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Stretch and unloading reflexes in a human hand muscle
EXPERIMENTAL
NEUROLOGY
94,348-358
Stretch and Unloading
(1986)
Reflexes in a Human Hand Muscle
RONALD W.ANGEL
ANDMICHAELWEINRICH
Department of Neurology, Stanford University Medical Center, and Neurology Service, VA Medical Center, Palo Alto, Carifmia 94304 Received April 18. I986 Stretch and unloading reflexes were demonstrated in the first dorsal interosseous muscle by averaging the electromyographic responses to brief mechanical stimuli. Subjects were not able to abolish these reflexes by altering their preparatory set. When subjects were prepared to contract or relax the muscle in response to a stretching force, the size of the stretch retlex was not affected significantly. When they were prepared to contract or relax in response to unloading, the “silent period” was diminished. In general, these reflexes were not modulated appropriately to improve the performance of an intended voluntary movement. Our results do not support the notion that spinal reflexes of the intrinsic hand muscles are “dominated” by corticospinal inputs. 8 1986 .hhti~ PBS, Ittc.
INTRODUCTION
Muscle stretch reflexes are tested routinely during the neurological examination and often provide useful diagnostic clues. Although their physiologic basis is well known, our knowledge of these reflexes is based largely on the study of proximal muscles in the cat (7-l 1). Several facts indicate the need for a better understanding of stretch reflexes in the small, distal muscles. First, the muscles of the hand are used in the most finely controlled and distinctively human types of movement. Compared with proximal muscles, these small muscles have a much larger cortical representation (2 I ). Moreover, corticospinal fibers are known to terminate directly upon motoneurons innervating the distal muscles (S), and the density of these direct terminations is greatest from regions of motor cortex representing the distal limb (18). Finally, the loss of manual dexterity is an early sign of upper motor 348 0014-4886/86 $3.00 Copyright Q 1986 by Academic Press, Inc. Au rig& of reproduction in my form -ed.
HAND
MUSCLE
REFLEXES
349
neuron disease. These facts motivated the present investigation of stretch and unloading reflexes in an intrinsic hand muscle. Previous workers have postulated a transcortical stretch reflex mechanism, which has evolved to its greatest extent for the control of the hand (15, 18). This mechanism is presumed to “dominate” the spinal cord and to prevent the latter from acting autonomously. By putting the cortex in full command, the transcortical mechanism would improve control of the muscles most concerned with delicate movements. Our working hypothesis was that the spinal reflexes of the intrinsic hand muscles are subordinate to corticospinal controls. On this basis, we predicted that the subjects’ preparatory set would suppress or modulate the stretch and unloading reflexes so as to aid the subjects’ voluntary efforts. MATERIALS
AND
METHODS
Nine men and one woman, age 22 to 62 years, participated in the study. All were in good health without evidence of neurologic disease. The subject was seated with the left forearm resting on a splint and held midway between pronation and supination. To immobilize the hand, the subject grasped a stationary handle with the thumb and digits 3 through 5. The index finger was extended with the distal phalanx pressed against a stimulus lever, which was driven by a DC motor. Under initial conditions, the lever produced a constant leftward force of approximately 1 N (Newton; equivalent to 0.1 kg weight), which tended to extend the finger. At the start of each trial, the finger was held in a neutral position (roughly 10“ of flexion). To maintain this position, the subject had to exert a counter force by contraction of the flexor muscles (first dorsal interosseous, flexor digitorum sublimis, and flexor digitorum profundus). On some trials, the stimulus consisted of a brief (20-ms) doubling of the force on the finger. These were designated as LOAD trials. On other trials, the stimulus consisted of a brief (20-ms) removal of the force. These were designated as UNLOAD trials. On all tests, the interstimulus interval was 2 s. Action potentials of the first dorsal interosseous muscle were detected by paired surface electrodes. These were amplified, full-wave rectified, and filtered, with an averaging period of 10 ms (6). A transducer attached to the stimulus lever registered the position of the distal phalanx. Voltages representing the EMG and finger position were averaged (Nit 1170, Nicolet Instrument Corp.) and stored on magnetic tape. After each experiment, the data were displayed on paper and measured. Trials were conducted in blocks of 64 under each of six experimental conditions, with the following instructions to the subject. LOAD hold the finger
350
ANGEL
AND WEINRICH
stationary. LOAD-FLEX: hold the starting position until you feel the force increase, and then flex the finger as rapidly as possible. LOAD-EXTEND: hold the starting position until you feel the force increase, and then extend the finger as rapidly as possible. UNLOAD: hold the finger in the neutral position at all times. UNLOAD-FLEX: hold the starting position until you feel the force decrease and then flex as rapidly as possible. UNLOAD-EXTEND: hold the starting position until you feel the force increase and then extend as rapidly as possible. The test conditions were presented in quasirandom order. To provide a standard for quantifying the EMG responses, we first determined the level of EMG activity recorded during the isometric contraction against the initial load, taking as zero the level recorded during muscular relaxation. Measured in this way, the amount of EMG activity recorded in the starting position was found to vary between experimental conditions, despite the fact that the same initial force was required under all conditions. Part of this variation was attributed to the fact that the first dorsal interosseous is