Journal of Physiology (1992), 447, pp. 563-573 With 5 figures Printed in Great Britain
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CHANGES IN THE STRETCH REFLEX OF THE HUMAN FIRST DORSAL INTEROSSEOUS MUSCLE DURING DIFFERENT TASKS
BY F. DOEMGES* AND P. M. H. RACK From the Department of Physiology, University of Birmingham, Birmingham B15 2TT
(Received 7 May 1991) SUMMARY
1. Subjects flexed the interphalangeal joint of the index finger against a lever which was mounted on the shaft of a torque motor. 2. There were two different tasks. In one, the subject attempted to maintain a constant finger position in the face of changing forces, whereas in the other the subject attempted to maintain a constant force while the motor moved the lever. 3. Each of the tasks was interrupted by ramp extensions. These evoked stretch reflexes which were recorded in the first dorsal interosseous (FDI) muscle electromyogram (EMG). 4. Long-latency (55-90 ms) reflex responses were larger during the 'maintain position' task than during the 'maintain force' task, although the ramp extensions began from a similar finger position, a similar flexing force, and with a similar amount of FDI EMG activity. 5. It is concluded that the nature of the task has an effect on the magnitude of the long-latency stretch reflex. INTRODUCTION
When a muscle is extended, stretch reflexes may generate a resisting force which impedes the extension, and thereby tends to prevent changes in limb position. In many circumstances this is a useful response, but position is not the only parameter which we may need to control. It is common experience that we have fine control of the pressure of our finger grip, and when we handle delicate objects, the control of force may often be more important than the exact position of the fingers (e.g. Johansson & Westling, 1988). To maintain a constant force, the fingers should absorb small perturbations, allowing movement to occur without alterations in force; under these circumstances a stretch reflex would be positively unhelpful. Hore, McCloskey & Taylor (1990) have shown that subjects who are attempting to maintain the position of the wrist joint against some pre-determined force resist movements with a greater stiffness than when they are attempting to maintain the same force but to allow movement. This difference occurs with movements which are too small and too slow to be consciously perceived, and it remains after the extensors *
Present address: Alfried Krupp Krankenhaus, Alfried-Krupp-Strasse 21, 4300 Essen,
Germany. MS 9372
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F. DOEMGES AND P. M. H. RACK
have been paralysed. The difference cannot therefore be attributed to co-contraction of antagonist muscles, and it is assumed to arise from task-related changes in the magnitude of a reflex response to the movement. The response to an imposed joint movement is affected by the intentions of the subject. When subjects have been instructed to resist a movement or to meet it with an opposite movement, muscles respond to extension more vigorously and more immediately than when they are instructed to 'let go' (e.g. Hammond, 1956, 1960; Lee & Tatton, 1975; Crago, Houk & Hasan, 1976; Evarts & Granit, 1976; Marsden, Merton & Morton, 1976; Marsden, Merton, Morton, Adam & Hallett, 1978; Colebatch, Gandevia, McCloskey & Potter, 1979; Rothwell, Traub & Marsden, 1980; Loo & McCloskey, 1985; Goodin, Aminoff & Shih, 1990). However, the results of these various investigations were not all the same, and it is still uncertain whether parts of this task-related response should be regarded as a pre-set reflex (Hammond, 1956, 1960), or whether the response should be described as a 'voluntary response' (Marsden et al. 1978) or a 'triggered response' (Crago et al. 1976). In those investigations, subjects who were maintaining a force, maintaining a position, or executing some preplanned movement were instructed to respond to a perturbation in different ways. We shall describe experiments in which subjects were engaged in two different tasks, a 'maintain position' task and a 'maintain force' task, but were instructed not to react to the imposed perturbation; we found that the same perturbation then provoked different responses, and these differences appeared so soon after the movement that they must be regarded as task-related alterations in long-latency stretch reflexes. In a rather similar experiment, Akazawa, Milner & Stein (1983) found a more vigorous flexor pollicis longus stretch reflex during a 'maintain position' task than during a 'maintain force' task. However, differences in the background muscle activation accounted for much of the reflex difference, though the authors did note that attempts to control an unstable load increased the reflex activity by more than it increased the muscle activation. Some of these results have already been published in abstract form (Doemges & Rack, 1991). METHODS
Experiments were carried out on nine normal adults aged 27-62 years, with their informed consent and with the permission of the Local Ethical Committee; four were male, five female. The subject was seated with the right forearm supported in a horizontal position, and a strap lightly restraining the wrist. The index finger and thumb gripped a pair of levers (Fig. 1A); the thumb lever was rigid, but the finger lever was attached to the shaft of a servo-controlled motor. The distance of the hand from the lever was such that the interphalangeal joints remained extended, and flexing movements occurred at the metacarpo-phalangeal joint. In that position the first dorsal interosseus muscle (FDI) flexes the interphalangeal joint, and electromyograms (EMG) were recorded from that muscle by means of silver disc electrodes taped to the skin. In some experiments the interphalangeal joints of the index finger were splinted in the extended position; this additional fixation did not affect either the performance of the task, or the response to imposed movements, so it was not usually done. The motor A printed circuit motor (Printed Motors Ltd, G9M4T) was modified; the brushes were removed and four wires were attached to chosen parts of the armature. These wires were taken downward
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through a hollowed main shaft, and brought out as flying leads. The motor was energized through these leads, but the signal from an angular position transducer (see below) was used to modulate the supply to the different armature connections in such a way that any chosen input signal generated the same torque whichever part of the armature lay between the magnetic poles. With this arrangement, friction from the brushes was avoided, and torques of up to 0-8 N m were available over the whole 90 deg range.
A
Printed circuit motor
Force
position
EMG
Fig. 1. The experimental arrangement. For explanation see the text.
Angular position The angular position was detected by a transducer (Thomson C. S. F. 'Transcosin', with Analog Devices IS40 resolver) attached to the lower end of the motor shaft. This was sensitive to movements of 0-02 deg.
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F. DOEMGES AND P. M. H. RACK
Force transducer The finger lever was mounted on a subsidiary spindle co-axial with the motor shaft. Torque was transmitted between the motor and this spindle by a beryllium-copper link, on which were mounted semiconductor 'strain gauges' (Kulite Sensors Ltd). When arranged in a bridge circuit, these gave an electrical signal proportional to torque. The force transducer and the lever together yielded by less than 0 04 deg N-1. Servo-control The motor and driving electronics described above served as the actuator for two different control mechanisms. Signals from the position transducer could be used in a conventional position servo-control mechanism, or alternatively, signals from the force transducer could be used in servocontrol of force. It was possible to switch between these two servo-mechanisms, but the transition between force and position control can only be smoothly made when the position, the force, and the motor drive signals are precisely matched to each other. Otherwise, switching results in abrupt and disturbing transients.
