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Regulation of motor output between young and elderly subjects
Clinical Neurophysiology 112 (2001) 1273±1279
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Regulation of motor output between young and elderly subjects Donald Earles, Vassilios Vardaxis, David Koceja* Motor Control Laboratory, Department of Kinesiology and Program in Neural Science, HPER 112, Indiana University, Bloomington, IN 47405, USA Accepted 9 April 2001
Abstract Objectives: Considerable information exists concerning the differences in motoneuron pool (MP) excitability between young and elderly subjects. A recent study demonstrated decreased heteronymous Ia facilitation with aging, suggesting increased presynaptic inhibition (PI) with increasing age as a mechanism for this change (Morita et al., Exp Brain Res 104 (1995) 167). It has been suggested that during voluntary movement, supraspinal, and possibly, segmental mechanisms (Hultborn et al., J Physiol 389 (1987) 757) modulate this inhibition. It is theorized that PI can modulate the recruitment gain of the MP during movement without altering the excitability of the motoneurons. Therefore, the purpose of this study was to examine the roles of PI and volitional volleys in modulating MP output in young and elderly subjects. Methods: Twenty apparently healthy females participated in this study, 10 college aged (mean age, 22.4 ^ 2.8 years) and 10 independent, community dwelling elderly (mean age, 77.6 ^ 5.4 years). All subjects were tested in a semi-recumbent position. H-re¯exes were elicited at rest, and at 10 and 20% of maximal voluntary contraction. To assess MP output, background electromyography (EMG) was monitored prior to stimulation. The stimulus intensity was adjusted during volitional contractions to ensure similar control re¯exes (25% of the maximal motor response (M-max)) at each level of contraction. Results: Control re¯exes at each level of volitional contraction (rest, 10 and 20%) were similar for both groups. To assess PI and to estimate the extent to which a change in the H-re¯ex amplitude re¯ects a change in MP gating, the common peroneal nerve was stimulated at 1.5 times the motor threshold 100 ms prior to stimulation of the tibial nerve. Signi®cantly greater PI was observed for the young subjects at rest (5 vs. 13% M-max). At both 10 and 20% levels of voluntary contraction, the conditioned re¯ex was signi®cantly different from rest for the young subjects. The elderly subjects, in contrast, failed to modulate the conditioned re¯ex until the 20% of maximal voluntary contraction (MVC) condition. When examining the recruitment gain in the MP during the PI condition (H-re¯ex amplitude as a function of EMG levels), a signi®cant group effect was observed, with the young subjects demonstrating signi®cantly higher PI gain. Conclusions: These results indicate differential control of MP output (e.g. PI vs. volitional volleys) in young and elderly subjects. q 2001 Published by Elsevier Science Ireland Ltd. All rights reserved. Keywords: H-re¯ex; Presynaptic inhibition; Aging; Re¯ex; Motor output
1. Introduction Spinal re¯exes are often referred to as the servomechanisms responsible for the control of limb position (Sage, 1977). The modulation of these mechanisms during volitional contraction has led to the question of their functional importance. Capaday and Stein (1986) have reported changes in the recruitment gain (as re¯ected by decreases in the soleus H-re¯ex amplitude) during different phases of the gait cycle. It is well established that motor ability deteriorates with progressing age and may re¯ect an inability to modulate these spinal mechanisms (Angulo-Kinzler et al., 1998; Koceja et al., 1995). * Corresponding author. Tel.: 11-812-855-7302; fax: 11-812-855-6778. E-mail address: [email protected] (D. Koceja).
More than 40 years ago, Frank and Fuortes (1957) proposed that monosynaptic excitatory post-synaptic potentials (EPSPs) could be depressed in the absence of any postsynaptic potential change in motoneuron excitability. These investigators theorized that this inhibition was being generated by a centrally driven decrease in the synaptic effectiveness of the Ia afferent prior to its synapse with the motoneuron. This concept of presynaptic inhibition (PI) is important because it suggests that Ia afferents do not function solely as sensory relays, but that these neurons may also function as ®lters, the properties of which may be controlled either centrally or volitionally by inputs to Ia terminals. Modulation of the human soleus H-re¯ex has been observed with changes in body position (Earles et al., 2000; Koceja et al., 1993; Capaday and Stein, 1986). PI has been suggested to be the mechanism responsible for
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these observations (Koceja et al., 1993; Capaday and Stein, 1986). It has been suggested that PI contributes to the execution of voluntary movement and that it can be rapidly and dramatically adapted to the task being carried out (Stein, 1995; Rudomin and Schmidt, 1999). Hultborn et al. (1987) introduced methods that permit the investigation of PI in humans. These studies have suggested that different subsets of interneurons transmit PI to Ia terminals projecting to numerous and varied motoneuron pools (MP). Examination of the extent to which the conditioned H-re¯ex is altered re¯ects a change in Ia gating. Meunier and Pierrot-Deseilligny (1989) developed methods that made it possible to study PI in humans during voluntary contractions. This led to the conclusion that at the onset of a volitional contraction, PI of the agonist primary afferent terminals is decreased while PI of the antagonistic terminals is increased. This selectivity of PI suggests that supraspinal centers do not disregard these interconnections; instead, they suppress their effect when an isolated contraction of a muscle is required. However, one limitation of most H-re¯ex studies and all PI studies to date has been inadequately controlled background electromyography (EMG) levels. Clearly, MP output is the result of both volitional motor commands and Ia gating. Therefore, it is the purpose of this study to examine the role of PI and volitional volleys in modulating the segmental re¯ex system during voluntary isometric contractions in young and elderly subjects. 2. Methods 2.1. Subjects Twenty apparently healthy females participated in this study, 10 independent, community dwelling elderly subjects (mean age, 77.6 ^ 5.4 years) and 10 young subjects (mean age, 22.4 ^ 2.8 years). All subjects indicated no neurological de®cits on a preliminary screening questionnaire. Prior to testing, each subject read and signed an informed consent form, as approved by the Indiana University Internal Review Board. Testing for each subject was conducted at the Motor Control Laboratory at Indiana University, Bloomington, IN and took approximately 2 h. 2.2. Equipment and procedures 2.2.1. H-Re¯ex To assess re¯ex pro®les, electrically evoked H-re¯exes were obtained from each subject (Hugon, 1973). Surface recording EMG electrodes were applied to the soleus and tibialis (TA) muscles of the lower right leg. The placement of the soleus EMG electrode was approximately 2 cm proximal to the musculo-tendinous junction of the triceps surae and the Achilles tendon. The placement of the TA electrode was parallel and lateral to the medial shaft of the tibia, at approximately one-quarter to one-third the distance between
