.0 ± 9.5 kg) and 10 elderly subjects (5 men and 5 women) over the age of 65 yr (age: 71.4 ± 5.1 yr; height: 167.6 ± 8.6 cm; weight: 68.6 ± 13.1 kg) were recruited. Only those individuals who were free from neurological disease and had no serious orthopedic injuries or dysfunctions were asked to participate in this project. Before being tested, each subject read and signed an informed consent form, as approved by the Human Subjects Committee of Indiana University.
Experimental procedures. In this 3-day study, all subjects were initially evaluated on the first day for their H/M and static balance characteristics. On the second day, subjects underwent balance perturbation to down train the H reflex. On the final day of testing, subjects initially performed an abbreviated perturbation session to determine the rate of down training reacquisition. After this, all subjects were again evaluated on H/M and static balance. A bilateral perturbation stimulus was used to ensure that the perturbation itself was in the anterior-posterior direction. Bilateral nerve stimulation avoids the creation of a rotational movement about the longitudinal axis of the subject.
Balance platform. The central piece of equipment that was used in this experiment was a custom-made balance platform. The balance platform had two aluminum bars mounted on the bottom of a 3-cm-thick, 47 × 50-cm rectangular platform of sturdy Formica. A subject standing on this platform had a reduced base of support in the sagittal plane. This base of support could be adjusted by varying the distance between the metal bars, thus providing a base of support range from 3 to 12 cm in the sagittal plane. The balance platform was free to rotate in the sagittal plane with an arc of motion of ±15°.
Subjects were instructed to stand on the balance platform in a relaxed balanced position, eyes forward and hands on hips, with the platform parallel to the floor. The flat base of the aluminum bars induced all subjects to a balanced position parallel to the floor when the center of pressure was centered over the platform's adjusted base of support. The base of support was adjusted to a point where the standardized perturbation stimulus would cause enough plantar flexion to tilt the platform out of balance by between 5 and 10°. This was subjectively determined to be enough perturbation to make down training of the H reflex functionally capable of enhancing recovery without the use of additional biomechanical strategies (i.e., hip rotation). If the perturbation was too extreme, then the spinal stretch reflex would probably not be the first point of postural correction.EMG. The raw and full-wave rectified and averaged EMG signals from the soleus and tibialis anterior muscles were monitored bilaterally. These EMG signals were obtained by using four actively amplified bipolar surface electrodes (Therapeutics Unlimited) with an intraelectrode distance of 2 cm. Each electrode was positioned over the test muscles by using standardized placements (15).
EMG recorded by the electrodes was routed through an EMG mainframe (Therapeutics Unlimited) that contained preamplifiers (gain = 1,000) to band pass and filter the signal (40-4,000 Hz). The output of the EMG mainframe was connected to a computer via an analog-to-digital converter (Data Translation). The placement of the soleus EMG electrode was ~2 cm proximal to the palpable musculotendinous junction of the triceps surae and the Achilles tendon. For the tibialis anterior, electrodes were placed on the proximal one-third of the muscle. A common reference electrode was placed over the lateral malleolus of the right leg.Soleus H-reflex setup. During balance training, bilateral soleus H reflexes were elicited with a 0.80-cm-diameter stimulating electrode placed in the popliteal fossa of both legs. A 4-cm-diameter dispersal pad was placed on the anterior aspect of each knee just above the patella. An electrical stimulator (Grass S8800) was used to generate a 1-ms-duration square-wave pulse. This pulse was routed through a stimulus isolation unit (Grass SIU-5) followed by a constant current unit (Grass CCU-1).
Initial measurements of Hmax amplitude and Mmax were recorded during mapping of the H reflex and motor response recruitment curve for each subject in both supine and standing positions. The standing measurements were used to standardize the stimulus intensity of balance perturbation to a peak-to-peak H reflex amplitude equal to ~35% of the peak-to-peak Mmax amplitude for each subject.Static balance testing. Static balance was measured with a force platform (Kistler) by using custom software and a sampling rate of 50 Hz. Subjects were asked to stand comfortably with their hands on their hips while focusing on an eye-level target. Each subject completed six 15-s trials under an eyes-open condition. The area within which the center of pressure remained was calculated to determine each subject's total area of sway (mm2/s).