only one of several flexor muscles, which can share the load in different proportions. Another source of variation would be cocontraction of the extensor muscles, requiring greater activity of the flexors to maintain a given amount of force. Hence, the absolute level of EMG activity during isometric contraction was not an acceptable standard for comparison between test conditions. Recognizing that any standard would be arbitrary, we elected to measure the greatest increase or depression of EMG activity occurring within 100 ms after the onset of the pulse to the DC motor. The peak recorded under the LOAD condition was measured in millimeters and used as a basis for comparison with peaks obtained under conditions LOAD-FLEX and LOADEXTEND. Similarly, the decrease of EMG activity recorded in the UNLOAD condition was used as a basis for comparison with the depressions obtained under UNLOAD-FLEX and UNLOAD-EXTEND. For example, the EMG tracing in Fig. 1 showed a decrease of 68 mm at the original magnification. Figure 2, taken from the same subject under the UNLOAD-FLEX condition, showed a decrease of 71 mm. The amplitude of the unloading reflex in Fig. 2 would then be expressed as 7 l/68 or 104% of that in Fig. I. The unit of measurement (millimeters) was arbitrary, because it depends on extraneous factors, such as electrode placement and amplifier gain. However, the percentages provided a basis for comparing the reflexes obtained under the various test conditions. To provide an estimate of the reflex latencies, we measured the time from the beginning of finger movement to the onset of the EMG response, as gauged by visual inspection of the tracing. These estimates were necessarily inexact, because the mechanical stimulus was not instantaneous, and the
HAND MUSCLE
351
REFLEXES
EMG
Position
t
11cm 100 ms
FIG. 1. Unloading reflex. The upper line is the rectified, filtered, and averaged EMG from the first dorsal interosseous muscle. The lower line is the position of the index finger. Finger hexion moved the trace downward. As the trace began, the index finger was in neutral position, and the flexor muscles were contracted against an opposing force of approximately 1 N. At the time shown by downturn of the position trace, the force was released for 20 ms and the finger flexed briefly. Unloading of the muscle caused a sharp decrease in the level of EMG activity (black arrow), followed by a burst of renewed activity (white arrow). In this and all other figures, each trace is the average of 128 trials with subject J.K.
onset of the EMG deflection was sometimes obscured by the fluctuating base line (see figures). Nevertheless, the estimated latencies provided a basis for comparison between the experimental conditions. RESULTS The mechanical effect of the 20-ms loading pulse was a brief extension of the finger, causing roughly 7” of rotation at the proximal joint. This was followed immediately by an equal and opposite flexion, which restored the resting position within 120 to 160 ms. The 20-ms unloading pulse caused a brief flexion of the finger, also 7” in amplitude and 120 to 160 ms in duration. The EMG response to the unloading pulse was a decrease in the level of motor unit activity, the unloading reflex (Fig. I), and the response to loading was an increase, the stretch reflex (Fig. 4). The mean latencies under the six test conditions were as follows: UNLOAD: 36.5 f 5.2 (mean f SD in milliseconds); UNLOAD-FLEX 36.5 f 9.64; UNLOAD-EXTEND: 35.1 Ifr 10.1; LOAD: 35.7 f 8.2; LOADFLEX: 42.4 f 12.4; LOAD-EXTEND: 33.1 f 7.1. These values agree with the latencies reported by Buller et al. (3), who found that mechanical pulses to the belly of the first dorsal interosseous produced an increase in the probability of motoneuron firing within 38 to 50 ms. Because there were no significant differences between the measures under different test conditions, we concluded that changes of the preparatory set had no effect on the latencies.
352
ANGEL
AND WEINRICH
EMG
M Positbn
t
FIG. 2. UNLOAD-FLEX condition. The initial conditions were the same as in Fig. 1. The subject was instructed to flex the finger as soon as possible in response to release of the external force. The position trace showed an initial flexion caused by unloading of muscle and a second, voluntary flexion. Although prepared to contract the muscle in response to the stimulus, the subject was unable to inhibit the decrease of EMG activity after unloading (black arrow). The amplitude of the unloading reflex was measured as 104% of that seen in Fig. 1. The “silent period” was followed by a rebound of activity, as in Fig. 1 (white arrow).
Under the UNLOAD-FLEX condition, in which the subject flexed the finger in response to the unloading stimulus, the amplitudes of the stretch reflex were found to range from 3 1to 111%of the values obtained under the UNLOAD condition (mean 62.8%, SD 29.2%) (Figs. 1 and 2). Thus, the mean difference between conditions was 37.2%, which was statistically sig-
FIG. 3. UNLOAD-EXTEND condition. The subject was instructed to extend the finger as soon as possible in response to release of the external force. The position trace showed an initial flexion caused by unloading of muscle and then a voluntary extension. Although prepared to relax the muscle, the subject was unable to enhance the decrease of EMG activity after unloading (black arrow) or to prevent the rebound following the initial drop (white arrow). The amplitude of the unloading reflex was measured as 5 1% of that seen in Fig. 1.
HAND
MUSCLE
353
REFLEXES
TABLE 1 Unloading Reflex in First Dorsal Interosseous Muscle Test condition UNLOAD
UNLOAD-FLEX
UNLOAD-EXTEND
Subject
mm’
%
mm”
%
mmn
%
D.S. R.A. M.P. T.G. P.S. D.E. J.M. M.W. S.W. J.K. Mean * SD
23 26 29 29 43 45 51 71 44 68
100 100
15 22 9 10 16 50 22 34 31 71
65 85 31 34 37 111 43 48 70 104 62.8 + 29.2
14 28 18 19 30 28 23 74 13 51
61 108 62 66 70 62 45 104 30 75 68.3 _t 23.7
100 100 100 100 100 100 100 100
’ Largest downward deflection of EMG tracing within 100 ms after unloading. Value under the UNLOAD condition is taken as 100%.