Computer control A digital computer (Digital Equipment PDP 11/53) controlled the experiments (Fig. IB). The input to the servo-systems could be from either a prerecorded magnetic tape or the computer's analog output (updated at 0-5 ms intervals); each of these signals could be used to control either lever position or motor force. Smooth transitions between these different possibilities were achieved by computer programs which operated the analog switches only when the tape signal, the actual force and the lever position were appropriately matched to each other. Rectified electromyograms, position signals and force signals were sampled at 2 ms intervals (12 bit resolution) and stored on disc for subsequent analysis. Experimental procedure The subjects carried out two different tasks. In the first task the motor controlled the position of the lever beneath the index finger and the subject was asked to maintain a constant grip force of 1-5 N (which was less than 10 % of maximal) while the lever moved in a pseudo-random manner under the control of a prerecorded tape (see below). In the other task the subject attempted to maintain a constant position while the motor modulated the force in a pseudo-random way around a mean value of 1-5 N. When the subject was performing one or other of these tasks, and had brought the position or force close to the target value, the experimenter closed a switch which initiated the testing routine. After some random interval the computer took charge of the motor, and (acting through its position-controlling servo) imposed a ramp movement of 8 mm at 300 mm s-' (see Fig. 2 C and D) which started from precisely the position that the joint had then reached. After the ramp was complete the joint was held in the extended position for a further 375 ms. In order that responses obtained during the two tasks could be compared, it was important that the reflexes were tested when the flexing force and the finger position were close to the chosen values. The computer was so programmed that the test movements only occurred when the finger was within 3 mm of the desired position, and the force was within + 15% of the target value. However, the subject had control of either force or position and needed some help to keep it within the target area. When he or she was maintaining position, a low-pass filtered version of the position signal (time constant approximately 2 s) was therefore displayed on an oscilloscope, and a similar force signal was provided when he or she was maintaining force. This visual display was blanked out during the ramp movements. The timing of the perturbations involved a random delay, but it also depended on how well the subject maintained the force or position. The interval between perturbations was never less than 5 s, and it might be as much as 30 s. A set of thirty-two perturbations usually took about 10 min, but subjects were free to rest for as long as they chose between individual tests. In practised subjects the intervals were similar during the two different tasks. In some early experiments, ramp flexion movements were used as well as extensions, and these were mixed together in random order. In later experiments, only extensions were used. The tape recording which generated the pseudo-random movements and forces consisted of a
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mixture of three sinusoids of unrelated frequencies all of which were less than 0 3 Hz. This input gave movements of up to +3 mm, or force changes of up to +0 7 N. In practice, this pattern of movements or forces could not be predicted. even by subjects who knew how they had been generated. Position, force and rectified EMIG records were collected for a period of 200 ms before and 400 ms after the beginning of each ramp extension. These records could later be displayed individually (Fig. 2C and D)! or after averaging (Figs 3-5). RESULTS
The two tasks are illustrated in Fig. 2A and B. In Fig. 2A the subject gripped the levers and attempted to maintain a constant mean flexing force of 15 N (upper trace), while the motor varied the lever position (lower trace). In Fig. 2B the subject attempted to hold the finger in the same position while the motor varied the force. These records illustrate the force and position control that we could expect from a practised subject; in neither case was the control perfect, some force changes did occur in Fig. 2A, and some position changes in Fig. 2B. Motor controls position
A
C
Subject maintains force N
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_ B
N
f
]10 mm
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Motor controls force Subject maintains position
_ | ~EMG
E_Force -
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5s ~~~~~~~~~0.5 s 15s 1105 Fig. 2. Oscilloscope photographs to show finger positions (lowest traces) and forces (above). In A and C the subject was attempting to maintain a constant force of 1-5 N (approximately 0-12 N m at the interphalangeal joint) against a moving lever, but in B and D he was attempting to maintain a constant position in spite of changing force. Records C and D show the responses (including the FDI EMG) during an imposed lengthening movement of 8 mm at 300 mm s-' (for an average length of index finger this is equivalent to 6 5 deg of movement at the metacarpo-phalangeal joint at 250 deg s-1); note faster time base.
The two tasks felt quite different even though the actual position of the finger, and the forces upon it, were similar. In the 'maintain force' task the subjects felt they were gripping something which was firm and unyielding, but which nevertheless expanded and contracted between the finger and thumb. By contrast, the 'maintain position' task could be compared to gripping a soft balloon, in which the pressure was gradually increased and decreased. The 'maintain force' task did not come naturally to all subjects, and some of them practised for a long period (1 or 2 h in a number of different sessions) before they felt
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F. DOEMGES AND P. M. H. RACK they had acquired the 'knack' of doing it. The 'maintain position' task seemed easier, but on first attempts many subjects stiffened the joints of the wrist and hand with palpable co-contraction of antagonist muscles. However, most subjects relaxed as they became more used to the task. A
B
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C
I
50 yV]
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Position 0
50 100 150 Time (ms)
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Fig. 3. Averaged position force and rectified EMGs recorded in a subject who was attempting to maintain constant force (A) and to maintain constant position (B). Each record is the averaged response to sixty-four extension movements (8 mm at 300 mm s-1). The 128 extensions were in four sets of thirty-two, the 'maintain position' and 'maintain force' tasks being alternated to reduce any effect of habituation or fatigue. In C the position and EMG records of A and B have been superimposed.
The oscilloscope display of the quantity to be controlled (force or position) was heavily low-pass filtered so that it did not help the subjects to correct for the fluctuations imposed by the tape recorder (in fact the filter introduced phase delays which made the signals positively unhelpful). Subjects found that they were best able to perform the tasks when they had learned to disregard small fluctuations of the visual display, and to rely on what their fingers 'felt' to be doing.