Soleus H-reflex down training. On the first day of the study, each subject was introduced to the balance platform and was given an opportunity to experience the perturbation protocol. An abbreviated session of balance perturbation was used to allow initial determination of appropriate base of support settings, and to allow the subject to become comfortable with the protocol. This served to reduce or eliminate any learning effects before the beginning of testing on the second day. Furthermore, Trimble and Koceja (11) demonstrated that background soleus EMG levels decreased across 3 days of balance perturbation. This decrease may have been due to a learning effect and, in itself, may have lowered the amplitude of the H reflex. Therefore, the balance perturbation on the first day served as an attempt to achieve more consistent levels of background EMG throughout the rest of the study.
The second day of the study served the primary role in assessing the ability of young and elderly subjects to modulate the soleus H reflex and will be referred to as day 1 of balance perturbation. With the use of information gathered from the first day, the platform's base of support was adjusted to allow the platform to rotate enough to cause a significant balance perturbation in response to the H reflex. In other words, when the subject received bilateral H reflexes, the resultant plantar flexion would cause the subject to momentarily lose balance. However, the perturbation was not large enough to cause the subject to fall. Day 1 of balance perturbation was comprised of seven blocks of seven bilateral soleus H-reflex perturbation trials while a subject was standing on the balance platform. These seven blocks of perturbation trials were preceded and followed by a block of seven control H-reflex trials. Control H reflexes were gathered while a subject was standing on the balance platform while it was stabilized (locked to prevent sagittal rotation). Each block of seven trials was separated by a short rest interval to prevent fatigue. Intertrial intervals were randomized between 15 and 30 s to reduce anticipation. The final day of the study was used to assess the rate of down training during an abbreviated perturbation session and will be referred to as day 2 of balance perturbation. In this case, four blocks of seven perturbation trials were used to elicit the initiation of H reflex down training. These perturbation blocks were preceded and followed by seven control H-reflex measurements while the balance platform was in the fixed position. After this perturbation session, measures of static balance were collected. The abbreviated training session was an attempt to determine whether subjects down trained the H reflex more quickly after the initial perturbation session.Analysis. The following designs were used to assess differences in the dependent variables between and within groups. To assess differences in H/M, a 2 × 2 × 2 (group × position × day) split-plot ANOVA design was used. The static balance results were examined with a 2 × 2 (group × day) split-plot ANOVA on the dependent variable sway area.
The effect of balance training on the soleus H reflex was assessed with a 2 × 2 × 2 × 2 (group × block × day × leg) split-plot ANOVA. This design was also used to verify the stability of soleus and tibialis anterior background EMG as well as stimulus intensity. In some cases, to evaluate experimentally important comparisons, simple main effects as described by Keppel (5) were performed. Because it was essential that any down training of the soleus H reflex was independent of changes in background soleus EMG, a Pearson product-moment correlation was used to assess the relationship between these two variables during the entire experiment.| |
RESULTS |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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Down training of the soleus H reflex. On day 1 of balance perturbation, significant down training of the soleus H reflex was demonstrated in both young [F(8,144) = 2.23, P < 0.05] and elderly subjects [F(8,144) = 2.27, P < 0.05]. In the final control block, young subjects demonstrated a 20.4% decrease (35.7-28.4% Mmax) in the peak-to-peak amplitude of the soleus H reflex from the initial control block. Elderly subjects demonstrated an 18.7% decrease (32.1-26.1% Mmax).
On day 2 of balance perturbation, significant down training of the soleus H reflex was demonstrated again in both young [F(5,90) = 7.57, P < 0.05] and elderly subjects [F(5,90) = 4.74, P < 0.05]. In the final control block, young subjects demonstrated a 24.6% decrease (39.1-29.5% Mmax) in the soleus H reflex from the initial control block. Elderly subjects demonstrated a 21.0% decrease (32.9-26.0% Mmax). These results are illustrated in Fig. 1.
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Background EMG levels.
Statistical analysis of the background EMG of the soleus and tibialis
anterior was performed for both days to ensure that the results were
not affected by changes in muscle activity. Analyses revealed no
significant background EMG differences in either the soleus or tibialis
anterior between the initial and final control blocks for either group
on either day (Table 1). Inspection of posttest EMG on each day reveals that background soleus and tibialis anterior activity levels were almost identical to pretest values in
both young and elderly subjects, whereas the soleus H reflex was
depressed in both groups. This interpretation supports the notion that
soleus H-reflex changes were independent of background EMG levels.