nificant (SE 9.24%, t 4.02, P < 0.0 1). Under the UNLOAD-EXTEND condition, the amplitudes of the stretch reflex ranged from 30% to 108% of the values obtained under the UNLOAD condition (mean 68.3%, SD 23.7%) (Fig. 3). The mean difference between the two conditions was 3 1.7%, which was statistically significant (SE 7.49, t 4.23, P < 0.01). Thus, the mean size of the unloading reflex was smaller under both UNLOAD-FLEX and UNLOAD-EXTEND, compared with the UNLOAD condition (Table 1). Under the LOAD-FLEX condition, the subject flexed the finger as soon as possible after he perceived the stimulus (Figs. 4 and 5). The size of the stretch retlex was found to range from 0% to 130% of the values found under the LOAD condition (mean 83.7%, SD 38.51%). The mean difference between the conditions (16.3%) was not statistically significant (t 1.34, P> 0.1). Under the LOAD-EXTEND condition, the size of the stretch reflex ranged from 43% to 138% of the value found under the LOAD condition (Fig. 6). Again, the mean difference (2.7%) was not statistically significant (t 0.28, P > 0.1) (Table 2). DISCUSSION Three principal findings emerged from this study: First, stretch and unloading reflexes were easily demonstrated in a small muscle of the hand, Sec-
354
ANGEL
EMG
AND WEINRICH
I
Ll
cm 100 ins
FIG. 4. Stretch reflex. The initial conditions were the same as in Fig. 1. At the time shown by the upturn of the velocity trace, the force was increased for 20 ms, causing extension of the finger and stretching the flexor muscle, which responded with an increase of EMG activity (arrow).
ond, these reflexes were not abolished by the subject’s preparatory set, i.e., the intention to contract or relax the muscles. Third, the reflexes were not generally modulated in an “appropriate” direction by the subject’s preparatory set. An exception was the fact that the decrease of EMG activity after unloading was less marked when the subject was prepared to contract the muscle. The tendon jerk has been examined by neurologists for more than a century, but its reflex nature was still controversial when Shenington wrote a
EMG
FIG. 5. LOAD-FLEX condition. The subject was instructed to flex the finger as soon as possible in response to the stretching force. The position trace showed an initial extension caused by the motor and then flexion produced voluntarily, The stretch reflex (arrow) was measured as 115% of that seen in Fig. 4.
HAND MUSCLE EMG
355
REFLEXES
I
Position
,
11cm 100 ms
FIG. 6. LOAD-EXTEND. The subject was instructed to extend the finger in response to the stretching force. The position trace showed an initial extension caused by the motor and then an extension produced voluntarily. The stretch reflex (arrow) was measured as 7 1% of that seen in Fig. 4.
textbook account in 1900 ( 19). Forty years elapsed before Lloyd (12, 13) finally proved that the reflex response to a brief muscle stretch is mediated “through arcs of two neurons.” There followed a series of classic experiments which demonstrated the mechanism of the stretch reflex in great detail ( 10, 11,14). However, our knowledge of this reflex has been derived mainly from TABLE 2 Stretch Reflex in First Dorsal Interosseous Muscle Test condition LOAD
LOAD-FLEX
LOAD-EXTEND
Subject
mm”
%
mm”
%
mm”
%
D.S. R.A. M.P. T.G. P.S. D.E. J.M. M.W. S.W. J.K. Mean + SD
21 26 23 26 24 103 62 76 38 78
100 100 100 100 100 loo 100 100 100 100
24 20 18 29 12 134 43 70 0 90
114 77 78 112 50 130 69 92 0 115 83.7 + 38.5
19 36 10 30 27 144 43 74 37 55
90 138 43 115 113 140 69 97 97 71 97.3 +- 30.8
’ Largest upward deflection of EMG tracing within 100 ms after loading. Value under the LOAD condition is taken as 100%.
356
ANGEL
AND WEINRICH
the study of large muscles in the hind limb of the cat. Similarly, the physiology of the unloading reflex has been investigated in experiments with large, proximal muscles (2,7). In recent studies of long-latency reflexes, attention has been directed to muscles of the upper limb, including biceps (5) wrist flexors (4, 9), and the flexor pollicis longus (1,15). Except for one study involving the flexor pollicis brevis (16) and two involving the first dorsal interosseous (3,17), the intrinsic muscles of the hand have been relatively neglected. The hand musculature appears to deserve study from the clinical, as well as the scientific viewpoint. As noted below, these small muscles are represented by a relatively large area of the motor cortex (2 I), and corticospinal fibers project directly upon their motoneurons (8). The direct cortical projections are most profuse to the motoneurons of the distal muscles and explain the preferential accessibility of these muscles to cortical stimulation (13). Hence, it is not surprising that a loss of manual dexterity is a sensitive indicator of corticospinal tract disease. Because of these strong corticospinal projections, one might suppose that the brain can modulate the segmental reflexes affecting the intrinsic hand muscles. Tanji and Evarts (20) noted that changes of pyramidal tract neuron activity with “intention” or “motor set” provide a mechanicm for suprasegmental control and presetting of spinal cord reflex excitability specific to the nature of an impending movement. Thus, the stretch reflex might be suppressed when the subject intends to relax the muscle and increased when he intends to contract it. Similarly, the unloading reflex might be suppressed when the subject intends to contract the muscle and increased when he intends to relax it. Of these predictions, only one was confirmed in our experiments. Under the UNLOAD-FLEX condition, the subject flexed the finger as soon as possible after perceiving the stimulus. This response called for contraction of the muscles that ordinarily show a “silent period” after unloading. This voluntary contraction would be hastened by abolition or a decrease in size of the unloading reflex. In 8 of 10 subjects, this reflex was, in fact, reduced in amplitude under the UNLOAD-FLEX condition. Thus, it was modulated in the “appropriate” way, though not completely suppressed. Under the UNLOAD-EXTEND condition, the subject was prepared to extend the finger, i.e., relax the flexor muscles immediately after perceiving the stimulus. Although the “appropriate” modulation would be an enhancement of the silent period, 8 of 10 subjects showed the opposite effect; i.e., the unloading reflex was smaller under the UNLOAD-EXTEND condition. Under the LOAD-FLEX and LOAD-EXTEND conditions, there was no significant change in size of the stretch reflex.