The response to abrupt extension movements While the subjects were attempting to 'maintain force' or to 'maintain position', the excitability of the FDI stretch reflex was examined by randomly timed extension movements of the finger (8 mm at 300 mm s-1). Figure 2C and D shows responses to these extensions during the same experiment as Fig. 2A and B (note faster time base). Throughout the 'maintain force' task (Fig. 2A and C) the motor was in control of finger position, and the imposed extension merely continued this situation. However, in the 'maintain position' task (Fig. 2B and D), the motor was at first in control of force, but then for the imposed extension movement and the subsequent 375 ms, it took charge of position. The subject could not prevent the extension, and the instruction was therefore to 'maintain the finger position, but do not intervene when it is forcibly disturbed'. (Attempts to respond to the extensions in different ways did not, in fact, alter EMG responses in the first 100 ms.) Figure 3 shows averaged responses of one subject to sixty-four extension movements during the 'maintain force' task (Fig. 3A) and sixty-four during the
TASK-DEPENDENT HUMAN STRETCH REFLEXES 569 'maintain position' task (Fig. 3B). The imposed extension was followed by a burst of EMG activity which began about 55 ms from the beginning of extension and lasted until about 90 ms. However, this reflex response was notably larger when the subject was attempting to maintain position (Fig. 3B), than when she was attempting to B
A Subject maintains force
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Subject maintains position
100 jV]J
l l
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m
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!
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0 50 100 150 50 100 150 Time (ms) Time (ms) Fig. 4. As for Fig. 3, but from a different subject. Each record is the averaged response to ninety-six extensions.
0
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'maintain force' (Fig. 3A). This difference between reflex EMG responses during the two tasks is more clearly seen when the two records are superimposed (Fig. 3 C). This task-related difference between the EMG responses at 50-90 ms (Fig. 3C) occurred consistently in all the subjects who had practised the task, and in some subjects it was obvious in the responses to individual extensions (as in Fig. 2C and D). However, there were some subjects in whom the reflex response also included earlier components which began about 30 ms after the onset of movement (Fig. 4). The rectified EMG records then included two peaks, the timings of which were similar to those reported by Noth, Podoll & Friedemann (1985) for the same muscle; these no doubt correspond to the fast-spinal and long-latency stretch reflexes which have been described for many other muscles (Hammond, 1960; Marsden et al. 1976). It was notable that when these early reflex components were present, they remained the same in both tasks, and it was only the latter (55-90 ms) components which decreased when the task was changed from 'maintain force' (Fig. 4A) to 'maintain position' (Fig. 4B). In this respect, the results differ from those of Kanosue, Akazawa & Fujii (1983), who concluded that the amplitudes of spinal stretch reflexes are also task dependent. In some subjects, the later reflex response was preceded by a brief decrease in the EMG signal without a preceding peak of fast-spinal reflex activity (Fig. 3). Presumably this dip in the record indicates the end of a fast-spinal response whose amplitude was too small, and whose onset too dispersed to appear as a significant peak in surface EMG.
The task-dependent differences in reflex response were seen when we compared attempts to maintain position against a changing force with attempts to maintain force against a changing position. When, however, the subject maintained force
F. DOEMGES AND P. M. H. RACK
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against a fixed lever, and then maintained position against a constant force, there was no significant alteration in the reflex responses. It is worth noting that subjects found these two static tasks similar to each other, and relatively easy to accomplish. During both of these static tasks there was a vigorous long-latency reflex response, similar to those seen when the subject was 'maintaining position' in the face of a changing force. In the present experiments it was only when subjects were maintaining a constant force against a moving lever that the long-latency stretch reflex was suppressed. It is notable that this was also the task which subjects found the most difficult.
A
B
Subject maintains force
Subject maintains position
100 MV]
1
3.0 Force (N)
10 mm Position 0
50 100 150 Time (ms)
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D
C
3.0 2.01 I
1.0 0
I
Ir
i
I
3.0
-
2.0
-
I I
T I ----I 50 100 150 0 50 100 150 0 Time (ms) Time (ms) Fig. 5. Averaged data from eight different subjects, using only experiments in which the EMG activity preceding the perturbation was equal in the two tasks. A-C are plotted in the same way as in Figs 3 and 4. For D the same EMG activity was expressed in terms of the preceding baseline level before averaging. The time scale starts with the first force
change.
I
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Co-activation of antagonist muscles When subjects were new to the tasks, their attempts to maintain a constant finger position were often accompanied by activation of other muscles of the wrist and hand. Contraction of antagonist muscles could have reduced the force of finger flexion, and the measurements of external force would not then give a reliable indication of the activation of the first dorsal interosseous muscle. It could be argued that the more powerful reflex activity in the 'maintain position' task was merely the accompaniment of a higher level of muscle activity. In order to avoid this complication, we have deliberately set aside experiments in which there was a different amount of FDI EMG activity in the two tasks. In Fig. 5 we show the average of all results obtained in experiments where the FDI activation was the same in both tasks (as judged from the rectified EMGs before the extension). Figure 5A-C shows that the reflex responses still differed from each other, confirming that the reflex was still task dependent even though the background EMG activity had been the same. Although Fig. 5A-C was constructed from records in which there was equal EMG activity in the 'maintain position' and 'maintain force' task, the absolute amounts of activity differed between subjects. After normalizing the results of individual subjects by expressing EMG activity in terms of the preceding EMG baseline level, these were averaged to give Fig. 5D. The standard error bars indicate that the EMG records differed significantly from each other in the time interval 68-86 ms after the first force change (the mean values are then separated by more than two standard errors). The integrated EMG activity in the time interval 55-90 ms was also measured for the averaged results of each subject. Student's paired t test confirmed the significant difference between the responses to the two tasks (P < 0.001). Although Fig. 5 compares records in which the levels of FDI activation were equal, the fingers were stiffer in the 'maintain position' than in the 'maintain force' tasks. In Fig. 5A the imposed movement was slightly smaller than in Fig. 5B, but it caused a larger rise in force; the differences are seen more clearly in Fig. 5 C. These changes in stiffness are visible in the first 40 ms, before there was time for any reflex force to develop. Presumably the 'maintain position' task involved some contraction of other flexors and extensors of the finger, even though the activity in the FDI had remained the same. DISCUSSION