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0.156. Each
of these correlations accounts for <5% of the soleus H reflex variance.
Comparison of static balance characteristics between young
and elderly groups.
Analysis of static sway after balance training revealed a significant
decrease [F(1,18) = 6.52, P < 0.05] in the area of sway in elderly subjects
from pretest (42.0 mm2/s) to posttest (37.8 mm2/s). No changes in the static sway areas from pretest
(25.1 mm2/s) to posttest (23.9 mm2/s) were
observed in young subjects [F(1,18) = 0.54, P > 0.05]. These observations are illustrated
in Fig. 2. Overall, young subjects demonstrated a significantly [F(1,18) = 6.13, P < 0.05] smaller static sway area (24.5 mm2/s) compared with elderly subjects (39.9 mm2/s).
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Comparison of H/M modulation from supine to standing of young and elderly subjects. A significant group × position interaction [F(1,18) = 5.77, P < 0.05] was initially observed in the overall ANOVA of H/M data. Simple main effects as described by Keppel (5) were used to break down the interaction. This analysis revealed that young subjects significantly decreased H/M from supine to standing positions [F(1,18) = 8.97, P < 0.05], whereas elderly subjects did not significantly modulate the ratio [F(1,18) = 0.16, P > 0.05]. Finally, in the overall ANOVA, a significant day effect was revealed with a first day mean ratio of 53.5% and a final day mean ratio of 49.7% [F(1,18) = 6.64, P < 0.05].
Further evaluation of the data by using a simple-simple main effects design allowed a clearer view of the group dynamics. Young subjects significantly decreased the H/M by 8.7% from supine (66.5%) to standing (60.7%) positions on the first day of testing [F(1,36) = 5.58, P < 0.05]. On the final day of testing, young subjects significantly decreased H/M by 9.6% from supine (63.3%) to standing (57.2%) positions [F(1,36) = 6.34, P < 0.05]. Elderly subjects did not significantly modulate H/M during either the pretest [F(1,36) = 0.07, P > 0.05] or the posttest [F(1,36) = 0.15, P > 0.05]. Elderly subjects increased H/M 1.6% from supine (43.1%) to standing (43.8%) positions on the first day of testing. On the final day of testing, elderly subjects increased H/M 2.6% from supine (38.6%) to standing (39.6%) positions. These results are illustrated in Fig. 3. Power and effect size analyses on the group × day interaction revealed both low power (0.062) and effect size (0.005), which confirmed that sample size was not a factor in this case.
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Methodological considerations.
It is important, at this point, to determine that the down training of
the soleus H reflex was due primarily to changes in Ia -motoneuron
efficacy and not to changes in background soleus and tibialis anterior
EMG. Two methods were employed to test these relationships. First,
Pearson product-moment correlations of the soleus H reflex with
background soleus and tibialis anterior EMG were calculated in an
effort to determine any confounding associations. The resulting
correlations demonstrated only a weak association among the measures.
This supports the assumption that the soleus H reflex modulation was
largely independent of changes in background EMG activity of the soleus
and tibialis anterior.
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DISCUSSION |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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This study demonstrated that healthy elderly subjects were equally capable of down training the soleus H reflex in response to a balance task compared with young subjects. After the first day of balance training, elderly subjects achieved nearly the same magnitude of down training as young subjects. Furthermore, on the second day of training, both groups demonstrated the ability of quickly reestablishing a significant depression of the soleus H reflex during an abbreviated balance-training session. The ability of elderly subjects to successfully down train the soleus H reflex demonstrated that the potential to functionally modulate reflex output persists despite the effects of aging.
The result of this study provides a human model parallel to the classic work of Wolpaw and O'Keefe (14) in which monkeys were operantly trained to up- or down train the spinal stretch reflex. Our results demonstrate the same rapid initial modulation, referred to as phase I changes in that research. The ability of elderly subjects to successfully initiate phase I changes in reflex output may be very important in regard to intervention or rehabilitation training programs aimed at improving spinal cord function.