HAND
MUSCLE
REFLEXES
351
These experiments demonstrated two well-known spinal reflexes in an intrinsic hand muscle. On the assumption that the control of this muscle is “dominated” by corticospinal signals, we tried to modulate the reflexes by requiring subjects to alter their “motor set.” The data showed that changes of test conditions had no effect on the latency of either the stretch or the unloading reflex and no effect on the size of the stretch reflex. The only “appropriate” change was a decrease in size of the unloading reflex under the test condition that called for muscular contraction. However, there was also a decreased unloading reflex under the condition in which the subject was prepared to relax the muscle. We conclude that stretch and unloading reflexes of this hand muscle, like those of the large, proximal muscles, are relatively autonomous. These spinal reflexes are not readily abolished or modulated to meet the demands of an intended voluntary movement. REFERENCES 1. AKAZAWA, K., T. E. MILNER, AND R. B. STEIN. 1983. Modulation of reflex EMG and stiffnessin response to stretch of human finger muscle. J. Neurophysiol. 49: 16-27. 2. ANGEL, R. W., W. EPPLER, AND A. IANNONE. 1965. Silent period produced by unloading of muscle during voluntary contraction. J. Physiol. (London) 180: 864-870. 3. BULLER, N. P., R. GARNET-~, AND J. A. STEPHENS. 1980. The reflex responses of single motor units in human hand muscles following muscle afferent stimulation. J. Physiol. (London)
303: 337-349.
4. Calancie, C., and P. Bawa. 1985. Firing patterns of human flexor carpi radialis during the stretch reflex. J. Neurophysiol. 53: 1179-l 193. 5. COOKE, J. D., AND M. J. EASTMAN. 1977. Long-loop reflexes in the tranquilized monkey. Exp. Brain Res. 21: 49 l-500. 6. GARLAND, H., R. W. ANGEL, AND R. D. MELEN. 197 1. A state variable averaging filter for electromyogram processing. Med. Biol. Eng. 10: 559-560. 7. HANSEN, K., AND P. HOFFMAN. 1922. Weitere Untersuchungen iiber die Bedeutung der Eigenreflexe fur unsere Bewegungen. I. Anspannungs- und Entspannungsreflex. Z. Biol. 75: 293-304. 8. LAWRENCE, D. G., AND D. A. HOPKINS. 1976. The development of motor control in the rhesus monkey: evidence concerning the role of corticomotoneuronal connections. Brain
99: 235-254.
9. LEE, R. G., AND W. G. TAI-~ON. 1975. Motor responses to sudden limb displacements in primates with specific CNS lesions and in human patients with motor system disorders. Can. J. Neurol.
Sci. 2: 285-293.
10. LIDDELL, E. G. T., AND C. C. SHERRINGTON. 1924. Reflexes in response to stretch (myotatic reflexes). Proc. Sot. Land. B 96: 2 12-242. 11. LIDDELL, E. G. T. 1960. The Discovery of Reflexes. Oxford Univ. Press, Clarendon. 12. LLOYD, D. P. C. 1943. Reflex action in relation to pattern and peripheral source of afferent stimulation. J. Neurophysiol. 6: 1 1 1- 119. 13. LLOYD, D. P. C. 1943. Conduction and synaptic transmission of reflex response to stretch in spinal cats. J. Neurophysiol. 5: 3 17-326. 14. LLOYD, D. P. C. 1946. Integrative pattern of excitation and inhibition in two-neuron reflex arcs. J. Neurophysiol. 9: 439-444.
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15. MARSDEN, C. D., P. A. MORTON, ANDH. B. MORTON.1976.Servoactionin the human thumb.J. Physiol. (London) 257: l-44. 16. MATTHEWS, P. B. C. 1984.The contrastingstretchreflexresponses of the longandshort Bexormuscles ofthe humanthumb.J. Physiol. (London) 34% 545-558. 17. NOTH,J., H. R. MATTHEWS ANDH. H. PRIEDMANN. 1984.Longlatencyreflexforceof humanfingermuscles in response to sinusoidal movement.Exp. Bruin Res. 55: 317324.
18. PHILLIPS, C. G., ANDR. PORTER. 1977. Corticospinal Neurons: Their Role in Movement, pp.42-46.AcademicPress, London. 19. SHERRINGTON, C. S. 1900.The knee-jerkand alliedphenomenon. Page870-873in SHAFER, E.A., Ed., TextbookofPhysiology, Vol. II. Pentland,Edinburgh. 20. TANJI,J., ANDE. EVARTS.1975.Anticipatoryactivity of motorcortexneuronsin relation to directionofan intendedmovement. J. Neurophysiol. 39: 1062-1068. 21. WOOLSEY, C. N., P.H. SEX-~LAGE, D. R. MEYER,W. SENCER, T. P. HAMW, ANDA. M. TRAVIS.1952.Patternsof localizationin precentraland“supplementary” motorareas andtheir relationto the conceptof a premotorarea.Res. Publ. Assoc. Res. Nerv. Ment. Dis. 30: 238-264.