There have been numerous descriptions of the responses of the flexor pollicis longus muscle to imposed extension movements of the thumb (see Marsden et al. 1976, 1978; Loo & McCloskey 1985). When the timing of the imposed movement was quite unpredictable, the EMG responses which occurred in the first 85 ms could not be modified in any consistent way by the prior intentions of the subject. After about 85 ms, the responses were indeed influenced by the subjects' intentions, but at that time voluntary responses could be expected anyway. It was therefore concluded that prior instructions have little effect on stretch reflex responses of this muscle, so long as the perturbing movement is quite unpredictable. The FDI has longer peripheral nerves than the flexor pollicis longus, and one would expect an even longer interval between the perturbation and any intentional
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modification of the response to it. However, the present results show that when subjects undertake different tasks, the FDI EMG is modified at 68 ms (Fig. 5), and sometimes appreciably earlier. This is considerably sooner than one would expect a voluntary response in so peripheral a muscle, and it must therefore be regarded as a reflex response which is task dependent. The task-dependent changes were appropriate; when it was necessary to maintain position and prevent movements, the reflex response was large, but during the 'maintain force' task, where movements were to be permitted without added resistance, the response was reduced. We conclude that subjects who are involved in a particular motor task alter their long-latency stretch reflexes in an appropriate way, whereas the mere instruction or intention to react in a particular way may not lead to consistent reflex changes. However, it is interesting to note that when a perturbation can be anticipated, the reflex response to it may be modified by the intentions of the subject (Rothwell et al. 1980; Goodin et al. 1990). The nervous system clearly has the capacity to alter the long-latency stretch reflex activity to suit a particular task, or in immediate anticipation of a movement (Gurfinkel, Kots, Krinskiy, Paltsev, Feldman, Tsetlin & Shik, 1971) or disturbance, but the present results do not support a suggestion that fast-spinal stretch reflexes are also task dependent (Kanosue, Akazawa & Fujii, 1983). Responses which occur after the minimum voluntary reaction time are very often described as 'voluntary responses', to distinguish them from stretch reflexes. This is a convenient though somewhat arbitrary distinction, since later components of a response may also occur without conscious thought; in fact, the 'reflex' reactions probably merge seamlessly into 'voluntary' response (Rack, 1981), without any clear dividing line. The following paper (Doemges & Rack, 1992) reports a task-dependent modification of stretch reflexes in wrist flexor muscles which persists after coactivation of other muscles has been prevented. The method used in that investigation enables the subject to 'maintain position' without the disrupting effect of imposed position ramps. The authors are grateful to Johannes Noth for his comments on the manuscript, and to Jane Arnold for technical assistance. The work was supported by a grant from the Medical Research Council, and F. D. received a grant from the Deutsche Forschungsgemeinschaft. REFERENCES
AKAZAWA, K., MILNER, T. E. & STEIN, R. B. (1983). Modulation of reflex EMU and stiffness in response to stretch of human finger muscles. Journal of Neurophysiology 49, 16-27. COLEBATCH, J. G., GANDEVIA, S. C., MCCLOSKEY, D. I. & POTTER, E. K. (1979). Subject instruction and long-latency reflex responses to muscle stretch. Journal of Physiology 292, 527-534. CRAGO, P. E., HOUK, J. C. & HASAN, Z. (1976). Regulatory actions of human stretch reflex. Journal of Neurophysiology 39, 925-935. DOEMGES, F. & RACK, P. M. H. (1991). Stretch reflexes diminish as normal human subjects learn to control the force of a precision grip. Journal of Physiology 435, 56P. DOEMGES, F. & RACK, P. M. H. (1992). Task-dependent changes in the response of human wrist joints to mechanical disturbance. Journal of Physiology 447, 575-585. EVARTS, E. V. & GRANIT, R. (1976). Relations of reflexes and intended movements. Progress in Brain Research 44, 1-14.
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GOODIN, D. S., AMINOFF, M. J. & SHIH, P.-Y. (1990). Evidence that long-latency stretch responses of the human wrist extensor muscle involve a transcerebral pathway. Brain 113, 1075-1091. GURFINKEL, V. S., KOTS, YA. M., KRINSKIY, V. I., PALTSEV, E. I., FELDMAN, A. G., TSETLIN, M. L. & SHIK, M. L. (1971). Concerning tuning before movement. In Models of Structural-functional Organization of Certain Biological Systems, ed. GELFAND, I. M., GURFINKEL, V. S., FOMIN, S. V. & TSETLIN, M. L., pp. 361-372 of English translation. MIT Press, Cambridge, MA, USA. HAMMOND, P. H. (1956). The influence of prior instruction to the subject on an apparently involuntary neuromuscular response. Journal of Physiology 182, 17-18P. HAMMOND, P. H. (1960). An experimental study of servo-action in human muscular control. In Proceedings of the 3rd Conference on Medical Electronics, pp. 190-199. Institution of Electrical Engineers, London. HORE, J., MCCLOSKEY, D. I. & TAYLOR, J. L. (1990). Task-dependent changes in gain of the reflex response to imperceptible perturbations of joint position in man. Journal of Physiology 429, 309-321. JOHANSSON, R. S. & WESTLING, G. (1988). Programmed and triggered actions to rapid load changes during precision grip. Experimental Brain Research 71, 72-88. KANOSUE, K., AKAZAWA, K. & Fujii, K. (1983). Modulation of reflex activity of motor units in response to stretch of a human finger muscle. Japanese Journal of Physiology 33, 995-1009. LEE, R. G. & TATTON, W. G. (1975). Motor responses to sudden limb displacements in primates with specific CNS lesions and in human patients with motor system disorders. Canadian Journal of Neurological Science 2, 285-293. Loo, C. K. C. & MCCLOSKEY, D. I. (1985). Effects of prior instruction and anaesthesia on longlatency responses to stretch in the long flexor of the human thumb. Journal of Physiology 365, 285-296. MARSDEN, C. D., MERTON, P. A. & MORTON, H. B. (1976). Servo action in the human thumb. Journal of Physiology 257, 1-44. MARSDEN, C. D., MERTON, P. A. MORTON, H. B., ADAM, J. E. R. & HALLETT, M. (1978). Automatic and voluntary responses to muscle stretch in man. In Cerebral Motor Control in Man: Long-loop Mechanisms, ed. DESMEDT, J. E., pp. 167-177. Karger, Basel. NOTH, J., PODOLL, K. & FRIEDEMANN, H.-H. (1985). Long-loop reflexes in small hand muscles studied in normal subjects and in patients with Huntington's disease. Brain 108, 65-80. RACK, P. M. H. (1981). Limitations of somatosensory feedback in control of posture and movement. In Handbook of Physiology, section 1, The Nervous System, vol. 2, Motor Control, ed. BROOKS, V. B. pp. 229-256. American Physiological Society, New York. ROTHWELL, J. C., TRAUB, M. M. & MARSDEN, C. D. (1980). Influence of voluntary intent on human long-latency stretch reflex. Nature 286, 496-498.
