Exp Brain Res (1992) 90:217-220
Experimental BrainResearch 9 Springer-Verlag1992
Research Note The effects of wrist muscle vibration on human voluntary elbow flexion-extension movements T. Kasai 1, M. Kawanishi 2, and S. Yahagi 3 t Department of Human Movement Studies, Faculty of Integrated Arts and Sciences, HiroshimaUniversity, 1-1-89, Higashisendamachi, Naka-ku, Hiroshima 730, Japan 2 Department of Sports Science, Hiroshima BunkyoWomen's College, 1-2-1, Kabehigashi,Asakita-ku, Hiroshima 731-02, Japan 3 Department of Sports Science, Hiroshima Syudo University, 1717, Ohtsuka, Numata-cho, Asaminami-ku,Hiroshima 731-31, Japan Received September 27, 1991 / Accepted March 16, 1992
Summary. The effect of forearm muscle tendon vibration during alternating step flexion-extension movements about the elbow was studied in normal humans. In one experiment, a vibrator was mounted over either the forearm flexor or the extensor muscle. In a second experiment, a vibrator was mounted over either the forearm muscle or the biceps muscle. In both experiments, vibration was applied either to a single muscle or simultaneously to both muscles during elbow flexion-extension movements. After a period of practice, subjects learned the required movements and were able to make them with their eyes closed. Application of vibration to the forearm and the biceps muscle during extension movements produced an undershoot of the required endmovement position. Moreover, application of highfrequency vibration (100 Hz) to the forearm extensor and flexor muscle produced an overshoot of the required end-movement position. The observed results are consistent with vibration induced activation of muscle spindle receptors not only in the lengthening muscle during movement but also in the forearm muscles. It is suggested that the pattern of distribution of muscle spindle afferent from the forearm muscle onto a-motoneurons of muscles acting at the elbow has played an important role of alternating step flexion-extension movements. Key words: Muscle vibration - Spindle afferents - Elbow movement - Forearm muscle - Human
In a number of studies of goal-directed elbow movements, a general finding has been that vibration of the antagonist, i.e. passively lengthening muscle, produces an undershoot of the intended target position whereas vibration of the actively shortening agonist has relatively little effect upon accuracy (Capady and Cooke 1981, 1983; Bullen and Brunt 1986; Sitting et al. 1985). This evidence suggests that muscle receptors such as muscle Correspondence to .' T. Kasai
spindles in the antagonist are a particularly important source of proprioceptive input during normal movements (Goodwin et al. 1972). The vibration-induced undershoot was associated with increased EMG activity of the vibrated (antagonist) muscle and a resultant increase in the ratio of the antagonist to agonist EMG activity (Capady and Cooke 1983). Cody et al. (1990) reported that vibration-induced undershoot of extension movements resulted largely from a reduction in activity in the prime-mover rather than increased antagonist activity. Furthermore, microneurographic recordings demonstrated that spindle primaries are powerfully excited by vibration of both relaxed and contracting muscles and are relatively more sensitive than spindle secondaries or tendon organs (Burke et al. 1976a, b; Roll and Vedel 1982; Gilholdes et al. 1986; Roll et al. 1989). These reports support the above mentioned view that proprioceptive sensory input from the passively lengthening antagonist muscle, arising mainly from muscle spindle Ia afferents, plays an important role. Recently, Cavallari and Katz (1989) reported the pattern of distribution of Ia afferents from muscles acting at the wrist onto motoneurons of muscles acting at the elbow. Activation of group I afferents contained in the median nerves and originating from wrist flexors and pronators, resulted in a strong, short latency facilitation of biceps brachii motoneurons. A similar effect was also produced by stimulation of group I afferents in the radial nerve. The latency of both median and radial-induced facilitation was compatible with a monosynaptic linkage. Stimulation of group I afferents in the median or the radial nerves produced inhibition of triceps motoneurons, with a latency compatible with a disynaptic linkage. We, therefore, hypothesized that vibration of the forearm flexor or extensor tendons should affect elbow flexion-extension movements through these median and radial nerve group I projections to biceps and triceps motoneurons. Two experimental procedures were used to estimate the effects of forearm muscle vibration on elbow flexionextension movements. (1) The amplitude of elbow
218
flexion-extension movements made without vibration at the forearm was compared to that with vibration. (2) The amplitude of elbow flexion-extension movements without excitatory and inhibitory convergence was compared to that with convergence. Experiments were made with eight normal humans who gave informed consent. To ensure the reproducibility of the results and to check the spread of the vibration wave, each experimental condition was repeated several times with each subject. During the experiment the subject was seated in a chair and grasped a manipulandum handle whose proximal end supported the elbow. The handle was connected to the shaft of a linear potentiometer and could be moved in the horizontal plane by either flexion or extension movements about the elbow joint (Kasai 1991). Subjects made alternate flexion and extension movements about the elbow cued by an acoustic signal given once every second. Target positions were not mechanically detectable and were not bounded by mechanical stops. Subjects were instructed to move "briskly and accurately" between the targets (Capady and Cooke 1981, 1983). After practice with visual guidance, subjects performed the task without visual guidance, i.e. with their eyes closed. All subjects were well practiced at the task and could move between the target position (flexion/ extension angle is about 40 ~) equally well without visual guidance. After 30 trials have passed since the experimental trial started, vibration was provided to muscle tendon during 20 trials. Subsequently, the subject was instructed to continue alternating step flexion-extension movements as same as initial trials in spite of vibration being stopped.