NEUROLOGY
94,348-358
Stretch and Unloading
(1986)
Reflexes in a Human Hand Muscle
RONALD W.ANGEL
ANDMICHAELWEINRICH
Department of Neurology, Stanford University Medical Center, and Neurology Service, VA Medical Center, Palo Alto, Carifmia 94304 Received April 18. I986 Stretch and unloading reflexes were demonstrated in the first dorsal interosseous muscle by averaging the electromyographic responses to brief mechanical stimuli. Subjects were not able to abolish these reflexes by altering their preparatory set. When subjects were prepared to contract or relax the muscle in response to a stretching force, the size of the stretch retlex was not affected significantly. When they were prepared to contract or relax in response to unloading, the “silent period” was diminished. In general, these reflexes were not modulated appropriately to improve the performance of an intended voluntary movement. Our results do not support the notion that spinal reflexes of the intrinsic hand muscles are “dominated” by corticospinal inputs. 8 1986 .hhti~ PBS, Ittc.
INTRODUCTION
Muscle stretch reflexes are tested routinely during the neurological examination and often provide useful diagnostic clues. Although their physiologic basis is well known, our knowledge of these reflexes is based largely on the study of proximal muscles in the cat (7-l 1). Several facts indicate the need for a better understanding of stretch reflexes in the small, distal muscles. First, the muscles of the hand are used in the most finely controlled and distinctively human types of movement. Compared with proximal muscles, these small muscles have a much larger cortical representation (2 I ). Moreover, corticospinal fibers are known to terminate directly upon motoneurons innervating the distal muscles (S), and the density of these direct terminations is greatest from regions of motor cortex representing the distal limb (18). Finally, the loss of manual dexterity is an early sign of upper motor 348 0014-4886/86 $3.00 Copyright Q 1986 by Academic Press, Inc. Au rig& of reproduction in my form -ed.
HAND
MUSCLE
REFLEXES
349
neuron disease. These facts motivated the present investigation of stretch and unloading reflexes in an intrinsic hand muscle. Previous workers have postulated a transcortical stretch reflex mechanism, which has evolved to its greatest extent for the control of the hand (15, 18). This mechanism is presumed to “dominate” the spinal cord and to prevent the latter from acting autonomously. By putting the cortex in full command, the transcortical mechanism would improve control of the muscles most concerned with delicate movements. Our working hypothesis was that the spinal reflexes of the intrinsic hand muscles are subordinate to corticospinal controls. On this basis, we predicted that the subjects’ preparatory set would suppress or modulate the stretch and unloading reflexes so as to aid the subjects’ voluntary efforts. MATERIALS
AND
METHODS
Nine men and one woman, age 22 to 62 years, participated in the study. All were in good health without evidence of neurologic disease. The subject was seated with the left forearm resting on a splint and held midway between pronation and supination. To immobilize the hand, the subject grasped a stationary handle with the thumb and digits 3 through 5. The index finger was extended with the distal phalanx pressed against a stimulus lever, which was driven by a DC motor. Under initial conditions, the lever produced a constant leftward force of approximately 1 N (Newton; equivalent to 0.1 kg weight), which tended to extend the finger. At the start of each trial, the finger was held in a neutral position (roughly 10“ of flexion). To maintain this position, the subject had to exert a counter force by contraction of the flexor muscles (first dorsal interosseous, flexor digitorum sublimis, and flexor digitorum profundus). On some trials, the stimulus consisted of a brief (20-ms) doubling of the force on the finger. These were designated as LOAD trials. On other trials, the stimulus consisted of a brief (20-ms) removal of the force. These were designated as UNLOAD trials. On all tests, the interstimulus interval was 2 s. Action potentials of the first dorsal interosseous muscle were detected by paired surface electrodes. These were amplified, full-wave rectified, and filtered, with an averaging period of 10 ms (6). A transducer attached to the stimulus lever registered the position of the distal phalanx. Voltages representing the EMG and finger position were averaged (Nit 1170, Nicolet Instrument Corp.) and stored on magnetic tape. After each experiment, the data were displayed on paper and measured. Trials were conducted in blocks of 64 under each of six experimental conditions, with the following instructions to the subject. LOAD hold the finger
350
ANGEL
AND WEINRICH
stationary. LOAD-FLEX: hold the starting position until you feel the force increase, and then flex the finger as rapidly as possible. LOAD-EXTEND: hold the starting position until you feel the force increase, and then extend the finger as rapidly as possible. UNLOAD: hold the finger in the neutral position at all times. UNLOAD-FLEX: hold the starting position until you feel the force decrease and then flex as rapidly as possible. UNLOAD-EXTEND: hold the starting position until you feel the force increase and then extend as rapidly as possible. The test conditions were presented in quasirandom order. To provide a standard for quantifying the EMG responses, we first determined the level of EMG activity recorded during the isometric contraction against the initial load, taking as zero the level recorded during muscular relaxation. Measured in this way, the amount of EMG activity recorded in the starting position was found to vary between experimental conditions, despite the fact that the same initial force was required under all conditions. Part of this variation was attributed to the fact that the first dorsal interosseous is only one of several flexor muscles, which can share the load