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CHANGES IN THE STRETCH REFLEX OF THE HUMAN FIRST DORSAL INTEROSSEOUS MUSCLE DURING DIFFERENT TASKS
BY F. DOEMGES* AND P. M. H. RACK From the Department of Physiology, University of Birmingham, Birmingham B15 2TT
(Received 7 May 1991) SUMMARY
1. Subjects flexed the interphalangeal joint of the index finger against a lever which was mounted on the shaft of a torque motor. 2. There were two different tasks. In one, the subject attempted to maintain a constant finger position in the face of changing forces, whereas in the other the subject attempted to maintain a constant force while the motor moved the lever. 3. Each of the tasks was interrupted by ramp extensions. These evoked stretch reflexes which were recorded in the first dorsal interosseous (FDI) muscle electromyogram (EMG). 4. Long-latency (55-90 ms) reflex responses were larger during the 'maintain position' task than during the 'maintain force' task, although the ramp extensions began from a similar finger position, a similar flexing force, and with a similar amount of FDI EMG activity. 5. It is concluded that the nature of the task has an effect on the magnitude of the long-latency stretch reflex. INTRODUCTION
When a muscle is extended, stretch reflexes may generate a resisting force which impedes the extension, and thereby tends to prevent changes in limb position. In many circumstances this is a useful response, but position is not the only parameter which we may need to control. It is common experience that we have fine control of the pressure of our finger grip, and when we handle delicate objects, the control of force may often be more important than the exact position of the fingers (e.g. Johansson & Westling, 1988). To maintain a constant force, the fingers should absorb small perturbations, allowing movement to occur without alterations in force; under these circumstances a stretch reflex would be positively unhelpful. Hore, McCloskey & Taylor (1990) have shown that subjects who are attempting to maintain the position of the wrist joint against some pre-determined force resist movements with a greater stiffness than when they are attempting to maintain the same force but to allow movement. This difference occurs with movements which are too small and too slow to be consciously perceived, and it remains after the extensors *
Present address: Alfried Krupp Krankenhaus, Alfried-Krupp-Strasse 21, 4300 Essen,
Germany. MS 9372
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F. DOEMGES AND P. M. H. RACK
have been paralysed. The difference cannot therefore be attributed to co-contraction of antagonist muscles, and it is assumed to arise from task-related changes in the magnitude of a reflex response to the movement. The response to an imposed joint movement is affected by the intentions of the subject. When subjects have been instructed to resist a movement or to meet it with an opposite movement, muscles respond to extension more vigorously and more immediately than when they are instructed to 'let go' (e.g. Hammond, 1956, 1960; Lee & Tatton, 1975; Crago, Houk & Hasan, 1976; Evarts & Granit, 1976; Marsden, Merton & Morton, 1976; Marsden, Merton, Morton, Adam & Hallett, 1978; Colebatch, Gandevia, McCloskey & Potter, 1979; Rothwell, Traub & Marsden, 1980; Loo & McCloskey, 1985; Goodin, Aminoff & Shih, 1990). However, the results of these various investigations were not all the same, and it is still uncertain whether parts of this task-related response should be regarded as a pre-set reflex (Hammond, 1956, 1960), or whether the response should be described as a 'voluntary response' (Marsden et al. 1978) or a 'triggered response' (Crago et al. 1976). In those investigations, subjects who were maintaining a force, maintaining a position, or executing some preplanned movement were instructed to respond to a perturbation in different ways. We shall describe experiments in which subjects were engaged in two different tasks, a 'maintain position' task and a 'maintain force' task, but were instructed not to react to the imposed perturbation; we found that the same perturbation then provoked different responses, and these differences appeared so soon after the movement that they must be regarded as task-related alterations in long-latency stretch reflexes. In a rather similar experiment, Akazawa, Milner & Stein (1983) found a more vigorous flexor pollicis longus stretch reflex during a 'maintain position' task than during a 'maintain force' task. However, differences in the background muscle activation accounted for much of the reflex difference, though the authors did note that attempts to control an unstable load increased the reflex activity by more than it increased the muscle activation. Some of these results have already been published in abstract form (Doemges & Rack, 1991). METHODS
Experiments were carried out on nine normal adults aged 27-62 years, with their informed consent and with the permission of the Local Ethical Committee; four were male, five female. The subject was seated with the right forearm supported in a horizontal position, and a strap lightly restraining the wrist. The index finger and thumb gripped a pair of levers (Fig. 1A); the thumb lever was rigid, but the finger lever was attached to the shaft of a servo-controlled motor. The distance of the hand from the lever was such that the interphalangeal joints remained extended, and flexing movements occurred at the metacarpo-phalangeal joint. In that position the first dorsal interosseus muscle (FDI) flexes the interphalangeal joint, and electromyograms (EMG) were recorded from that muscle by means of silver disc electrodes taped to the skin. In some experiments the interphalangeal joints of the index finger were splinted in the extended position; this additional fixation did not affect either the performance of the task, or the response to imposed movements, so it was not usually done. The motor A printed circuit motor (Printed Motors Ltd, G9M4T) was modified; the brushes were removed and four wires were attached to chosen parts of the armature. These wires were taken downward
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through a hollowed main shaft, and brought out as flying leads. The motor was energized through these leads, but the signal from an angular position transducer (see below) was used to modulate the supply to the different armature connections in such a way that any chosen input signal generated the same torque whichever part of the armature lay between the magnetic poles. With this arrangement, friction from the brushes was avoided, and torques of up to 0-8 N m were available over the whole 90 deg range.
A
Printed circuit motor
Force
position
EMG
Fig. 1. The experimental arrangement. For explanation see the text.
Angular position The angular position was detected by a transducer (Thomson C. S. F. 'Transcosin', with Analog Devices IS40 resolver) attached to the lower end of the motor shaft. This was sensitive to movements of 0-02 deg.
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F. DOEMGES AND P. M. H. RACK
Force transducer The finger lever was mounted on a subsidiary spindle co-axial with the motor shaft. Torque was transmitted between the motor and this spindle by a beryllium-copper link, on which were mounted semiconductor 'strain gauges' (Kulite Sensors Ltd). When arranged in a bridge circuit, these gave an electrical signal proportional to torque. The force transducer and the lever together yielded by less than 0 04 deg N-1. Servo-control The motor and driving electronics described above served as the actuator for two different control mechanisms. Signals from the position transducer could be used in a conventional position servo-control mechanism, or alternatively, signals from the force transducer could be used in servocontrol of force. It was possible to switch between these two servo-mechanisms, but the transition between force and position control can only be smoothly made when the position, the force, and the motor drive signals are precisely matched to each other. Otherwise, switching results in abrupt and disturbing transients.
