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Stiffness regulation provided by short-latency reflexes in human triceps surae muscles
Brain Research, 234 (1982) 159-164 Elsevier Biomedical Press
159
Stiffness regulation provided by short-latency reflexes in human triceps surae muscles
J. H. J. ALLUM, K.-H. MAURITZ and H. VOGELE Brain Research Institute, August-Forel-Strasse 1, CH-8029 Zurich (Switzerland) and (K.-H.M. and H.V.) Department of Neurology, University of Freiburg, Freiburg (F.R.G.)
(Accepted November 12th, 198l) Key words: stretch reflex - - muscle stiffness - - triceps surae muscles - - human
The triceps surae muscles of normal human subjects were rapidly stretched and released by rotating the foot about the ankle joint with a torque motor. Following the initial intrinsic resistance, the yielding observed in incremental force records was more rapid for stretch than for release responses. Short-latency EMG responses elicited by stretch recruit force, to compensate for the yielding and to maintain the total (intrinsic plus reflex) resistance constant as the prior force level changes. Spinal stretch reflexes produce at least two burst of reflex E M G activity in a stretched muscle4, is. The most distinct, the short-latency (SL) reflex, is characterized by a highly synchronized burst o f E M G activity. In man, the functional significance and mechanical effectiveness of the SL reflex, whose onset delay is consistent with a segmental, perhaps even monosynaptic, pathway is not well understood. The intrinsic stiffness of stretched muscles is often considered more important in providing an early load resistance because little force seems to be recruited by SL reflexes 7,1~ and because intrinsic stiffness is present from the very onset of stretchl,lk In contrast, in the cat, two phases o f muscle yielding, appearing in the responses to stretch of cat soleus muscle deprived of reflex action, can reduce force below its prestretch leveP °,14. This yielding, however, is smoothed out when spinal reflexes are left intact ~4. Other studies in the cat indicate that SL reflexes not only provide compensation for the intrinsic muscle non-linearities underlying yielding, but also recruit substantial force to resist sudden muscle stretchg,lz, ~5. SL reflex action, in the cat, ensures that the total (reflex plus intrinsic) force response, once stretch terminates, varies less as the initial force level is changed than does the intrinsic muscle responseg, 15. In this study, we report on stretch force responses in man which indicate that, just as in the cat, SL reflexes maintain the total force response approximately constant as initial force level varies. In addition we compare the mechanical effectiveness o f stretch and release responses in h u m a n triceps surae muscles and cat soleus muscles. Muscle stretch which terminated before force was recruited by reflex action was employed. It was then possible to observe force changes associated with muscle yielding separate in time from those caused by SL reflex action. 0006-8993/82/0000-0000/$02.75 © Elsevier Biomedical Press
160 Experiments were carried out on 4 normal subjects (age range 29 37 years). During the experiments subjects were comfortably seated with the knee flexed 110 and the bare right foot strapped onto a platform which could be rotated about an axis colinear with the ankle joint. The rotations. 1-14 ° amplitude, duration 56 ms. were applied by a servo-controlled torque motor which otherwise held the foot isometrically. Each rotation started from 88 ° of ankle flexion. Subjects were asked to maintain :t constant plantar-flexion torque on the platform (measured with a strain gauge s)stem and displayed to the subject as torque about the ankle joint) prior to each rotation bx contracting the triceps surae muscles (TS). Surface EMG signals were recorded differ-
TIBIALIS
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Fig. 1, Incremental 'muscle' force responses to stretch (A) and release (B) of human triceps surae muscles. Each record is the average of 10 responses at each of 3 prior force levels. The records are taken from the same subject and aligned with the onset of the torque motor c o m m a n d . M u s c l e force ts equal to the recorded torque with inertial reaction torques removed. For ease of comparison the baselines of force records at 6. 12 and 14 N m have been aligned. The corresponding E M G records are shifted from alignment with absolute zero activity (marked with a s h o r t horizontal bar ~. For a p rior force of 6 N m the m a x i m m n force response due to intrinsic muscle stiffness, and the total force produced at 120 ms by intrinsic a n d reflex components of the stretch reflex, are marked with vertical bars. Arrows m a r k the onset of reflex changes in E M G activity. Latencies were measured from the onset of platform rotation.