the knee and the ankle. A reference electrode was placed over the lateral malleolus of the leg. The soleus H-re¯ex was elicited with a 0.80 cm diameter-stimulating electrode placed in the popliteal fossa. A 4 cm diameter dispersal pad was placed on the anterior aspect of the knee, just above the patella. An electrical stimulator (Grass instruments S88) was used to generate a 1 ms duration squarewave pulse. Initial measurements of the maximal H-re¯ex amplitude (H-max) and maximal motor response (M-max) were obtained. The intensity of the stimulus was then adjusted to approximately 25% of M-max to ensure that the same percentage of the MP was activated in both young and elderly subjects (Crone et al., 1990; Meinck, 1980). All subjects performed 3 isometric plantar ¯exion maximal voluntary contractions, during which maximal peak-topeak EMG was recorded. These values were used in conjunction with customized software during the voluntary isometric contraction conditions to give the subjects verbal feedback to rest, or contract and hold 10 or 20% of maximal peak-to-peak EMG. Each contraction was a brief duration (1 s) contraction that produced little or no fatigue. The rest period between each contraction was approximately 1 min. The intensity delivered by the stimulator was adjusted to maintain the amplitude of the control re¯ex at 25% of Mmax across all trials. When possible, the trial M-wave that accompanied the control H-re¯ex was used to ensure that the stimulus intensity remained constant from trial to trial. In all cases, this resulted in the H-re¯ex being on the upsloping portion of the control H-re¯ex recruitment curve. On each trial, the dependent variable was the peak-topeak amplitude of the H-re¯ex recorded by computer program and con®rmed by measurement on an oscilloscope. Also, root mean squared background EMG activity was recorded for 75 ms prior to the stimulus in both the soleus and TA muscles. 2.2.2. Soleus H-re¯ex inhibition PI of the soleus Ia afferents was induced by a single conditioning stimulus to the group I afferents of the common peroneal nerve (CP) at the head of the ®bula. The CP was stimulated at a level equivalent to 1.5 times the motor threshold for eliciting an M-wave in the TA muscle. The degree of PI was assessed by comparison of the control and conditioned re¯exes. A condition-test (C-T) interval of 100 ms was used since other investigators have recommended this interval (Zehr and Stein, 1999; Capaday et al., 1995; Iles, 1996; Iles and Pardoe, 1999) for the measurement of PI. To ensure this, one subject was tested with intervals ranging from 1 to 160 ms, and the deep depression of the H-re¯ex was observed at 100 ms. Monitoring the peak-to-peak activity of the TA was used to assessed the stability of the conditioning stimulus. Fig. 1 displays an unconditioned trial and a conditioned trial for a typical young and elderly subject. Note that the
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Fig. 1. Raw EMG tracing of an unconditioned and conditioned trial for a typical young and elderly subject. Note the background EMG prior to the stimulus artifact followed by the test M-wave, and lastly, the test H-re¯ex. (A) rest, unconditioned; (B) rest, conditioned; (C) 20% voluntary activity, unconditioned; (D) 20% voluntary activity, conditioned.
background EMG can be observed prior to the stimulus artifact followed by the H-re¯ex. 2.3. Data acquisition and analysis All data were collected on-line using a custom QuickBASIC computer program with a sampling rate of 2 kHz. EMG pre-ampli®ed electrodes were utilized and connected in series to an EMG mainframe (Therapeutics Unlimited) with a ®nal signal gain of 1000. A dual-channel electrical stimulator (Grass Instruments S88) was used to generate a 1 ms duration square-wave pulse to the tibial and peroneal nerves. Data analysis consisted of a split-plot ANOVA design (group £ percentage effort) with repeated measures on the percentage effort factor. Simple main effects (Keppel, 1991) were run to determine differences within a group, as well as
between groups. For all group comparisons, data were represented as the percentage of M-wave, and the Bonfferoni adjustment was used for multiple comparisons. To compare values with the rest condition for each group, the Dunnett's post-hoc test for comparisons with a control value was used. 3. Results 3.1. Comparisons of EMG levels It is well known that the level of voluntary EMG of the soleus in¯uences the amplitude of the soleus H-re¯ex. Therefore, during voluntary activation, for any comparison between control and conditioned re¯exes to be valid, EMG levels must be recorded just prior to the initiation of the
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stimulus. In this experiment, voluntary EMG was maintained at a constant level during the control and PI conditions at each volitional contraction for each group. For the elderly group, the recti®ed EMG activities were 0.17, 0.43 and 0.78 mV at rest, 10 and 20%, respectively for the control condition, and 0.14, 0.38 and 0.71 mV at rest, 10 and 20%, respectively for the PI condition. For the young group, the recti®ed EMG activities were 0.18, 0.43 and 0.82 mV at rest, 10 and 20%, respectively for the control condition, and 0.10, 0.38 and 0.82 mV at rest, 10 and 20%, respectively for the PI condition. Voluntary EMG levels, as expected, increased linearly at each level of voluntary contraction. 3.2. MP excitability One important aspect of this experiment was to maintain the MP excitability at a constant level as re¯ected by control re¯exes at 0, 10 and 20% of voluntary effort at similar levels. The analyses indicated that control re¯exes across the levels of voluntary contraction (0, 10, and 20% of voluntary effort) were similar for both groups and did not change across the volitional efforts. These values (expressed as a percentage of M-max) were 25.0, 24.1 and 26.4% for the young, and 25.0, 25.7 and 26.3% for the elderly at the rest, 10 and 20% conditions. This was achieved through careful manipulation of stimulus intensity during the onset of volitional contraction, using guidelines outlined by Meunier and Pierrot-Deseilligny (1989). During volitional contractions, the stimulus intensity was adjusted concurrently with the amount of EMG activity to maintain the excitability of the soleus motor pool at 25% of the maximum output. As a result, valid comparisons of PI across voluntary contraction conditions were maintained. 3.3. Comparison of modulation of the conditioned re¯ex When examining PI using a conditioning stimulus to the CP, the young subjects demonstrated greater inhibition of
Fig. 2. Changes in PI during low-force voluntary contractions in young and elderly subjects. Data presented as the percentage of motor pool (mean ^ SE). Note the signi®cant (P , 0:05) difference between young and elderly subjects at rest, with no differences between groups at 10 and 20% of voluntary effort.