Computer control A digital computer (Digital Equipment PDP 11/53) controlled the experiments (Fig. IB). The input to the servo-systems could be from either a prerecorded magnetic tape or the computer's analog output (updated at 0-5 ms intervals); each of these signals could be used to control either lever position or motor force. Smooth transitions between these different possibilities were achieved by computer programs which operated the analog switches only when the tape signal, the actual force and the lever position were appropriately matched to each other. Rectified electromyograms, position signals and force signals were sampled at 2 ms intervals (12 bit resolution) and stored on disc for subsequent analysis. Experimental procedure The subjects carried out two different tasks. In the first task the motor controlled the position of the lever beneath the index finger and the subject was asked to maintain a constant grip force of 1-5 N (which was less than 10 % of maximal) while the lever moved in a pseudo-random manner under the control of a prerecorded tape (see below). In the other task the subject attempted to maintain a constant position while the motor modulated the force in a pseudo-random way around a mean value of 1-5 N. When the subject was performing one or other of these tasks, and had brought the position or force close to the target value, the experimenter closed a switch which initiated the testing routine. After some random interval the computer took charge of the motor, and (acting through its position-controlling servo) imposed a ramp movement of 8 mm at 300 mm s-' (see Fig. 2 C and D) which started from precisely the position that the joint had then reached. After the ramp was complete the joint was held in the extended position for a further 375 ms. In order that responses obtained during the two tasks could be compared, it was important that the reflexes were tested when the flexing force and the finger position were close to the chosen values. The computer was so programmed that the test movements only occurred when the finger was within 3 mm of the desired position, and the force was within + 15% of the target value. However, the subject had control of either force or position and needed some help to keep it within the target area. When he or she was maintaining position, a low-pass filtered version of the position signal (time constant approximately 2 s) was therefore displayed on an oscilloscope, and a similar force signal was provided when he or she was maintaining force. This visual display was blanked out during the ramp movements. The timing of the perturbations involved a random delay, but it also depended on how well the subject maintained the force or position. The interval between perturbations was never less than 5 s, and it might be as much as 30 s. A set of thirty-two perturbations usually took about 10 min, but subjects were free to rest for as long as they chose between individual tests. In practised subjects the intervals were similar during the two different tasks. In some early experiments, ramp flexion movements were used as well as extensions, and these were mixed together in random order. In later experiments, only extensions were used. The tape recording which generated the pseudo-random movements and forces consisted of a
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mixture of three sinusoids of unrelated frequencies all of which were less than 0 3 Hz. This input gave movements of up to +3 mm, or force changes of up to +0 7 N. In practice, this pattern of movements or forces could not be predicted. even by subjects who knew how they had been generated. Position, force and rectified EMIG records were collected for a period of 200 ms before and 400 ms after the beginning of each ramp extension. These records could later be displayed individually (Fig. 2C and D)! or after averaging (Figs 3-5). RESULTS
The two tasks are illustrated in Fig. 2A and B. In Fig. 2A the subject gripped the levers and attempted to maintain a constant mean flexing force of 15 N (upper trace), while the motor varied the lever position (lower trace). In Fig. 2B the subject attempted to hold the finger in the same position while the motor varied the force. These records illustrate the force and position control that we could expect from a practised subject; in neither case was the control perfect, some force changes did occur in Fig. 2A, and some position changes in Fig. 2B. Motor controls position
A
C
Subject maintains force N
-
Force Position
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_ B
N
f
]10 mm
D
Motor controls force Subject maintains position
_ | ~EMG
E_Force -
_
Position
5s ~~~~~~~~~0.5 s 15s 1105 Fig. 2. Oscilloscope photographs to show finger positions (lowest traces) and forces (above). In A and C the subject was attempting to maintain a constant force of 1-5 N (approximately 0-12 N m at the interphalangeal joint) against a moving lever, but in B and D he was attempting to maintain a constant position in spite of changing force. Records C and D show the responses (including the FDI EMG) during an imposed lengthening movement of 8 mm at 300 mm s-' (for an average length of index finger this is equivalent to 6 5 deg of movement at the metacarpo-phalangeal joint at 250 deg s-1); note faster time base.
The two tasks felt quite different even though the actual position of the finger, and the forces upon it, were similar. In the 'maintain force' task the subjects felt they were gripping something which was firm and unyielding, but which nevertheless expanded and contracted between the finger and thumb. By contrast, the 'maintain position' task could be compared to gripping a soft balloon, in which the pressure was gradually increased and decreased. The 'maintain force' task did not come naturally to all subjects, and some of them practised for a long period (1 or 2 h in a number of different sessions) before they felt
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F. DOEMGES AND P. M. H. RACK they had acquired the 'knack' of doing it. The 'maintain position' task seemed easier, but on first attempts many subjects stiffened the joints of the wrist and hand with palpable co-contraction of antagonist muscles. However, most subjects relaxed as they became more used to the task. A
B
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Subject maintains position
C
I
50 yV]
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Position 0
50 100 150 Time (ms)
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Fig. 3. Averaged position force and rectified EMGs recorded in a subject who was attempting to maintain constant force (A) and to maintain constant position (B). Each record is the averaged response to sixty-four extension movements (8 mm at 300 mm s-1). The 128 extensions were in four sets of thirty-two, the 'maintain position' and 'maintain force' tasks being alternated to reduce any effect of habituation or fatigue. In C the position and EMG records of A and B have been superimposed.
The oscilloscope display of the quantity to be controlled (force or position) was heavily low-pass filtered so that it did not help the subjects to correct for the fluctuations imposed by the tape recorder (in fact the filter introduced phase delays which made the signals positively unhelpful). Subjects found that they were best able to perform the tasks when they had learned to disregard small fluctuations of the visual display, and to rely on what their fingers 'felt' to be doing.