161
entially from soleus (SOL) and tibialis anterior (TA) muscles with pairs of silver-silver chloride electrodes, then full-wave rectified and smoothed. Under these experimental conditions only small electrical potentials were recorded from the TA electrodes prior to each rotation (Fig. 1). Prior co-contraction of TA was therefore weak. Thus a contribution of TA intrinsic muscle stiffness to torque responses was presumed negligible. Inertial reaction torques were removed from the measured torque responses by subtracting away the product of a constant, proportional to the moment of inertia of the foot, and the measured platform acceleration. The constant was set equal to the ratio of peak acceleration and the local torque peak (of amplitude about 3 Nm and removed in Fig. 1) which occurred some 2-4 ms after peak acceleration, i.e. at the first inflection of ankle torque in Fig. I. The result of this subtraction is termed 'muscle force' hereafter. Because the torque motor completely resisted a subject's efforts to rotate the foot, platform accelerations (and therefore inertial reaction corrections to torque records) only occurred during angle changes commanded by the experimenter and not after ankle angle reached a plateau value. A rapid dorsiflexion of the foot stretching TS resulted in a pattern of EMG activity in SOL which included a SL component at 38, 40, 42 and 43 ms (mean values for the 4 subjects, n -= 30, 10.9 ° amplitude), and a medium latency (ML) component at 125, 115. 151 and 131 ms respectively (Fig. 1A shows one subject's responses). All latencies were measured from the onset of platform rotation. Subjects were instructed to increase force rapidly by contracting TS once a perturbation started. Thus, a longer latency voluntarily activated E M G component contributed at a later stage to existing M L activity 13. As other investigators 5 have also noted, SL and M L activity had similar onset times for lateral gastrocnemius and no reflex EMG activity was observed in TA on stretching TS. Prior to SL reflex EMG activity in SOL, muscle force rose rapidly following stretch onset and then began to yield steeply as the foot was decelerated. When the SL EMG response is reduced to 1 0 ~ of its normal amplitude by ischemia, yielding continues until force is equal to 50 ~ of the peak force response at the yield point:L Given this latter information, the delayed arrival of force recruited by SL reflex, some 20 ms after the onset of SL EMG activity, may be described as reversing the yielding by adding force to the ongoing intrinsic mechanical response (Fig. IA). Force, following the reversal of yielding, then continued to increase but tended to level off just prior to ML EMG activity. Changes brought about by an increase in the prior force level are observed in Fig. I A. Although the maximum response at the yield point increases, the force following the reversal of yielding tends to rise less steeply as prior force level increased. The force just prior to the onset of the M L force response, varied less as initial force was changed than did the mechanical response at the yield point. Fig. 2 illustrates this effect as here the maximum force at the yield point and the force at 120 ms (corresponding to the vertical bars on the force response to stretch at 6 Nm in Fig. 1A) are compared for 3 magnitudes of muscle stretch at 3 initial force levels. The force at 120 ms was chosen for comparison since it is just prior to the earliest M L force response and, based on electrical stimulation of soleus muscle efferents aT, at this time
162 A:
NTRINSIC FORCE RESPONSE AT YIELD POINT
B
TOTAL (REFLEX PLUS INTRINSIC) FORCE RESPONSE AT 120 ms FROM
ROTATION ONSET Nnq
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Fig. 2. Comparison of intrinsic force at the yield point with total (reflex plus intrinsicj force at 120 ms. The force at the yield point and at 120 ms were measured for 3 different prior force levels and 3 amplitudes of dorsiflexion: 2.9, 6.9 and 10.9°. Data for two subjects are illustrated, filled symbols for one subject, open for the other. Each data point is the average value from 10 responses. point the 'twitch' contraction elicited by the SL E M G response should be peaking. Intrinsic muscle force, represented by the force at yielding (Fig, 2A), increased with force level and with the magnitude of stretch (see numbers in Fig. 2 indicating stretch amplitude). 