the conditioned soleus H-re¯ex (5.3% M-max) when compared with the elderly subjects (13.2% M-max), indicating greater PI in the young group. This simple main effect comparison was signi®cant (F 1;54 5:79; P 0:02), and is shown in Fig. 2. Comparisons between groups at 10 and 20% of voluntary effort were not signi®cant, as depicted in Fig. 2. This is contrary to the results reported by Morita et al. (1995), who suggested that the elderly possess greater PI at rest than young individuals, but consistent with the results of Butchart et al. (1993). When examining differences in the conditioned re¯ex within each group, signi®cant effects were observed for both the young (F 2;36 18:03; P 0:001) and elderly subjects (F 2;36 6:24; P 0:005). Utilizing the Dunnett's post-hoc test to compare the 10 and 20% voluntary effort values with rest, in the young group, the amplitude of the conditioned re¯ex was signi®cantly greater at the 10 and 20% voluntary effort conditions when compared with the rest condition. For example, the young subjects changed PI levels from 5.3% of M-max at rest to 17.1 and 19.8%, at the 10 and 20% voluntary conditions, respectively. The elderly subjects, in contrast, did not signi®cantly modulate the conditioned re¯ex until the 20% voluntary effort condition (13.2% of M-max at rest vs. 22.1% of M-max at 20% MVC). These results are shown in Fig. 2. 3.4. PI gain As mentioned, all H-re¯ex testing is dependent upon the excitability of the target MP prior to the H-re¯ex stimulus. In this study, the EMG was recorded as a measure of motor pool excitability. When the H-re¯ex amplitude was plotted as a function of voluntary EMG during the PI condition, it was observed that the young subjects demonstrated signi®cantly higher recruitment gain. This is shown for all subjects in Fig. 3. Since the intercepts of the lines of best ®t between the two groups were not signi®cantly different (young, 0.4706; elderly, 0.5295), raw amplitude values were used. A signi®-
Fig. 3. Soleus H-re¯ex amplitude for both groups during the PI condition as a function of background EMG activity. There was no signi®cant difference in the intercept value between young and old. Note the marked difference in the slopes (b 1:3103 young, P 0:0001; and b 0:1812 old, P 0:420) of the lines of best ®t. SEE, standard error of the estimate.
D. Earles et al. / Clinical Neurophysiology 112 (2001) 1273±1279
cant difference in the slope between the two groups was observed (b 1:3103 young; b 0:1812 old). From these results, it was concluded that the gain of the conditioned re¯ex was different between young and elderly subjects. Individuals in each group were re¯ective of this trend. For example, Figs. 4 and 5 depict the re¯ex gain under the two conditions for a typical elderly and young subject. Note that there is little change in the slope of the line during the control condition. This is attributable to the fact that during volitional contractions, the stimulus intensity was adjusted concurrently with the amount of voluntary EMG to maintain the excitability of the soleus motor pool at 25% of the maximum output. However, during the PI condition, the elderly subject demonstrates a smaller slope change than the young subject.
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Fig. 5. Soleus H-re¯ex amplitude for a typical elderly subject during both conditions as a function of background EMG activity. Note that there is little change in the slope of the line during the control condition. This is attributable to the fact that during volitional contractions, the stimulus intensity was adjusted concurrently with the amount of background EMG activity to maintain the excitability of the soleus motor pool at 25% of maximum output.
4. Discussion The results of this study reveal that young subjects display greater PI at rest than elderly subjects. It was also observed that across all levels of voluntary isometric contraction, young subjects demonstrate a signi®cantly higher gain of PI. These results suggest that young and elderly subjects use different control mechanisms when mediating motor output. It appears that to maintain motor output at equal levels during submaximal contractions, young subjects modulate PI, whereas elderly subjects rely less on PI and more on direct motor activation. Monosynaptic stretch re¯exes are often referred to as the servomechanisms responsible for the control of limb position (Sage, 1977). Matthews (1972) reported observing gain in these mechanisms during steady contraction. Since that time, many investigators have tried to elucidate on the functional importance of these modulatory effects. For example, studies from our laboratory demonstrated that when task complexity is increased, the soleus H-re¯ex is down-regulated (Trimble and Koceja, 1994; Hoffman and Koceja, 1995). Similarly, Capaday and Stein (1986) demonstrated
Fig. 4. Soleus H-re¯ex amplitude for a typical young subject during both conditions as a function of background EMG activity. Note that there is little change in the slope of the line during the control condition. This is attributable to the fact that during volitional contractions, the stimulus intensity was adjusted concurrently with the amount of background EMG activity to maintain the excitability of the soleus motor pool at 25% of maximum output.
that the amplitude of the soleus H-re¯ex was depressed when subjects walked compared with when they stood relaxed. They later showed that the amplitude of the soleus H-re¯ex was further depressed when subjects ran compared with when they walked (Capaday and Stein, 1987). In all of these studies, PI was mentioned as a possible mediating mechanism for these observed H-re¯ex changes. Problems have been noted when comparing H-re¯exes at rest and during voluntary contraction (Rudomin, 1999). This is due to the fact that contraction may induce greater excitability of the MP, resulting in a change in the recruitment gain of the re¯ex. Crone et al. (1990) reported that the sensitivity of the H-re¯ex to facilitation and inhibition could vary with the size of the control re¯ex. Therefore, in the present study, we adjusted the test stimulus intensity so that the size of the unconditioned re¯ex was the same at each level of contraction. This technique has been recommended by Crone et al. (1990) and should allow for comparisons across percentages of MVC. It is also worth noting that in this study, the use of surface EMG was used to monitor voluntary effort, and perhaps similar EMG levels were observed with shifts in motoneuron recruitment between the groups. Although this cannot be ruled out entirely, the relationship between EMG and force is linear at these moderate force levels, and recti®ed EMG values are expected to be representative of motor output. With respect to H-re¯ex differences with aging, Koceja et al. (1995) reported that young subjects depress the amplitude of the soleus H-re¯ex when moving from a prone to a weight-bearing position, whereas elderly subjects facilitate the amplitude of the soleus H-re¯ex. This result is counter-intuitive to re¯ex gain, as greater background EMG activity is present when weight-bearing. A more recent study from our laboratory controlled for background EMG levels by examining the gain of the soleus H-re¯ex and reported similar results Ð young subjects decreased the gain in unstable environments, whereas elderly subjects increased the gain in unstable