The response to abrupt extension movements While the subjects were attempting to 'maintain force' or to 'maintain position', the excitability of the FDI stretch reflex was examined by randomly timed extension movements of the finger (8 mm at 300 mm s-1). Figure 2C and D shows responses to these extensions during the same experiment as Fig. 2A and B (note faster time base). Throughout the 'maintain force' task (Fig. 2A and C) the motor was in control of finger position, and the imposed extension merely continued this situation. However, in the 'maintain position' task (Fig. 2B and D), the motor was at first in control of force, but then for the imposed extension movement and the subsequent 375 ms, it took charge of position. The subject could not prevent the extension, and the instruction was therefore to 'maintain the finger position, but do not intervene when it is forcibly disturbed'. (Attempts to respond to the extensions in different ways did not, in fact, alter EMG responses in the first 100 ms.) Figure 3 shows averaged responses of one subject to sixty-four extension movements during the 'maintain force' task (Fig. 3A) and sixty-four during the
TASK-DEPENDENT HUMAN STRETCH REFLEXES 569 'maintain position' task (Fig. 3B). The imposed extension was followed by a burst of EMG activity which began about 55 ms from the beginning of extension and lasted until about 90 ms. However, this reflex response was notably larger when the subject was attempting to maintain position (Fig. 3B), than when she was attempting to B
A Subject maintains force
C
Subject maintains position
100 jV]J
l l
I
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Force 30
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m
Position
!
I
10 mm
0 50 100 150 50 100 150 Time (ms) Time (ms) Fig. 4. As for Fig. 3, but from a different subject. Each record is the averaged response to ninety-six extensions.
0
50 100 150 Time (ms)
0
'maintain force' (Fig. 3A). This difference between reflex EMG responses during the two tasks is more clearly seen when the two records are superimposed (Fig. 3 C). This task-related difference between the EMG responses at 50-90 ms (Fig. 3C) occurred consistently in all the subjects who had practised the task, and in some subjects it was obvious in the responses to individual extensions (as in Fig. 2C and D). However, there were some subjects in whom the reflex response also included earlier components which began about 30 ms after the onset of movement (Fig. 4). The rectified EMG records then included two peaks, the timings of which were similar to those reported by Noth, Podoll & Friedemann (1985) for the same muscle; these no doubt correspond to the fast-spinal and long-latency stretch reflexes which have been described for many other muscles (Hammond, 1960; Marsden et al. 1976). It was notable that when these early reflex components were present, they remained the same in both tasks, and it was only the latter (55-90 ms) components which decreased when the task was changed from 'maintain force' (Fig. 4A) to 'maintain position' (Fig. 4B). In this respect, the results differ from those of Kanosue, Akazawa & Fujii (1983), who concluded that the amplitudes of spinal stretch reflexes are also task dependent. In some subjects, the later reflex response was preceded by a brief decrease in the EMG signal without a preceding peak of fast-spinal reflex activity (Fig. 3). Presumably this dip in the record indicates the end of a fast-spinal response whose amplitude was too small, and whose onset too dispersed to appear as a significant peak in surface EMG.
The task-dependent differences in reflex response were seen when we compared attempts to maintain position against a changing force with attempts to maintain force against a changing position. When, however, the subject maintained force
F. DOEMGES AND P. M. H. RACK
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against a fixed lever, and then maintained position against a constant force, there was no significant alteration in the reflex responses. It is worth noting that subjects found these two static tasks similar to each other, and relatively easy to accomplish. During both of these static tasks there was a vigorous long-latency reflex response, similar to those seen when the subject was 'maintaining position' in the face of a changing force. In the present experiments it was only when subjects were maintaining a constant force against a moving lever that the long-latency stretch reflex was suppressed. It is notable that this was also the task which subjects found the most difficult.
A
B
Subject maintains force
Subject maintains position
100 MV]
1
3.0 Force (N)
10 mm Position 0
50 100 150 Time (ms)
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D
C
3.0 2.01 I
1.0 0
I
Ir
i
I
3.0
-
2.0
-
I I
T I ----I 50 100 150 0 50 100 150 0 Time (ms) Time (ms) Fig. 5. Averaged data from eight different subjects, using only experiments in which the EMG activity preceding the perturbation was equal in the two tasks. A-C are plotted in the same way as in Figs 3 and 4. For D the same EMG activity was expressed in terms of the preceding baseline level before averaging. The time scale starts with the first force
change.
I
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Co-activation of antagonist muscles When subjects were new to the tasks, their attempts to maintain a constant finger position were often accompanied by activation of other muscles of the wrist and hand. Contraction of antagonist muscles could have reduced the force of finger flexion, and the measurements of external force would not then give a reliable indication of the activation of the first dorsal interosseous muscle. It could be argued that the more powerful reflex activity in the 'maintain position' task was merely the accompaniment of a higher level of muscle activity. In order to avoid this complication, we have deliberately set aside experiments in which there was a different amount of FDI EMG activity in the two tasks. In Fig. 5 we show the average of all results obtained in experiments where the FDI activation was the same in both tasks (as judged from the rectified EMGs before the extension). Figure 5A-C shows that the reflex responses still differed from each other, confirming that the reflex was still task dependent even though the background EMG activity had been the same. Although Fig. 5A-C was constructed from records in which there was equal EMG activity in the 'maintain position' and 'maintain force' task, the absolute amounts of activity differed between subjects. After normalizing the results of individual subjects by expressing EMG activity in terms of the preceding EMG baseline level, these were averaged to give Fig. 5D. The standard error bars indicate that the EMG records differed significantly from each other in the time interval 68-86 ms after the first force change (the mean values are then separated by more than two standard errors). The integrated EMG activity in the time interval 55-90 ms was also measured for the averaged results of each subject. Student's paired t test confirmed the significant difference between the responses to the two tasks (P < 0.001). Although Fig. 5 compares records in which the levels of FDI activation were equal, the fingers were stiffer in the 'maintain position' than in the 'maintain force' tasks. In Fig. 5A the imposed movement was slightly smaller than in Fig. 5B, but it caused a larger rise in force; the differences are seen more clearly in Fig. 5 C. These changes in stiffness are visible in the first 40 ms, before there was time for any reflex force to develop. Presumably the 'maintain position' task involved some contraction of other flexors and extensors of the finger, even though the activity in the FDI had remained the same. DISCUSSION