2 and 8 Nm are approximately equal to 8 and 32% of the maximum force which was developed tonically by our subjects. Fig. 2B, however, shows that the force at 120 ms, which represents the combined intrinsic and SL reflex forces, changed less with force level. When these force values are considered as local dynamic stiffness by dividing by stretch amplitude, it was found that the largest stiffness values occurred for a muscle stretch amplitude close to the estimated short range elastic limit of soleus in man 6,16. Strictly, we should compare the force at 120 ms in the presence of the SL reflex with the force at 120 ms when the reflex is absent, and not with the force at the yield point before the onset of the reflex. To do so in human subjects, however, would require at least 9 experiments per subject under painful ischemic conditions to yield data for comparison with that shown in Fig. 2A. Experimental data obtained under ischemic conditions with a stretch amplitude of 6.9 ° at a prior force level of 8 Nm indicate that the force at 120 ms is 50% of that at the yield point 3. If the scaling procedure adopted by other investigators 14 is applied to the results in Fig. 2A, i.e. all 6.9 ° values scaled by 0.5. the results still indicate that the total (reflex plus intrinsic) force response varied less, as initial force level changed, than the underlying intrinsic mechanical response. According to one definition of SL load compensation we employed, SL load compensation occurs when SL activity recruits sufficient force to bring total force
163 above the level required to compensate for muscle yielding. A SL force response could then be classified as load compensatory when, for example, the force developed by 120 ms exceeded the force at the yield point. If corresponding points are examined in Fig. 2A and B, the force at 120 ms exceeds the maximum intrinsic force on average by 26 ~,, and in several cases is less than the maximum intrinsic force (e.g. for 6.9 ° stretch at 8 Nm). This result indicates that SL load compensation, as defined above, is weak in human TS muscles. A plantar flexion of the foot, releasing TS, produced little EMG activity in SOL prior to 120 ms (Fig. 1). The instructions to the subject were identical to those for dorsiflexion rotations, i.e. a rapid TS contraction was required. The activity which commenced a 120-130 ms in all subjects was preceded by a decrease in SOL EMG activity at 75-85 ms. Identical changes in EMG SOL activity were observed by Gottlieb and Agarwal z under similar experimental conditions. Inconsistently, but generally for rotations over 6 °, a ML activity occurred at 80 ms in TA. 'Muscle force' recorded when TS was released differed in one major aspect from that recorded during stretch. Following the initial rapid force change the yielding towards prior force level was more gradual (Fig. 1B). A similar result was obtained for cat soleus muscle (ref. 15, Fig. 12). From comparisons with responses obtained under ischemic conditions 3 we concluded that the weak reflex activity following release tended to arrest this slow yielding after 80 ms (Fig. 1). Our results confirm previous reportsl,7,11,13 that in man the initial resistance to a load disturbance is provided by the intrinsic stiffness of activated muscle since it occurs before an EMG response. The dependence of the intrinsic response on the initial force level (Fig. 1) and the delayed reflex action produced force responses whose shape is almost identical to those recorded under comparable stretch conditions in the cat (ref. 15, Fig. 10). The similarity between our force responses prior to SL reflex action and those recorded from cat soleus muscle deprived of reflex action 9,12,~5 suggests that the early resistance to dorsiflexion about the human ankle joint is dominated by the intrinsic stiffness of active TS muscle fibers and not by passive elastic tissue. The mechanical resistance following yielding has, however, a pronounced asymmetric response to symmetric inputs. Corresponding to this non-linear behavior, reflex action recruits force to compensate for the rapid yielding during stretch, but little force during release. When combined with the intrinsic mechanical response the force recruited by SL reflex activity tends to maintain the total force response nearly constant once stretch has terminated, even as the initial force level increases (Fig. 1A). Presumably, this is accomplished by recruiting more force as yielding increases with initial force level. Thus, our results lend support to the original hypothesis of Nichols and Houk a4 that segmental reflexes compensate for intrinsic muscle non-linearities and maintain stiffness approximately constant. Finally, it should be noted that the rates of ankle dorsiflexion used in this study (peak 205 "/s for a 6.9 ° foot rotation) were purposely chosen so as to reveal intrinsic muscle mechanical properties. For the slower rates of dorsiflexion encountered during the stance phase of walking (25 °/s) s, it might be expected that SL reflex action
164 smoothly and completely compensates for muscle yielding to provide a steady elastic support
during the stance phase.
Disturbances
w h i c h t e s t T S m u s c l e stiffness a t
c o m p a r a b l e v e l o c i t i e s (22 °/s) p r o d u c e p e r f e c t l y c o m p e n s a t e d r e s p o n s e s in w h i c h f o r c e r e c r u i t e d b y S L reflexes is n o t o b s e r v a b l e a s a s e p a r a t e c o m p o n e n t L T h i s r e s e a r c h w a s s u p p o r t e d b y t h e Swiss N a t i o n a l S c i e n c e F o u n d a t i o n n o . 3.585.79 a n d 3.505.79. t h e D r . Eric S l a c k - G y r - F o u n d a t i o n , tion, and Deutsche Forschungsgemeinschaft
Grants
the Sandoz Founda-
G r a n t S F B 70.