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environments (Earles et al., 2000). Again, PI was identi®ed as a potential mediating mechanism. The present results help to clarify these past ®ndings by revealing differences in PI gain between young and elderly subjects. Our present results also point towards the importance of monitoring background EMG in the interpretation of Hre¯ex modulation. At rest, we report that PI is less in elderly subjects Ð this is in opposition to the results of Morita et al. (1995) who reported increased PI at rest in an aged sample. We offer two explanations for the con¯icting results. One, Morita et al. (1995) utilized a heteronymous conditioning protocol to assess the modulation of PI interneurons. In the present study, we utilized a peroneal conditioning protocol, which assesses PI of soleus Ia ®bers. We suggest that the two protocols may, in fact, measure different facets of PI to the soleus Ia ®bers. Inspection of Fig. 2 from Hultborn et al. (1987) bears this out. The heteronymous conditioning protocol assesses PI of quadriceps Ia ®bers, which synapse to the soleus motor pool; the peroneal conditioning protocol assesses PI of soleus Ia ®bers activated through tibialis anterior Ia ®ber connections. It is suggested that the effects observed with one protocol are not identical to the effects observed with the other protocol. It is recommended, therefore, that consideration be given to the measurement protocol when examining PI in humans. Second, Morita et al. (1995) failed to measure background EMG activity. In the present study, con¯icting interpretations can arise from failure to monitor and closely control background EMG, as the net motor output (e.g. Hre¯ex amplitude) is in¯uenced by both PI and background excitability levels of the motoneurons. Thus, it is also recommended that in all re¯ex studies, background EMG must be accounted for when discussing modulatory changes in motor output. This is true regardless of whether voluntary effort is being exerted (e.g. at rest in this study), as small shifts in motor pool excitability may result in alterations in presynaptic neurons. This argument is supported by the similar results between this study and those of Butchart et al. (1993), who reported less PI in elderly subjects at rest and during voluntary contractions. Butchart et al. (1993) utilized the same muscle groups, but a different stimulus Ð a vibratory stimulus to the tibialis anterior tendon. In the present study, an electrical stimulus was applied to the peroneal nerve and similar results were obtained, both at rest and during voluntary effort. However, in the present study, muscle activation was maintained at consistent levels (e.g. 10 and 20%) across groups, so that comparisons of equal relative muscle activation were used. The observed decrease in PI at low levels of voluntary contraction in young subjects resulted in the maintenance in the level of gain of the soleus H-re¯ex. This may be of functional importance at the initiation of movements before the force requirement is known. The presence of large amounts of PI at rest may be the means by which centrally driven mechanisms focus activity on the motor pools needed
for the performance of the task. In elderly subjects, in contrast, lower levels of PI at rest, and an inability to modulate PI during movement, results in motor control being shifted from speci®c control mechanisms (e.g. PI) to more general control mechanisms (e.g. motor drive), although this interpretation remains to be fully explored. Note that Fig. 3 represents this fact, as the slope of the line of best ®t for the elderly subjects is very small, depicting little change in recruitment gain during the PI condition when performing low-force contractions. Of course, the role of post-synaptic mechanisms (e.g. recurrent inhibition, Ib inhibition) cannot be ruled out entirely from these experiments, and may have impacted on the results. In conclusion, the present study reveals differential gain control of the soleus H-re¯ex in young and elderly subjects. It appears that to maintain motor output at equal levels during submaximal contractions, young subjects modulate PI, whereas elderly subjects rely less on PI and more on direct motor activation. It appears that the level of supraspinal input plays an important role in the gain regulation in both young and elderly subjects and that young subjects are capable of releasing PI with less input. The functional signi®cance of this difference warrants further investigation. Acknowledgements This work was supported in part by a grant from the National Institutes of Health (R29 AG/OD 13660-01) to D.M. Koceja. References Angulo-Kinzler R, Mynark RM, Koceja DM. Soleus H-re¯ex modulation in young and elderly subjects: modulation due to body position. J Gerontol 1998;53:M120±M125. Butchart P, Farquhar R, Part NJ, Roberts RC. The effect of age and voluntary contraction on presynaptic inhibition of soleus muscle Ia afferent terminals in man. Exp Physiol 1993;78(2):235±242. Capaday C, Stein RB. Amplitude modulation of the soleus H-re¯ex in the human during walking and standing. J Neurosci 1986;6:1308±1313. Capaday C, Stein RB. Differences in the amplitude of the soleus H-re¯ex during walking and running. J Physiol 1987;392:513±522. Capaday C, Lavoie BA, Comeau F. Differential effects of a ¯exor nerve input on the soleus H-re¯ex during standing versus walking. Can J Physiol Pharmacol 1995;73(4):436±449. Crone C, Hultborn H, Mazieres L, Morin C, Nielsen J, Pierrot-Deseilligny E. Sensitivity of monosynaptic test re¯exes to facilitation and inhibition as a function of the test re¯ex size: a study in man and the cat. Exp Brain Res 1990;81:35±45. Earles DR, Shively CW, Koceja DM. The effects of vision and task complexity on Hoffmann re¯ex gain in elderly and young subjects. Int J Neurosci 2000 in press. Frank K, Fuortes MGF. Presynaptic and postsynaptic inhibition of monosynaptic re¯exes. Fed Proc 1957;16:39±40. Hoffman M, Koceja DM. The effects of vision and task complexity on Hoffmann re¯ex gain. Brain Res 1995;700:303±307. Hugon M. Methodology of the Hoffmann re¯ex. In: Desmedt JE, editor.
D. Earles et al. / Clinical Neurophysiology 112 (2001) 1273±1279 New developments in electromyography and clinical neurophysiology, Vol. 3. Basel: Karger, 1973. pp. 277±293. Hultborn H, Menuier S, Pierrot-Deseilligny E, Shindo M. Changes in presynaptic inhibition of Ia ®bers at the onset of voluntary contraction in man. J Physiol 1987;389:757±772. Iles JF. Evidence for cutaneous and corticospinal modulation of presynaptic inhibition of Ia afferents from the human lower limb. J Physiol 1996;491:197±207. Iles JF, Pardoe J. Changes in transmission in the pathway of heteronymous spinal recurrent inhibition from soleus to quadriceps motor neurons during movement in man. Brain 1999;122:1757±1764. Keppel G. Design and analysis: a researcher's handbook, Englewood Cliffs, NJ: Prentice±Hall, 1991. Koceja DM, Trimble MH, Earles DR. Inhibition of the soleus H-re¯ex in standing man. Brain Res 1993;629:155±158. Koceja DM, Markus CA, Trimble MH. Postural modulation of the soleus H-re¯ex in young and old subjects. Electroenceph clin Neurophysiol 1995;97:387±393. Matthews PBC. Mammalian muscle spindles and their central action, London: Arnold, 1972.