in different proportions. Another source of variation would be cocontraction of the extensor muscles, requiring greater activity of the flexors to maintain a given amount of force. Hence, the absolute level of EMG activity during isometric contraction was not an acceptable standard for comparison between test conditions. Recognizing that any standard would be arbitrary, we elected to measure the greatest increase or depression of EMG activity occurring within 100 ms after the onset of the pulse to the DC motor. The peak recorded under the LOAD condition was measured in millimeters and used as a basis for comparison with peaks obtained under conditions LOAD-FLEX and LOADEXTEND. Similarly, the decrease of EMG activity recorded in the UNLOAD condition was used as a basis for comparison with the depressions obtained under UNLOAD-FLEX and UNLOAD-EXTEND. For example, the EMG tracing in Fig. 1 showed a decrease of 68 mm at the original magnification. Figure 2, taken from the same subject under the UNLOAD-FLEX condition, showed a decrease of 71 mm. The amplitude of the unloading reflex in Fig. 2 would then be expressed as 7 l/68 or 104% of that in Fig. I. The unit of measurement (millimeters) was arbitrary, because it depends on extraneous factors, such as electrode placement and amplifier gain. However, the percentages provided a basis for comparing the reflexes obtained under the various test conditions. To provide an estimate of the reflex latencies, we measured the time from the beginning of finger movement to the onset of the EMG response, as gauged by visual inspection of the tracing. These estimates were necessarily inexact, because the mechanical stimulus was not instantaneous, and the
HAND MUSCLE
351
REFLEXES
EMG
Position
t
11cm 100 ms
FIG. 1. Unloading reflex. The upper line is the rectified, filtered, and averaged EMG from the first dorsal interosseous muscle. The lower line is the position of the index finger. Finger hexion moved the trace downward. As the trace began, the index finger was in neutral position, and the flexor muscles were contracted against an opposing force of approximately 1 N. At the time shown by downturn of the position trace, the force was released for 20 ms and the finger flexed briefly. Unloading of the muscle caused a sharp decrease in the level of EMG activity (black arrow), followed by a burst of renewed activity (white arrow). In this and all other figures, each trace is the average of 128 trials with subject J.K.
onset of the EMG deflection was sometimes obscured by the fluctuating base line (see figures). Nevertheless, the estimated latencies provided a basis for comparison between the experimental conditions. RESULTS The mechanical effect of the 20-ms loading pulse was a brief extension of the finger, causing roughly 7” of rotation at the proximal joint. This was followed immediately by an equal and opposite flexion, which restored the resting position within 120 to 160 ms. The 20-ms unloading pulse caused a brief flexion of the finger, also 7” in amplitude and 120 to 160 ms in duration. The EMG response to the unloading pulse was a decrease in the level of motor unit activity, the unloading reflex (Fig. I), and the response to loading was an increase, the stretch reflex (Fig. 4). The mean latencies under the six test conditions were as follows: UNLOAD: 36.5 f 5.2 (mean f SD in milliseconds); UNLOAD-FLEX 36.5 f 9.64; UNLOAD-EXTEND: 35.1 Ifr 10.1; LOAD: 35.7 f 8.2; LOADFLEX: 42.4 f 12.4; LOAD-EXTEND: 33.1 f 7.1. These values agree with the latencies reported by Buller et al. (3), who found that mechanical pulses to the belly of the first dorsal interosseous produced an increase in the probability of motoneuron firing within 38 to 50 ms. Because there were no significant differences between the measures under different test conditions, we concluded that changes of the preparatory set had no effect on the latencies.
352
ANGEL
AND WEINRICH
EMG
M Positbn
t
FIG. 2. UNLOAD-FLEX condition. The initial conditions were the same as in Fig. 1. The subject was instructed to flex the finger as soon as possible in response to release of the external force. The position trace showed an initial flexion caused by unloading of muscle and a second, voluntary flexion. Although prepared to contract the muscle in response to the stimulus, the subject was unable to inhibit the decrease of EMG activity after unloading (black arrow). The amplitude of the unloading reflex was measured as 104% of that seen in Fig. 1. The “silent period” was followed by a rebound of activity, as in Fig. 1 (white arrow).
Under the UNLOAD-FLEX condition, in which the subject flexed the finger in response to the unloading stimulus, the amplitudes of the stretch reflex were found to range from 3 1to 111%of the values obtained under the UNLOAD condition (mean 62.8%, SD 29.2%) (Figs. 1 and 2). Thus, the mean difference between conditions was 37.2%, which was statistically sig-
FIG. 3. UNLOAD-EXTEND condition. The subject was instructed to extend the finger as soon as possible in response to release of the external force. The position trace showed an initial flexion caused by unloading of muscle and then a voluntary extension. Although prepared to relax the muscle, the subject was unable to enhance the decrease of EMG activity after unloading (black arrow) or to prevent the rebound following the initial drop (white arrow). The amplitude of the unloading reflex was measured as 5 1% of that seen in Fig. 1.
HAND
MUSCLE
353
REFLEXES
TABLE 1 Unloading Reflex in First Dorsal Interosseous Muscle Test condition UNLOAD
UNLOAD-FLEX
UNLOAD-EXTEND
Subject
mm’
%
mm”
%
mmn
%
D.S. R.A. M.P. T.G. P.S. D.E. J.M. M.W. S.W. J.K. Mean * SD
23 26 29 29 43 45 51 71 44 68
100 100
15 22 9 10 16 50 22 34 31 71
65 85 31 34 37 111 43 48 70 104 62.8 + 29.2
14 28 18 19 30 28 23 74 13 51
61 108 62 66 70 62 45 104 30 75 68.3 _t 23.7
100 100 100 100 100 100 100 100
’ Largest downward deflection of EMG tracing within 100 ms after unloading. Value under the UNLOAD condition is taken as 100%.