1 Allum. J. H. J., Responses to load disturbances in human shoulder muscles: the hypothesis that one component is a pulse test information signal, Exp. Brain Res.. 22 [1975) 307 -326. 2 Allure. J. H. J.. Observations on the control of human ankle position by stretch reflexes. In A. Taylor and A. Prochazka (Eds.), Muscle Receptors and Movement. MacMillan, London. 1981. pp. 325-337. 3 Allum. J. H. J., Mauritz, K.-H and V6gele, H., The mechanical effectiveness of short latency reflexes in human triceps surae muscles revealed by ischaemia and vibration, submitted. 4 Ghez, C. and Shinoda. Y.. Spinal mechanisms o f the functional stretch reflex, Exp. Bruin Re,~.. 32 (1978) 55-68. 5 Gottlieb, G. L. and Agarwal, G. C., Response to sudden torques about ankle in man. II. Postmyotatic reactions. J. Neurophysiol., 43 (1980) 86-101. 6 Gurfinkel. V. S.. Lipshits, M. I., Mori, S. and Popov. K. E.. The state of stretch reflex during quiet standing in man. In S. Homma IEd.I. Understanding the Stretch Reflex, Progress in Brain Research. Vol. 44, Elsevier, North-Holland, Amsterdam, 1976, pp. 473~,86. 7 Hammond. P. H.. An experimental study of servoaction in human muscular control. In 3rd Int. Congr. Med. Electronics, 1960, pp. 190-199. 8 Herman. R., Wirta, R., Bampton, S. and Finley, F. R., Human solutions for locomotion. In R. M. Herman, S. Grillner, P. S. G. Stein and D. G. Stuart (Eds.). Neural Control ~f Locomotion. Plenum, New York, 1976, pp. 13-49. 9 Hoffer. J. A. and Andreassen. S., Regulation of soleus muscle stiffness in premammillary cats: intrinsic and reflex components. J. Neurophysiol., 45 (1981) 267-285. I 0 Joyce, G. C., Rack, P. M. H. and Westbury, D. R.. The mechanical properties of cat soleus muscle during controlled lengthening and shortening movements, J. Physiol. (Lond.). 204 (1969~ 461 4 7 4 . 11 Marsden, C. D., Merton. P. A. and Morton, H. B., The sensory mechanism of servo action in human muscle. J. Physiol. (Lond.). 265 (1977) 521-535. 12 Matthews, P. B. C., The dependence of tension upon extension in the stretch reflex of the soleus muscle of the decerebrate cat, J. Physiol. (Lond.). 147 (1959} 521 546. 13 Melvill-Jones, G. and Watt. D. G. D.. Observations on the control of stepping and hopping movements in man, J. Physiol. (Lond.), 219 (1971) 709-727. 14 Nichols. T. R. and Houk. J. C., Reflex compensation for variations in the mechamcal properties of a muscle, Science. 181 (1973) 182-184. 15 Nichols. T. R. and Houk, J. C.. Improvement in linearity and regulation of stiffness that results from actions of the stretch reflex. J. Neurophysiol.. 39 (t976) 119-142. 16 Rack, P. M. H. and Westbury, D. R.. The short range stiffness of active mammalian muscle and its effect on mechanical properties, J. Physiol. {Lond.), 240 (1974) 331-350. 17 Stein, R. B. and Bawa, P., Reflex responses of human soleus muscle to small perturbations. J. Neurophysiol., 39 (1976) 1105-t116. 18 Tracey, D. J., Watsmley, B and Brinkman, J.. 'Longqoop' reflexes can be obtained in spinal monkeys, Neurosci. Lett.. 18 (1980) 59--65.
159
Stiffness regulation provided by short-latency reflexes in human triceps surae muscles
J. H. J. ALLUM, K.-H. MAURITZ and H. VOGELE Brain Research Institute, August-Forel-Strasse 1, CH-8029 Zurich (Switzerland) and (K.-H.M. and H.V.) Department of Neurology, University of Freiburg, Freiburg (F.R.G.)