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Meinck HM. Facilitation and inhibition of the human H-re¯ex as a function of the amplitude of the control re¯ex. Electroenceph clin Neurophysiol 1980;48(2):203±211. Meunier S, Pierrot-Deseilligny E. Gating of the afferent volley of the monosynaptic stretch re¯ex during movement in man. J Physiol 1989;419:753±763. Morita H, Shindo M, Yanagawa S, Yoshida T, Momoi H, Yanagisawa N. Progressive decrease in heteronymous monosynaptic Ia facilitation with human ageing. Exp Brain Res 1995;104:167±170. Rudomin P. Presynaptic selection of afferent in¯ow in the spinal cord. J Physiol 1999;93(4):329±347. Rudomin P, Schmidt RF. Presynaptic inhibition in the vertebrate spinal cord revisited. Exp Brain Res 1999;129(1):1±37. Sage GH. Introduction to motor behavior: a neuropsychological approach, Reading, MA: Addison±Wesley, 1977. Stein RB. Presynaptic inhibition in humans. Prog Neurobiol 1995;47:533± 544. Trimble MH, Koceja DM. Modulation of the triceps surae H-re¯ex with training. Int J Neurosci 1994;76:293±303. Zehr EP, Stein RB. Interaction of the Jendrassik maneuver with segmental presynaptic inhibition. Exp Brain Res 1999;124:474±480.
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Regulation of motor output between young and elderly subjects Donald Earles, Vassilios Vardaxis, David Koceja* Motor Control Laboratory, Department of Kinesiology and Program in Neural Science, HPER 112, Indiana University, Bloomington, IN 47405, USA Accepted 9 April 2001
Abstract Objectives: Considerable information exists concerning the differences in motoneuron pool (MP) excitability between young and elderly subjects. A recent study demonstrated decreased heteronymous Ia facilitation with aging, suggesting increased presynaptic inhibition (PI) with increasing age as a mechanism for this change (Morita et al., Exp Brain Res 104 (1995) 167). It has been suggested that during voluntary movement, supraspinal, and possibly, segmental mechanisms (Hultborn et al., J Physiol 389 (1987) 757) modulate this inhibition. It is theorized that PI can modulate the recruitment gain of the MP during movement without altering the excitability of the motoneurons. Therefore, the purpose of this study was to examine the roles of PI and volitional volleys in modulating MP output in young and elderly subjects. Methods: Twenty apparently healthy females participated in this study, 10 college aged (mean age, 22.4 ^ 2.8 years) and 10 independent, community dwelling elderly (mean age, 77.6 ^ 5.4 years). All subjects were tested in a semi-recumbent position. H-re¯exes were elicited at rest, and at 10 and 20% of maximal voluntary contraction. To assess MP output, background electromyography (EMG) was monitored prior to stimulation. The stimulus intensity was adjusted during volitional contractions to ensure similar control re¯exes (25% of the maximal motor response (M-max)) at each level of contraction. Results: Control re¯exes at each level of volitional contraction (rest, 10 and 20%) were similar for both groups. To assess PI and to estimate the extent to which a change in the H-re¯ex amplitude re¯ects a change in MP gating, the common peroneal nerve was stimulated at 1.5 times the motor threshold 100 ms prior to stimulation of the tibial nerve. Signi®cantly greater PI was observed for the young subjects at rest (5 vs. 13% M-max). At both 10 and 20% levels of voluntary contraction, the conditioned re¯ex was signi®cantly different from rest for the young subjects. The elderly subjects, in contrast, failed to modulate the conditioned re¯ex until the 20% of maximal voluntary contraction (MVC) condition. When examining the recruitment gain in the MP during the PI condition (H-re¯ex amplitude as a function of EMG levels), a signi®cant group effect was observed, with the young subjects demonstrating signi®cantly higher PI gain. Conclusions: These results indicate differential control of MP output (e.g. PI vs. volitional volleys) in young and elderly subjects. q 2001 Published by Elsevier Science Ireland Ltd. All rights reserved. Keywords: H-re¯ex; Presynaptic inhibition; Aging; Re¯ex; Motor output
1. Introduction Spinal re¯exes are often referred to as the servomechanisms responsible for the control of limb position (Sage, 1977). The modulation of these mechanisms during volitional contraction has led to the question of their functional importance. Capaday and Stein (1986) have reported changes in the recruitment gain (as re¯ected by decreases in the soleus H-re¯ex amplitude) during different phases of the gait cycle. It is well established that motor ability deteriorates with progressing age and may re¯ect an inability to modulate these spinal mechanisms (Angulo-Kinzler et al., 1998; Koceja et al., 1995). * Corresponding author. Tel.: 11-812-855-7302; fax: 11-812-855-6778. E-mail address: [email protected] (D. Koceja).