nificant (SE 9.24%, t 4.02, P < 0.0 1). Under the UNLOAD-EXTEND condition, the amplitudes of the stretch reflex ranged from 30% to 108% of the values obtained under the UNLOAD condition (mean 68.3%, SD 23.7%) (Fig. 3). The mean difference between the two conditions was 3 1.7%, which was statistically significant (SE 7.49, t 4.23, P < 0.01). Thus, the mean size of the unloading reflex was smaller under both UNLOAD-FLEX and UNLOAD-EXTEND, compared with the UNLOAD condition (Table 1). Under the LOAD-FLEX condition, the subject flexed the finger as soon as possible after he perceived the stimulus (Figs. 4 and 5). The size of the stretch retlex was found to range from 0% to 130% of the values found under the LOAD condition (mean 83.7%, SD 38.51%). The mean difference between the conditions (16.3%) was not statistically significant (t 1.34, P> 0.1). Under the LOAD-EXTEND condition, the size of the stretch reflex ranged from 43% to 138% of the value found under the LOAD condition (Fig. 6). Again, the mean difference (2.7%) was not statistically significant (t 0.28, P > 0.1) (Table 2). DISCUSSION Three principal findings emerged from this study: First, stretch and unloading reflexes were easily demonstrated in a small muscle of the hand, Sec-
354
ANGEL
EMG
AND WEINRICH
I
Ll
cm 100 ins
FIG. 4. Stretch reflex. The initial conditions were the same as in Fig. 1. At the time shown by the upturn of the velocity trace, the force was increased for 20 ms, causing extension of the finger and stretching the flexor muscle, which responded with an increase of EMG activity (arrow).
ond, these reflexes were not abolished by the subject’s preparatory set, i.e., the intention to contract or relax the muscles. Third, the reflexes were not generally modulated in an “appropriate” direction by the subject’s preparatory set. An exception was the fact that the decrease of EMG activity after unloading was less marked when the subject was prepared to contract the muscle. The tendon jerk has been examined by neurologists for more than a century, but its reflex nature was still controversial when Shenington wrote a
EMG
FIG. 5. LOAD-FLEX condition. The subject was instructed to flex the finger as soon as possible in response to the stretching force. The position trace showed an initial extension caused by the motor and then flexion produced voluntarily, The stretch reflex (arrow) was measured as 115% of that seen in Fig. 4.
HAND MUSCLE EMG
355
REFLEXES
I
Position
,
11cm 100 ms
FIG. 6. LOAD-EXTEND. The subject was instructed to extend the finger in response to the stretching force. The position trace showed an initial extension caused by the motor and then an extension produced voluntarily. The stretch reflex (arrow) was measured as 7 1% of that seen in Fig. 4.
textbook account in 1900 ( 19). Forty years elapsed before Lloyd (12, 13) finally proved that the reflex response to a brief muscle stretch is mediated “through arcs of two neurons.” There followed a series of classic experiments which demonstrated the mechanism of the stretch reflex in great detail ( 10, 11,14). However, our knowledge of this reflex has been derived mainly from TABLE 2 Stretch Reflex in First Dorsal Interosseous Muscle Test condition LOAD
LOAD-FLEX
LOAD-EXTEND
Subject
mm”
%
mm”
%
mm”
%
D.S. R.A. M.P. T.G. P.S. D.E. J.M. M.W. S.W. J.K. Mean + SD
21 26 23 26 24 103 62 76 38 78
100 100 100 100 100 loo 100 100 100 100
24 20 18 29 12 134 43 70 0 90
114 77 78 112 50 130 69 92 0 115 83.7 + 38.5
19 36 10 30 27 144 43 74 37 55
90 138 43 115 113 140 69 97 97 71 97.3 +- 30.8
’ Largest upward deflection of EMG tracing within 100 ms after loading. Value under the LOAD condition is taken as 100%.
356
ANGEL
AND WEINRICH
the study of large muscles in the hind limb of the cat. Similarly, the physiology of the unloading reflex has been investigated in experiments with large, proximal muscles (2,7). In recent studies of long-latency reflexes, attention has been directed to muscles of the upper limb, including biceps (5) wrist flexors (4, 9), and the flexor pollicis longus (1,15). Except for one study involving the flexor pollicis brevis (16) and two involving the first dorsal interosseous (3,17), the intrinsic muscles of the hand have been relatively neglected. The hand musculature appears to deserve study from the clinical, as well as the scientific viewpoint. As noted below, these small muscles are represented by a relatively large area of the motor cortex (2 I), and corticospinal fibers project directly upon their motoneurons (8). The direct cortical projections are most profuse to the motoneurons of the distal muscles and explain the preferential accessibility of these muscles to cortical stimulation (13). Hence, it is not surprising that a loss of manual dexterity is a sensitive indicator of corticospinal tract disease. Because of these strong corticospinal projections, one might suppose that the brain can modulate the segmental reflexes affecting the intrinsic hand muscles. Tanji and Evarts (20) noted that changes of pyramidal tract neuron activity with “intention” or “motor set” provide a mechanicm for suprasegmental control and presetting of spinal cord reflex excitability specific to the nature of an impending movement. Thus, the stretch reflex might be suppressed when the subject intends to relax the muscle and increased when he intends to contract it. Similarly, the unloading reflex might be suppressed when the subject intends to contract the muscle and increased when he intends to relax it. Of these predictions, only one was confirmed in our experiments. Under the UNLOAD-FLEX condition, the subject flexed the finger as soon as possible after perceiving the stimulus. This response called for contraction of the muscles that ordinarily show a “silent period” after unloading. This voluntary contraction would be hastened by abolition or a decrease in size of the unloading reflex. In 8 of 10 subjects, this reflex was, in fact, reduced in amplitude under the UNLOAD-FLEX condition. Thus, it was modulated in the “appropriate” way, though not completely suppressed. Under the UNLOAD-EXTEND condition, the subject was prepared to extend the finger, i.e., relax the flexor muscles immediately after perceiving the stimulus. Although the “appropriate” modulation would be an enhancement of the silent period, 8 of 10 subjects showed the opposite effect; i.e., the unloading reflex was smaller under the UNLOAD-EXTEND condition. Under the LOAD-FLEX and LOAD-EXTEND conditions, there was no significant change in size of the stretch reflex.