(Accepted November 12th, 198l) Key words: stretch reflex - - muscle stiffness - - triceps surae muscles - - human
The triceps surae muscles of normal human subjects were rapidly stretched and released by rotating the foot about the ankle joint with a torque motor. Following the initial intrinsic resistance, the yielding observed in incremental force records was more rapid for stretch than for release responses. Short-latency EMG responses elicited by stretch recruit force, to compensate for the yielding and to maintain the total (intrinsic plus reflex) resistance constant as the prior force level changes. Spinal stretch reflexes produce at least two burst of reflex E M G activity in a stretched muscle4, is. The most distinct, the short-latency (SL) reflex, is characterized by a highly synchronized burst o f E M G activity. In man, the functional significance and mechanical effectiveness of the SL reflex, whose onset delay is consistent with a segmental, perhaps even monosynaptic, pathway is not well understood. The intrinsic stiffness of stretched muscles is often considered more important in providing an early load resistance because little force seems to be recruited by SL reflexes 7,1~ and because intrinsic stiffness is present from the very onset of stretchl,lk In contrast, in the cat, two phases o f muscle yielding, appearing in the responses to stretch of cat soleus muscle deprived of reflex action, can reduce force below its prestretch leveP °,14. This yielding, however, is smoothed out when spinal reflexes are left intact ~4. Other studies in the cat indicate that SL reflexes not only provide compensation for the intrinsic muscle non-linearities underlying yielding, but also recruit substantial force to resist sudden muscle stretchg,lz, ~5. SL reflex action, in the cat, ensures that the total (reflex plus intrinsic) force response, once stretch terminates, varies less as the initial force level is changed than does the intrinsic muscle responseg, 15. In this study, we report on stretch force responses in man which indicate that, just as in the cat, SL reflexes maintain the total force response approximately constant as initial force level varies. In addition we compare the mechanical effectiveness o f stretch and release responses in h u m a n triceps surae muscles and cat soleus muscles. Muscle stretch which terminated before force was recruited by reflex action was employed. It was then possible to observe force changes associated with muscle yielding separate in time from those caused by SL reflex action. 0006-8993/82/0000-0000/$02.75 © Elsevier Biomedical Press
160 Experiments were carried out on 4 normal subjects (age range 29 37 years). During the experiments subjects were comfortably seated with the knee flexed 110 and the bare right foot strapped onto a platform which could be rotated about an axis colinear with the ankle joint. The rotations. 1-14 ° amplitude, duration 56 ms. were applied by a servo-controlled torque motor which otherwise held the foot isometrically. Each rotation started from 88 ° of ankle flexion. Subjects were asked to maintain :t constant plantar-flexion torque on the platform (measured with a strain gauge s)stem and displayed to the subject as torque about the ankle joint) prior to each rotation bx contracting the triceps surae muscles (TS). Surface EMG signals were recorded differ-
TIBIALIS
ANT
SURFACE SOLEUS SURFACE
EMG
/
I
EMG 4 i
.j'k
I
12Nm --
~Nm ,/
'
1
'
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'2
f
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I ANGULAR,'ACCELERATION "MUSCLE"FORCE i
ANKLEANGLE (690
/ / , ~
_
/
MU5 C L E " / / f / I F ~ c E # /
I~Nm 10Nm
'E"I 50
0
50
....... 100
150
200 250m,~
- 50
(
50
t0
iBO
~0(
~'50 r~
Fig. 1, Incremental 'muscle' force responses to stretch (A) and release (B) of human triceps surae muscles. Each record is the average of 10 responses at each of 3 prior force levels. The records are taken from the same subject and aligned with the onset of the torque motor c o m m a n d . M u s c l e force ts equal to the recorded torque with inertial reaction torques removed. For ease of comparison the baselines of force records at 6. 12 and 14 N m have been aligned. The corresponding E M G records are shifted from alignment with absolute zero activity (marked with a s h o r t horizontal bar ~. For a p rior force of 6 N m the m a x i m m n force response due to intrinsic muscle stiffness, and the total force produced at 120 ms by intrinsic a n d reflex components of the stretch reflex, are marked with vertical bars. Arrows m a r k the onset of reflex changes in E M G activity. Latencies were measured from the onset of platform rotation.