More than 40 years ago, Frank and Fuortes (1957) proposed that monosynaptic excitatory post-synaptic potentials (EPSPs) could be depressed in the absence of any postsynaptic potential change in motoneuron excitability. These investigators theorized that this inhibition was being generated by a centrally driven decrease in the synaptic effectiveness of the Ia afferent prior to its synapse with the motoneuron. This concept of presynaptic inhibition (PI) is important because it suggests that Ia afferents do not function solely as sensory relays, but that these neurons may also function as ®lters, the properties of which may be controlled either centrally or volitionally by inputs to Ia terminals. Modulation of the human soleus H-re¯ex has been observed with changes in body position (Earles et al., 2000; Koceja et al., 1993; Capaday and Stein, 1986). PI has been suggested to be the mechanism responsible for
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these observations (Koceja et al., 1993; Capaday and Stein, 1986). It has been suggested that PI contributes to the execution of voluntary movement and that it can be rapidly and dramatically adapted to the task being carried out (Stein, 1995; Rudomin and Schmidt, 1999). Hultborn et al. (1987) introduced methods that permit the investigation of PI in humans. These studies have suggested that different subsets of interneurons transmit PI to Ia terminals projecting to numerous and varied motoneuron pools (MP). Examination of the extent to which the conditioned H-re¯ex is altered re¯ects a change in Ia gating. Meunier and Pierrot-Deseilligny (1989) developed methods that made it possible to study PI in humans during voluntary contractions. This led to the conclusion that at the onset of a volitional contraction, PI of the agonist primary afferent terminals is decreased while PI of the antagonistic terminals is increased. This selectivity of PI suggests that supraspinal centers do not disregard these interconnections; instead, they suppress their effect when an isolated contraction of a muscle is required. However, one limitation of most H-re¯ex studies and all PI studies to date has been inadequately controlled background electromyography (EMG) levels. Clearly, MP output is the result of both volitional motor commands and Ia gating. Therefore, it is the purpose of this study to examine the role of PI and volitional volleys in modulating the segmental re¯ex system during voluntary isometric contractions in young and elderly subjects. 2. Methods 2.1. Subjects Twenty apparently healthy females participated in this study, 10 independent, community dwelling elderly subjects (mean age, 77.6 ^ 5.4 years) and 10 young subjects (mean age, 22.4 ^ 2.8 years). All subjects indicated no neurological de®cits on a preliminary screening questionnaire. Prior to testing, each subject read and signed an informed consent form, as approved by the Indiana University Internal Review Board. Testing for each subject was conducted at the Motor Control Laboratory at Indiana University, Bloomington, IN and took approximately 2 h. 2.2. Equipment and procedures 2.2.1. H-Re¯ex To assess re¯ex pro®les, electrically evoked H-re¯exes were obtained from each subject (Hugon, 1973). Surface recording EMG electrodes were applied to the soleus and tibialis (TA) muscles of the lower right leg. The placement of the soleus EMG electrode was approximately 2 cm proximal to the musculo-tendinous junction of the triceps surae and the Achilles tendon. The placement of the TA electrode was parallel and lateral to the medial shaft of the tibia, at approximately one-quarter to one-third the distance between
the knee and the ankle. A reference electrode was placed over the lateral malleolus of the leg. The soleus H-re¯ex was elicited with a 0.80 cm diameter-stimulating electrode placed in the popliteal fossa. A 4 cm diameter dispersal pad was placed on the anterior aspect of the knee, just above the patella. An electrical stimulator (Grass instruments S88) was used to generate a 1 ms duration squarewave pulse. Initial measurements of the maximal H-re¯ex amplitude (H-max) and maximal motor response (M-max) were obtained. The intensity of the stimulus was then adjusted to approximately 25% of M-max to ensure that the same percentage of the MP was activated in both young and elderly subjects (Crone et al., 1990; Meinck, 1980). All subjects performed 3 isometric plantar ¯exion maximal voluntary contractions, during which maximal peak-topeak EMG was recorded. These values were used in conjunction with customized software during the voluntary isometric contraction conditions to give the subjects verbal feedback to rest, or contract and hold 10 or 20% of maximal peak-to-peak EMG. Each contraction was a brief duration (1 s) contraction that produced little or no fatigue. The rest period between each contraction was approximately 1 min. The intensity delivered by the stimulator was adjusted to maintain the amplitude of the control re¯ex at 25% of Mmax across all trials. When possible, the trial M-wave that accompanied the control H-re¯ex was used to ensure that the stimulus intensity remained constant from trial to trial. In all cases, this resulted in the H-re¯ex being on the upsloping portion of the control H-re¯ex recruitment curve. On each trial, the dependent variable was the peak-topeak amplitude of the H-re¯ex recorded by computer program and con®rmed by measurement on an oscilloscope. Also, root mean squared background EMG activity was recorded for 75 ms prior to the stimulus in both the soleus and TA muscles. 2.2.2. Soleus H-re¯ex inhibition PI of the soleus Ia afferents was induced by a single conditioning stimulus to the group I afferents of the common peroneal nerve (CP) at the head of the ®bula. The CP was stimulated at a level equivalent to 1.5 times the motor threshold for eliciting an M-wave in the TA muscle. The degree of PI was assessed by comparison of the control and conditioned re¯exes. A condition-test (C-T) interval of 100 ms was used since other investigators have recommended this interval (Zehr and Stein, 1999; Capaday et al., 1995; Iles, 1996; Iles and Pardoe, 1999) for the measurement of PI. To ensure this, one subject was tested with intervals ranging from 1 to 160 ms, and the deep depression of the H-re¯ex was observed at 100 ms. Monitoring the peak-to-peak activity of the TA was used to assessed the stability of the conditioning stimulus. Fig. 1 displays an unconditioned trial and a conditioned trial for a typical young and elderly subject. Note that the
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Fig. 1. Raw EMG tracing of an unconditioned and conditioned trial for a typical young and elderly subject. Note the background EMG prior to the stimulus artifact followed by the test M-wave, and lastly, the test H-re¯ex. (A) rest, unconditioned; (B) rest, conditioned; (C) 20% voluntary activity, unconditioned; (D) 20% voluntary activity, conditioned.
background EMG can be observed prior to the stimulus artifact followed by the H-re¯ex. 2.3. Data acquisition and analysis All data were collected on-line using a custom QuickBASIC computer program with a sampling rate of 2 kHz. EMG pre-ampli®ed electrodes were utilized and connected in series to an EMG mainframe (Therapeutics Unlimited) with a ®nal signal gain of 1000. A dual-channel electrical stimulator (Grass Instruments S88) was used to generate a 1 ms duration square-wave pulse to the tibial and peroneal nerves. Data analysis consisted of a split-plot ANOVA design (group £ percentage effort) with repeated measures on the percentage effort factor. Simple main effects (Keppel, 1991) were run to determine differences within a group, as well as
between groups. For all group comparisons, data were represented as the percentage of M-wave, and the Bonfferoni adjustment was used for multiple comparisons. To compare values with the rest condition for each group, the Dunnett's post-hoc test for comparisons with a control value was used. 3. Results 3.1. Comparisons of EMG levels It is well known that the level of voluntary EMG of the soleus in¯uences the amplitude of the soleus H-re¯ex. Therefore, during voluntary activation, for any comparison between control and conditioned re¯exes to be valid, EMG levels must be recorded just prior to the initiation of the
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stimulus. In this experiment, voluntary EMG was maintained at a constant level during the control and PI conditions at each volitional contraction for each group. For the elderly group, the recti®ed EMG activities were 0.17, 0.43 and 0.78 mV at rest, 10 and 20%, respectively for the control condition, and 0.14, 0.38 and 0.71 mV at rest, 10 and 20%, respectively for the PI condition. For the young group, the recti®ed EMG activities were 0.18, 0.43 and 0.82 mV at rest, 10 and 20%, respectively for the control condition, and 0.10, 0.38 and 0.82 mV at rest, 10 and 20%, respectively for the PI condition. Voluntary EMG levels, as expected, increased linearly at each level of voluntary contraction. 3.2. MP excitability One important aspect of this experiment was to maintain the MP excitability at a constant level as re¯ected by control re¯exes at 0, 10 and 20% of voluntary effort at similar levels. The analyses indicated that control re¯exes across the levels of voluntary contraction (0, 10, and 20% of voluntary effort) were similar for both groups and did not change across the volitional efforts. These values (expressed as a percentage of M-max) were 25.0, 24.1 and 26.4% for the young, and 25.0, 25.7 and 26.3% for the elderly at the rest, 10 and 20% conditions. This was achieved through careful manipulation of stimulus intensity during the onset of volitional contraction, using guidelines outlined by Meunier and Pierrot-Deseilligny (1989). During volitional contractions, the stimulus intensity was adjusted concurrently with the amount of EMG activity to maintain the excitability of the soleus motor pool at 25% of the maximum output. As a result, valid comparisons of PI across voluntary contraction conditions were maintained. 3.3. Comparison of modulation of the conditioned re¯ex When examining PI using a conditioning stimulus to the CP, the young subjects demonstrated greater inhibition of
Fig. 2. Changes in PI during low-force voluntary contractions in young and elderly subjects. Data presented as the percentage of motor pool (mean ^ SE). Note the signi®cant (P , 0:05) difference between young and elderly subjects at rest, with no differences between groups at 10 and 20% of voluntary effort.