There have been numerous descriptions of the responses of the flexor pollicis longus muscle to imposed extension movements of the thumb (see Marsden et al. 1976, 1978; Loo & McCloskey 1985). When the timing of the imposed movement was quite unpredictable, the EMG responses which occurred in the first 85 ms could not be modified in any consistent way by the prior intentions of the subject. After about 85 ms, the responses were indeed influenced by the subjects' intentions, but at that time voluntary responses could be expected anyway. It was therefore concluded that prior instructions have little effect on stretch reflex responses of this muscle, so long as the perturbing movement is quite unpredictable. The FDI has longer peripheral nerves than the flexor pollicis longus, and one would expect an even longer interval between the perturbation and any intentional
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modification of the response to it. However, the present results show that when subjects undertake different tasks, the FDI EMG is modified at 68 ms (Fig. 5), and sometimes appreciably earlier. This is considerably sooner than one would expect a voluntary response in so peripheral a muscle, and it must therefore be regarded as a reflex response which is task dependent. The task-dependent changes were appropriate; when it was necessary to maintain position and prevent movements, the reflex response was large, but during the 'maintain force' task, where movements were to be permitted without added resistance, the response was reduced. We conclude that subjects who are involved in a particular motor task alter their long-latency stretch reflexes in an appropriate way, whereas the mere instruction or intention to react in a particular way may not lead to consistent reflex changes. However, it is interesting to note that when a perturbation can be anticipated, the reflex response to it may be modified by the intentions of the subject (Rothwell et al. 1980; Goodin et al. 1990). The nervous system clearly has the capacity to alter the long-latency stretch reflex activity to suit a particular task, or in immediate anticipation of a movement (Gurfinkel, Kots, Krinskiy, Paltsev, Feldman, Tsetlin & Shik, 1971) or disturbance, but the present results do not support a suggestion that fast-spinal stretch reflexes are also task dependent (Kanosue, Akazawa & Fujii, 1983). Responses which occur after the minimum voluntary reaction time are very often described as 'voluntary responses', to distinguish them from stretch reflexes. This is a convenient though somewhat arbitrary distinction, since later components of a response may also occur without conscious thought; in fact, the 'reflex' reactions probably merge seamlessly into 'voluntary' response (Rack, 1981), without any clear dividing line. The following paper (Doemges & Rack, 1992) reports a task-dependent modification of stretch reflexes in wrist flexor muscles which persists after coactivation of other muscles has been prevented. The method used in that investigation enables the subject to 'maintain position' without the disrupting effect of imposed position ramps. The authors are grateful to Johannes Noth for his comments on the manuscript, and to Jane Arnold for technical assistance. The work was supported by a grant from the Medical Research Council, and F. D. received a grant from the Deutsche Forschungsgemeinschaft. REFERENCES
AKAZAWA, K., MILNER, T. E. & STEIN, R. B. (1983). Modulation of reflex EMU and stiffness in response to stretch of human finger muscles. Journal of Neurophysiology 49, 16-27. COLEBATCH, J. G., GANDEVIA, S. C., MCCLOSKEY, D. I. & POTTER, E. K. (1979). Subject instruction and long-latency reflex responses to muscle stretch. Journal of Physiology 292, 527-534. CRAGO, P. E., HOUK, J. C. & HASAN, Z. (1976). Regulatory actions of human stretch reflex. Journal of Neurophysiology 39, 925-935. DOEMGES, F. & RACK, P. M. H. (1991). Stretch reflexes diminish as normal human subjects learn to control the force of a precision grip. Journal of Physiology 435, 56P. DOEMGES, F. & RACK, P. M. H. (1992). Task-dependent changes in the response of human wrist joints to mechanical disturbance. Journal of Physiology 447, 575-585. EVARTS, E. V. & GRANIT, R. (1976). Relations of reflexes and intended movements. Progress in Brain Research 44, 1-14.
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GOODIN, D. S., AMINOFF, M. J. & SHIH, P.-Y. (1990). Evidence that long-latency stretch responses of the human wrist extensor muscle involve a transcerebral pathway. Brain 113, 1075-1091. GURFINKEL, V. S., KOTS, YA. M., KRINSKIY, V. I., PALTSEV, E. I., FELDMAN, A. G., TSETLIN, M. L. & SHIK, M. L. (1971). Concerning tuning before movement. In Models of Structural-functional Organization of Certain Biological Systems, ed. GELFAND, I. M., GURFINKEL, V. S., FOMIN, S. V. & TSETLIN, M. L., pp. 361-372 of English translation. MIT Press, Cambridge, MA, USA. HAMMOND, P. H. (1956). The influence of prior instruction to the subject on an apparently involuntary neuromuscular response. Journal of Physiology 182, 17-18P. HAMMOND, P. H. (1960). An experimental study of servo-action in human muscular control. In Proceedings of the 3rd Conference on Medical Electronics, pp. 190-199. Institution of Electrical Engineers, London. HORE, J., MCCLOSKEY, D. I. & TAYLOR, J. L. (1990). Task-dependent changes in gain of the reflex response to imperceptible perturbations of joint position in man. Journal of Physiology 429, 309-321. JOHANSSON, R. S. & WESTLING, G. (1988). Programmed and triggered actions to rapid load changes during precision grip. Experimental Brain Research 71, 72-88. KANOSUE, K., AKAZAWA, K. & Fujii, K. (1983). Modulation of reflex activity of motor units in response to stretch of a human finger muscle. Japanese Journal of Physiology 33, 995-1009. LEE, R. G. & TATTON, W. G. (1975). Motor responses to sudden limb displacements in primates with specific CNS lesions and in human patients with motor system disorders. Canadian Journal of Neurological Science 2, 285-293. Loo, C. K. C. & MCCLOSKEY, D. I. (1985). Effects of prior instruction and anaesthesia on longlatency responses to stretch in the long flexor of the human thumb. Journal of Physiology 365, 285-296. MARSDEN, C. D., MERTON, P. A. & MORTON, H. B. (1976). Servo action in the human thumb. Journal of Physiology 257, 1-44. MARSDEN, C. D., MERTON, P. A. MORTON, H. B., ADAM, J. E. R. & HALLETT, M. (1978). Automatic and voluntary responses to muscle stretch in man. In Cerebral Motor Control in Man: Long-loop Mechanisms, ed. DESMEDT, J. E., pp. 167-177. Karger, Basel. NOTH, J., PODOLL, K. & FRIEDEMANN, H.-H. (1985). Long-loop reflexes in small hand muscles studied in normal subjects and in patients with Huntington's disease. Brain 108, 65-80. RACK, P. M. H. (1981). Limitations of somatosensory feedback in control of posture and movement. In Handbook of Physiology, section 1, The Nervous System, vol. 2, Motor Control, ed. BROOKS, V. B. pp. 229-256. American Physiological Society, New York. ROTHWELL, J. C., TRAUB, M. M. & MARSDEN, C. D. (1980). Influence of voluntary intent on human long-latency stretch reflex. Nature 286, 496-498.