161
entially from soleus (SOL) and tibialis anterior (TA) muscles with pairs of silver-silver chloride electrodes, then full-wave rectified and smoothed. Under these experimental conditions only small electrical potentials were recorded from the TA electrodes prior to each rotation (Fig. 1). Prior co-contraction of TA was therefore weak. Thus a contribution of TA intrinsic muscle stiffness to torque responses was presumed negligible. Inertial reaction torques were removed from the measured torque responses by subtracting away the product of a constant, proportional to the moment of inertia of the foot, and the measured platform acceleration. The constant was set equal to the ratio of peak acceleration and the local torque peak (of amplitude about 3 Nm and removed in Fig. 1) which occurred some 2-4 ms after peak acceleration, i.e. at the first inflection of ankle torque in Fig. I. The result of this subtraction is termed 'muscle force' hereafter. Because the torque motor completely resisted a subject's efforts to rotate the foot, platform accelerations (and therefore inertial reaction corrections to torque records) only occurred during angle changes commanded by the experimenter and not after ankle angle reached a plateau value. A rapid dorsiflexion of the foot stretching TS resulted in a pattern of EMG activity in SOL which included a SL component at 38, 40, 42 and 43 ms (mean values for the 4 subjects, n -= 30, 10.9 ° amplitude), and a medium latency (ML) component at 125, 115. 151 and 131 ms respectively (Fig. 1A shows one subject's responses). All latencies were measured from the onset of platform rotation. Subjects were instructed to increase force rapidly by contracting TS once a perturbation started. Thus, a longer latency voluntarily activated E M G component contributed at a later stage to existing M L activity 13. As other investigators 5 have also noted, SL and M L activity had similar onset times for lateral gastrocnemius and no reflex EMG activity was observed in TA on stretching TS. Prior to SL reflex EMG activity in SOL, muscle force rose rapidly following stretch onset and then began to yield steeply as the foot was decelerated. When the SL EMG response is reduced to 1 0 ~ of its normal amplitude by ischemia, yielding continues until force is equal to 50 ~ of the peak force response at the yield point:L Given this latter information, the delayed arrival of force recruited by SL reflex, some 20 ms after the onset of SL EMG activity, may be described as reversing the yielding by adding force to the ongoing intrinsic mechanical response (Fig. IA). Force, following the reversal of yielding, then continued to increase but tended to level off just prior to ML EMG activity. Changes brought about by an increase in the prior force level are observed in Fig. I A. Although the maximum response at the yield point increases, the force following the reversal of yielding tends to rise less steeply as prior force level increased. The force just prior to the onset of the M L force response, varied less as initial force was changed than did the mechanical response at the yield point. Fig. 2 illustrates this effect as here the maximum force at the yield point and the force at 120 ms (corresponding to the vertical bars on the force response to stretch at 6 Nm in Fig. 1A) are compared for 3 magnitudes of muscle stretch at 3 initial force levels. The force at 120 ms was chosen for comparison since it is just prior to the earliest M L force response and, based on electrical stimulation of soleus muscle efferents aT, at this time
162 A:
NTRINSIC FORCE RESPONSE AT YIELD POINT
B
TOTAL (REFLEX PLUS INTRINSIC) FORCE RESPONSE AT 120 ms FROM
ROTATION ONSET Nnq
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~J-'~ 109°
A~
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Fig. 2. Comparison of intrinsic force at the yield point with total (reflex plus intrinsicj force at 120 ms. The force at the yield point and at 120 ms were measured for 3 different prior force levels and 3 amplitudes of dorsiflexion: 2.9, 6.9 and 10.9°. Data for two subjects are illustrated, filled symbols for one subject, open for the other. Each data point is the average value from 10 responses. point the 'twitch' contraction elicited by the SL E M G response should be peaking. Intrinsic muscle force, represented by the force at yielding (Fig, 2A), increased with force level and with the magnitude of stretch (see numbers in Fig. 2 indicating stretch amplitude). 