HAND
MUSCLE
REFLEXES
351
These experiments demonstrated two well-known spinal reflexes in an intrinsic hand muscle. On the assumption that the control of this muscle is “dominated” by corticospinal signals, we tried to modulate the reflexes by requiring subjects to alter their “motor set.” The data showed that changes of test conditions had no effect on the latency of either the stretch or the unloading reflex and no effect on the size of the stretch reflex. The only “appropriate” change was a decrease in size of the unloading reflex under the test condition that called for muscular contraction. However, there was also a decreased unloading reflex under the condition in which the subject was prepared to relax the muscle. We conclude that stretch and unloading reflexes of this hand muscle, like those of the large, proximal muscles, are relatively autonomous. These spinal reflexes are not readily abolished or modulated to meet the demands of an intended voluntary movement. REFERENCES 1. AKAZAWA, K., T. E. MILNER, AND R. B. STEIN. 1983. Modulation of reflex EMG and stiffnessin response to stretch of human finger muscle. J. Neurophysiol. 49: 16-27. 2. ANGEL, R. W., W. EPPLER, AND A. IANNONE. 1965. Silent period produced by unloading of muscle during voluntary contraction. J. Physiol. (London) 180: 864-870. 3. BULLER, N. P., R. GARNET-~, AND J. A. STEPHENS. 1980. The reflex responses of single motor units in human hand muscles following muscle afferent stimulation. J. Physiol. (London)
303: 337-349.
4. Calancie, C., and P. Bawa. 1985. Firing patterns of human flexor carpi radialis during the stretch reflex. J. Neurophysiol. 53: 1179-l 193. 5. COOKE, J. D., AND M. J. EASTMAN. 1977. Long-loop reflexes in the tranquilized monkey. Exp. Brain Res. 21: 49 l-500. 6. GARLAND, H., R. W. ANGEL, AND R. D. MELEN. 197 1. A state variable averaging filter for electromyogram processing. Med. Biol. Eng. 10: 559-560. 7. HANSEN, K., AND P. HOFFMAN. 1922. Weitere Untersuchungen iiber die Bedeutung der Eigenreflexe fur unsere Bewegungen. I. Anspannungs- und Entspannungsreflex. Z. Biol. 75: 293-304. 8. LAWRENCE, D. G., AND D. A. HOPKINS. 1976. The development of motor control in the rhesus monkey: evidence concerning the role of corticomotoneuronal connections. Brain
99: 235-254.
9. LEE, R. G., AND W. G. TAI-~ON. 1975. Motor responses to sudden limb displacements in primates with specific CNS lesions and in human patients with motor system disorders. Can. J. Neurol.
Sci. 2: 285-293.
10. LIDDELL, E. G. T., AND C. C. SHERRINGTON. 1924. Reflexes in response to stretch (myotatic reflexes). Proc. Sot. Land. B 96: 2 12-242. 11. LIDDELL, E. G. T. 1960. The Discovery of Reflexes. Oxford Univ. Press, Clarendon. 12. LLOYD, D. P. C. 1943. Reflex action in relation to pattern and peripheral source of afferent stimulation. J. Neurophysiol. 6: 1 1 1- 119. 13. LLOYD, D. P. C. 1943. Conduction and synaptic transmission of reflex response to stretch in spinal cats. J. Neurophysiol. 5: 3 17-326. 14. LLOYD, D. P. C. 1946. Integrative pattern of excitation and inhibition in two-neuron reflex arcs. J. Neurophysiol. 9: 439-444.
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AND WEINRICH
15. MARSDEN, C. D., P. A. MORTON, ANDH. B. MORTON.1976.Servoactionin the human thumb.J. Physiol. (London) 257: l-44. 16. MATTHEWS, P. B. C. 1984.The contrastingstretchreflexresponses of the longandshort Bexormuscles ofthe humanthumb.J. Physiol. (London) 34% 545-558. 17. NOTH,J., H. R. MATTHEWS ANDH. H. PRIEDMANN. 1984.Longlatencyreflexforceof humanfingermuscles in response to sinusoidal movement.Exp. Bruin Res. 55: 317324.
18. PHILLIPS, C. G., ANDR. PORTER. 1977. Corticospinal Neurons: Their Role in Movement, pp.42-46.AcademicPress, London. 19. SHERRINGTON, C. S. 1900.The knee-jerkand alliedphenomenon. Page870-873in SHAFER, E.A., Ed., TextbookofPhysiology, Vol. II. Pentland,Edinburgh. 20. TANJI,J., ANDE. EVARTS.1975.Anticipatoryactivity of motorcortexneuronsin relation to directionofan intendedmovement. J. Neurophysiol. 39: 1062-1068. 21. WOOLSEY, C. N., P.H. SEX-~LAGE, D. R. MEYER,W. SENCER, T. P. HAMW, ANDA. M. TRAVIS.1952.Patternsof localizationin precentraland“supplementary” motorareas andtheir relationto the conceptof a premotorarea.Res. Publ. Assoc. Res. Nerv. Ment. Dis. 30: 238-264.