the conditioned soleus H-re¯ex (5.3% M-max) when compared with the elderly subjects (13.2% M-max), indicating greater PI in the young group. This simple main effect comparison was signi®cant (F 1;54 5:79; P 0:02), and is shown in Fig. 2. Comparisons between groups at 10 and 20% of voluntary effort were not signi®cant, as depicted in Fig. 2. This is contrary to the results reported by Morita et al. (1995), who suggested that the elderly possess greater PI at rest than young individuals, but consistent with the results of Butchart et al. (1993). When examining differences in the conditioned re¯ex within each group, signi®cant effects were observed for both the young (F 2;36 18:03; P 0:001) and elderly subjects (F 2;36 6:24; P 0:005). Utilizing the Dunnett's post-hoc test to compare the 10 and 20% voluntary effort values with rest, in the young group, the amplitude of the conditioned re¯ex was signi®cantly greater at the 10 and 20% voluntary effort conditions when compared with the rest condition. For example, the young subjects changed PI levels from 5.3% of M-max at rest to 17.1 and 19.8%, at the 10 and 20% voluntary conditions, respectively. The elderly subjects, in contrast, did not signi®cantly modulate the conditioned re¯ex until the 20% voluntary effort condition (13.2% of M-max at rest vs. 22.1% of M-max at 20% MVC). These results are shown in Fig. 2. 3.4. PI gain As mentioned, all H-re¯ex testing is dependent upon the excitability of the target MP prior to the H-re¯ex stimulus. In this study, the EMG was recorded as a measure of motor pool excitability. When the H-re¯ex amplitude was plotted as a function of voluntary EMG during the PI condition, it was observed that the young subjects demonstrated signi®cantly higher recruitment gain. This is shown for all subjects in Fig. 3. Since the intercepts of the lines of best ®t between the two groups were not signi®cantly different (young, 0.4706; elderly, 0.5295), raw amplitude values were used. A signi®-
Fig. 3. Soleus H-re¯ex amplitude for both groups during the PI condition as a function of background EMG activity. There was no signi®cant difference in the intercept value between young and old. Note the marked difference in the slopes (b 1:3103 young, P 0:0001; and b 0:1812 old, P 0:420) of the lines of best ®t. SEE, standard error of the estimate.
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cant difference in the slope between the two groups was observed (b 1:3103 young; b 0:1812 old). From these results, it was concluded that the gain of the conditioned re¯ex was different between young and elderly subjects. Individuals in each group were re¯ective of this trend. For example, Figs. 4 and 5 depict the re¯ex gain under the two conditions for a typical elderly and young subject. Note that there is little change in the slope of the line during the control condition. This is attributable to the fact that during volitional contractions, the stimulus intensity was adjusted concurrently with the amount of voluntary EMG to maintain the excitability of the soleus motor pool at 25% of the maximum output. However, during the PI condition, the elderly subject demonstrates a smaller slope change than the young subject.
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Fig. 5. Soleus H-re¯ex amplitude for a typical elderly subject during both conditions as a function of background EMG activity. Note that there is little change in the slope of the line during the control condition. This is attributable to the fact that during volitional contractions, the stimulus intensity was adjusted concurrently with the amount of background EMG activity to maintain the excitability of the soleus motor pool at 25% of maximum output.
4. Discussion The results of this study reveal that young subjects display greater PI at rest than elderly subjects. It was also observed that across all levels of voluntary isometric contraction, young subjects demonstrate a signi®cantly higher gain of PI. These results suggest that young and elderly subjects use different control mechanisms when mediating motor output. It appears that to maintain motor output at equal levels during submaximal contractions, young subjects modulate PI, whereas elderly subjects rely less on PI and more on direct motor activation. Monosynaptic stretch re¯exes are often referred to as the servomechanisms responsible for the control of limb position (Sage, 1977). Matthews (1972) reported observing gain in these mechanisms during steady contraction. Since that time, many investigators have tried to elucidate on the functional importance of these modulatory effects. For example, studies from our laboratory demonstrated that when task complexity is increased, the soleus H-re¯ex is down-regulated (Trimble and Koceja, 1994; Hoffman and Koceja, 1995). Similarly, Capaday and Stein (1986) demonstrated
Fig. 4. Soleus H-re¯ex amplitude for a typical young subject during both conditions as a function of background EMG activity. Note that there is little change in the slope of the line during the control condition. This is attributable to the fact that during volitional contractions, the stimulus intensity was adjusted concurrently with the amount of background EMG activity to maintain the excitability of the soleus motor pool at 25% of maximum output.