2 and 8 Nm are approximately equal to 8 and 32% of the maximum force which was developed tonically by our subjects. Fig. 2B, however, shows that the force at 120 ms, which represents the combined intrinsic and SL reflex forces, changed less with force level. When these force values are considered as local dynamic stiffness by dividing by stretch amplitude, it was found that the largest stiffness values occurred for a muscle stretch amplitude close to the estimated short range elastic limit of soleus in man 6,16. Strictly, we should compare the force at 120 ms in the presence of the SL reflex with the force at 120 ms when the reflex is absent, and not with the force at the yield point before the onset of the reflex. To do so in human subjects, however, would require at least 9 experiments per subject under painful ischemic conditions to yield data for comparison with that shown in Fig. 2A. Experimental data obtained under ischemic conditions with a stretch amplitude of 6.9 ° at a prior force level of 8 Nm indicate that the force at 120 ms is 50% of that at the yield point 3. If the scaling procedure adopted by other investigators 14 is applied to the results in Fig. 2A, i.e. all 6.9 ° values scaled by 0.5. the results still indicate that the total (reflex plus intrinsic) force response varied less, as initial force level changed, than the underlying intrinsic mechanical response. According to one definition of SL load compensation we employed, SL load compensation occurs when SL activity recruits sufficient force to bring total force
163 above the level required to compensate for muscle yielding. A SL force response could then be classified as load compensatory when, for example, the force developed by 120 ms exceeded the force at the yield point. If corresponding points are examined in Fig. 2A and B, the force at 120 ms exceeds the maximum intrinsic force on average by 26 ~,, and in several cases is less than the maximum intrinsic force (e.g. for 6.9 ° stretch at 8 Nm). This result indicates that SL load compensation, as defined above, is weak in human TS muscles. A plantar flexion of the foot, releasing TS, produced little EMG activity in SOL prior to 120 ms (Fig. 1). The instructions to the subject were identical to those for dorsiflexion rotations, i.e. a rapid TS contraction was required. The activity which commenced a 120-130 ms in all subjects was preceded by a decrease in SOL EMG activity at 75-85 ms. Identical changes in EMG SOL activity were observed by Gottlieb and Agarwal z under similar experimental conditions. Inconsistently, but generally for rotations over 6 °, a ML activity occurred at 80 ms in TA. 'Muscle force' recorded when TS was released differed in one major aspect from that recorded during stretch. Following the initial rapid force change the yielding towards prior force level was more gradual (Fig. 1B). A similar result was obtained for cat soleus muscle (ref. 15, Fig. 12). From comparisons with responses obtained under ischemic conditions 3 we concluded that the weak reflex activity following release tended to arrest this slow yielding after 80 ms (Fig. 1). Our results confirm previous reportsl,7,11,13 that in man the initial resistance to a load disturbance is provided by the intrinsic stiffness of activated muscle since it occurs before an EMG response. The dependence of the intrinsic response on the initial force level (Fig. 1) and the delayed reflex action produced force responses whose shape is almost identical to those recorded under comparable stretch conditions in the cat (ref. 15, Fig. 10). The similarity between our force responses prior to SL reflex action and those recorded from cat soleus muscle deprived of reflex action 9,12,~5 suggests that the early resistance to dorsiflexion about the human ankle joint is dominated by the intrinsic stiffness of active TS muscle fibers and not by passive elastic tissue. The mechanical resistance following yielding has, however, a pronounced asymmetric response to symmetric inputs. Corresponding to this non-linear behavior, reflex action recruits force to compensate for the rapid yielding during stretch, but little force during release. When combined with the intrinsic mechanical response the force recruited by SL reflex activity tends to maintain the total force response nearly constant once stretch has terminated, even as the initial force level increases (Fig. 1A). Presumably, this is accomplished by recruiting more force as yielding increases with initial force level. Thus, our results lend support to the original hypothesis of Nichols and Houk a4 that segmental reflexes compensate for intrinsic muscle non-linearities and maintain stiffness approximately constant. Finally, it should be noted that the rates of ankle dorsiflexion used in this study (peak 205 "/s for a 6.9 ° foot rotation) were purposely chosen so as to reveal intrinsic muscle mechanical properties. For the slower rates of dorsiflexion encountered during the stance phase of walking (25 °/s) s, it might be expected that SL reflex action
164 smoothly and completely compensates for muscle yielding to provide a steady elastic support
during the stance phase.
Disturbances
w h i c h t e s t T S m u s c l e stiffness a t
c o m p a r a b l e v e l o c i t i e s (22 °/s) p r o d u c e p e r f e c t l y c o m p e n s a t e d r e s p o n s e s in w h i c h f o r c e r e c r u i t e d b y S L reflexes is n o t o b s e r v a b l e a s a s e p a r a t e c o m p o n e n t L T h i s r e s e a r c h w a s s u p p o r t e d b y t h e Swiss N a t i o n a l S c i e n c e F o u n d a t i o n n o . 3.585.79 a n d 3.505.79. t h e D r . Eric S l a c k - G y r - F o u n d a t i o n , tion, and Deutsche Forschungsgemeinschaft
Grants
the Sandoz Founda-
G r a n t S F B 70.
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