In addition to the changes observed in H-reflex amplitude, elderly subjects also demonstrated a significant 10.1% decrease in the area of static sway after balance training. This improvement in static stability through balance training may provide further evidence that balance can be retrained and rehabilitated in subjects with a decreased ability to modulate reflex output.
Effect of soleus H-reflex down training. With balance training, elderly subjects were capable of down training the soleus H reflex with a rate and magnitude similar to young subjects. It is important to remember that, even in the active and healthy sample of elderly subjects studied, there were dramatic differences in many of the dependent variables, such as postural stability and H/M. These measures often provide insight into the functional status of the postural reflex system of elderly subjects. For example, the modulation of H/M from supine to standing positions has been correlated to the magnitude of sway area in elderly subjects (6). Therefore, the role that this modulation plays may relate to the ability of the body to functionally adapt to the environment. Previous studies have demonstrated that elderly subjects have a general lack of H/M modulation from supine to standing compared with young subjects (6). This phenomenon is very characteristic of elderly subjects and points to a fundamental difference in reflex function between young and elderly subjects that seems to have an impact on the ability of elderly subjects to maintain postural stability.
The demonstration that the CNS of elderly subjects retains the ability to functionally modulate spinal stretch reflex amplitude provides evidence that an intervention or rehabilitation program aimed at this mechanism of postural control may be feasible. Without evidence of this adaptability, retraining programs impacting on the circuitry of the spinal cord might have to be discarded with the focus moving to the learning of more cognitive balance strategies. Instead, the fact that elderly subjects can down train the H reflex provides support for the use of reflex training to increase the dynamic range of reflex modulation. In the long term, maintaining a more dynamic reflex modulation profile may prevent some of the loss of balance ability due to the inevitable effects of aging on the central and peripheral components of postural control.Effect of H-reflex down training on postural control. The difference in static balance demonstrated between young and elderly subjects supports previous research in the area (4, 6). Analysis of the effect of H-reflex down training on static balance revealed a significant decrease in the area of sway in elderly subjects from pretest to posttest. No changes in the static sway areas were observed in young subjects. This lack of change in young subjects was most likely due to a floor effect. There is certainly a minimum sway area that can be attained during free standing, and healthy young subjects are probably very close to this minimum. Therefore, any improvements in static balance would be very hard to detect compared with that of elderly subjects.
It may seem counterintuitive that a decrease in reflex output could lead to an increase in static balance performance. However, the dynamic perturbations may, for example, have the beneficial effect of increasing muscle spindle sensitivity through changes in
-drive, for
example. This increased sensitivity would result in a more vigorous
muscle spindle response to stretch compared with preperturbation
conditions. The result of this increased sensitivity would be increased
control of static posture. Additionally, an increased efficiency of
presynaptic Ia inhibitory mechanisms could provide another explanation
for the increased postural control.
These results demonstrate an important functional effect of balance
training on elderly subjects. The changes in reflex behavior demonstrated in this study have manifested themselves in a significant decrease in the area of static sway of elderly subjects. This functional change provides important support and incentive for future
research in balance training paradigms that may prevent or rehabilitate
the decline in static balance often observed in elderly individuals.
Effect of H-reflex down training on H/M modulation.
Measurement of H/M was conducted as an attempt to identify the
initiation of any structural changes to the reflex arc. If a decrease
in the ratio was identified in both postures, that could point to an
overall decrease in the excitability of the motoneurons. If a decrease
in the ratio was observed during standing, then changes in presynaptic
control could possibly be identified. As the results indicate, neither
of these situations occurred. However, because no changes in
presynaptic control were apparent during standing testing, that could
provide evidence that the improvements in the static balance of elderly
subjects were due to changes in -drive.
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ACKNOWLEDGEMENTS |
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This study was supported in part by National Institute on Aging Grant R29 AG/OD 13660-01 (to D. M. Koceja).
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FOOTNOTES |
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Address for reprint requests and other correspondence: R. G. Mynark, Dept. of Exercise and Sport Science, CB# 8605, 312 Woollen Hall, Univ. of North Carolina, Chapel Hill, NC 27599-8605 (E-mail: mynark{at}emailunc.edu).
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.
First published March 22, 2002;10.1152/japplphysiol.00007.2001
Received 4 January 2001; accepted in final form 13 March 2002.
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RESULTS
DISCUSSION
REFERENCES
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