that the amplitude of the soleus H-re¯ex was depressed when subjects walked compared with when they stood relaxed. They later showed that the amplitude of the soleus H-re¯ex was further depressed when subjects ran compared with when they walked (Capaday and Stein, 1987). In all of these studies, PI was mentioned as a possible mediating mechanism for these observed H-re¯ex changes. Problems have been noted when comparing H-re¯exes at rest and during voluntary contraction (Rudomin, 1999). This is due to the fact that contraction may induce greater excitability of the MP, resulting in a change in the recruitment gain of the re¯ex. Crone et al. (1990) reported that the sensitivity of the H-re¯ex to facilitation and inhibition could vary with the size of the control re¯ex. Therefore, in the present study, we adjusted the test stimulus intensity so that the size of the unconditioned re¯ex was the same at each level of contraction. This technique has been recommended by Crone et al. (1990) and should allow for comparisons across percentages of MVC. It is also worth noting that in this study, the use of surface EMG was used to monitor voluntary effort, and perhaps similar EMG levels were observed with shifts in motoneuron recruitment between the groups. Although this cannot be ruled out entirely, the relationship between EMG and force is linear at these moderate force levels, and recti®ed EMG values are expected to be representative of motor output. With respect to H-re¯ex differences with aging, Koceja et al. (1995) reported that young subjects depress the amplitude of the soleus H-re¯ex when moving from a prone to a weight-bearing position, whereas elderly subjects facilitate the amplitude of the soleus H-re¯ex. This result is counter-intuitive to re¯ex gain, as greater background EMG activity is present when weight-bearing. A more recent study from our laboratory controlled for background EMG levels by examining the gain of the soleus H-re¯ex and reported similar results Ð young subjects decreased the gain in unstable environments, whereas elderly subjects increased the gain in unstable
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environments (Earles et al., 2000). Again, PI was identi®ed as a potential mediating mechanism. The present results help to clarify these past ®ndings by revealing differences in PI gain between young and elderly subjects. Our present results also point towards the importance of monitoring background EMG in the interpretation of Hre¯ex modulation. At rest, we report that PI is less in elderly subjects Ð this is in opposition to the results of Morita et al. (1995) who reported increased PI at rest in an aged sample. We offer two explanations for the con¯icting results. One, Morita et al. (1995) utilized a heteronymous conditioning protocol to assess the modulation of PI interneurons. In the present study, we utilized a peroneal conditioning protocol, which assesses PI of soleus Ia ®bers. We suggest that the two protocols may, in fact, measure different facets of PI to the soleus Ia ®bers. Inspection of Fig. 2 from Hultborn et al. (1987) bears this out. The heteronymous conditioning protocol assesses PI of quadriceps Ia ®bers, which synapse to the soleus motor pool; the peroneal conditioning protocol assesses PI of soleus Ia ®bers activated through tibialis anterior Ia ®ber connections. It is suggested that the effects observed with one protocol are not identical to the effects observed with the other protocol. It is recommended, therefore, that consideration be given to the measurement protocol when examining PI in humans. Second, Morita et al. (1995) failed to measure background EMG activity. In the present study, con¯icting interpretations can arise from failure to monitor and closely control background EMG, as the net motor output (e.g. Hre¯ex amplitude) is in¯uenced by both PI and background excitability levels of the motoneurons. Thus, it is also recommended that in all re¯ex studies, background EMG must be accounted for when discussing modulatory changes in motor output. This is true regardless of whether voluntary effort is being exerted (e.g. at rest in this study), as small shifts in motor pool excitability may result in alterations in presynaptic neurons. This argument is supported by the similar results between this study and those of Butchart et al. (1993), who reported less PI in elderly subjects at rest and during voluntary contractions. Butchart et al. (1993) utilized the same muscle groups, but a different stimulus Ð a vibratory stimulus to the tibialis anterior tendon. In the present study, an electrical stimulus was applied to the peroneal nerve and similar results were obtained, both at rest and during voluntary effort. However, in the present study, muscle activation was maintained at consistent levels (e.g. 10 and 20%) across groups, so that comparisons of equal relative muscle activation were used. The observed decrease in PI at low levels of voluntary contraction in young subjects resulted in the maintenance in the level of gain of the soleus H-re¯ex. This may be of functional importance at the initiation of movements before the force requirement is known. The presence of large amounts of PI at rest may be the means by which centrally driven mechanisms focus activity on the motor pools needed
for the performance of the task. In elderly subjects, in contrast, lower levels of PI at rest, and an inability to modulate PI during movement, results in motor control being shifted from speci®c control mechanisms (e.g. PI) to more general control mechanisms (e.g. motor drive), although this interpretation remains to be fully explored. Note that Fig. 3 represents this fact, as the slope of the line of best ®t for the elderly subjects is very small, depicting little change in recruitment gain during the PI condition when performing low-force contractions. Of course, the role of post-synaptic mechanisms (e.g. recurrent inhibition, Ib inhibition) cannot be ruled out entirely from these experiments, and may have impacted on the results. In conclusion, the present study reveals differential gain control of the soleus H-re¯ex in young and elderly subjects. It appears that to maintain motor output at equal levels during submaximal contractions, young subjects modulate PI, whereas elderly subjects rely less on PI and more on direct motor activation. It appears that the level of supraspinal input plays an important role in the gain regulation in both young and elderly subjects and that young subjects are capable of releasing PI with less input. The functional signi®cance of this difference warrants further investigation. Acknowledgements This work was supported in part by a grant from the National Institutes of Health (R29 AG/OD 13660-01) to D.M. Koceja. References Angulo-Kinzler R, Mynark RM, Koceja DM. Soleus H-re¯ex modulation in young and elderly subjects: modulation due to body position. J Gerontol 1998;53:M120±M125. Butchart P, Farquhar R, Part NJ, Roberts RC. The effect of age and voluntary contraction on presynaptic inhibition of soleus muscle Ia afferent terminals in man. Exp Physiol 1993;78(2):235±242. Capaday C, Stein RB. Amplitude modulation of the soleus H-re¯ex in the human during walking and standing. J Neurosci 1986;6:1308±1313. Capaday C, Stein RB. Differences in the amplitude of the soleus H-re¯ex during walking and running. J Physiol 1987;392:513±522. Capaday C, Lavoie BA, Comeau F. Differential effects of a ¯exor nerve input on the soleus H-re¯ex during standing versus walking. Can J Physiol Pharmacol 1995;73(4):436±449. Crone C, Hultborn H, Mazieres L, Morin C, Nielsen J, Pierrot-Deseilligny E. Sensitivity of monosynaptic test re¯exes to facilitation and inhibition as a function of the test re¯ex size: a study in man and the cat. Exp Brain Res 1990;81:35±45. Earles DR, Shively CW, Koceja DM. The effects of vision and task complexity on Hoffmann re¯ex gain in elderly and young subjects. Int J Neurosci 2000 in press. Frank K, Fuortes MGF. Presynaptic and postsynaptic inhibition of monosynaptic re¯exes. Fed Proc 1957;16:39±40. Hoffman M, Koceja DM. The effects of vision and task complexity on Hoffmann re¯ex gain. Brain Res 1995;700:303±307. Hugon M. Methodology of the Hoffmann re¯ex. In: Desmedt JE, editor.
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