Vibration on forearm flexor
Vibration on forearm extensor
A
40 Hz
In the first experiment, vibrators were mounted over the forearm extensor and flexor tendons using adjustable velcro straps. Vibration could be applied to each tendon either separately or simultaneously during flexion and extension movements. In the second experiment, one vibrator was mounted over the forearm extensor or flexor tendon and another was mounted over the biceps tendon. Vibration could thus be applied to either of the forearm extensor or flexor tendons and to the biceps tendon either separately or simultaneously. Vibration frequency was varied between 30-100 Hz. Experimental sequences were controlled by a personal computer system (NEC model PC-9801vm2) which was specially modified for the present study. The position of the handle and thus of the forearm (derived from a precision potentiometer) was recorded and displayed on a rectigraph (SANEI-8K 13) together with a signal indicating the time of application of vibration. This made it possible to determine the effect of the relevant phenomena. Vibration of either or both forearm muscles resulted in an undershoot of elbow extension movements with vibration frequencies of 50 Hz or greater. The degree of undershoot depended on the vibration frequency being greatest with 100 Hz vibration (Fig. 1A and B, second traces). During 100 Hz subjects also showed a slight overshoot of the flexion target (Fig. 1A and B, arrows in third traces). Subjects verbally reported that vibration separately applied to the individual forearm muscles induced "easier" flexion movements. Vibration simultaneously applied to both forearm muscles also produced an undershoot of elbow extension movements (Fig. 1C). Such undershoot occurred at vibration frequencies which were ineffective when applied to the individual tendons.
B
40 Hz
50 Hz
50 Hz
100Hz
100Hz
Vibration on both forearms
C
30 Hz
40 Hz
20s
Fig. 1A-C. Effects of continuous muscle vibration during step elbow flexion-extension movement (data from subject SY). A, B Show records of arm position during vibration separately applied to the forearm extensor (A) and forearm flexor (B). First and second traces are records of arm position during subthreshold (40 Hz) and suprathreshold (50 Hz) vibration, respectively. Third traces are records of arm position during high frequency (100 Hz) vibration. Arrows
I E 40 ~ F
show overshoot of flexion movement. C Shows records of arm position during vibration simultaneously applied to both forearms. Tendon vibration was applied during the period indicated by the solid bar over each position record. E; elbow extension movement, F; elbow flexion movement. The horizontal calibration represents 20 s and the vertical calibration for position are 40 deg
2]9 Similar results were obtained in seven of the 8 subjects. One subject was discarded from the study as vibration produced no consistent effect on the end-movement position. In the early stage of the first experiment, under the condition where vibration was applied to the forearm extensor, we could not obtain an undershoot of elbow extension movements, but rather an undershoot of elbow flexion movements. The results indicated that the spread of the forearm vibration wave produced direct activation of triceps brachii spindle endings. Therefore, we changed the location or reduced the frequency of the vibrator, and checked the spread of the vibration wave to see whether the results were modified or not. Furthermore, we examined the reproducibility of the results. This procedure was used with every subject. Furthermore, when vibration was applied to the forearm flexor, the same procedure was used to check the spread of the vibration wave to muscle spindle of other muscles. Figure 2 shows results when one vibration was applied to the forearm muscle and another was applied to the biceps muscle. Vibration separately applied to the forearm extensor, flexor or biceps muscles resulted in an undershoot of elbow extension movements with vibration frequencies o f 50 Hz. However, vibration frequencies of 40 Hz were ineffective, similar to the result shown in Fig. 1A and B (Fig. 2A-C). Vibration simultaneously applied to the forearm extensor and biceps muscles with vibration frequencies of 40 Hz produced an undershoot Vibration on forearm extensor
A
40 Hz
of elbow extension movements (Fig. 2D). Such undershoot occurred when vibration was applied to the forearm flexor and biceps muscles (Fig. 2E). A similar results was found in six subjects in spite of individual differences in the amount of undershoot. Modification of active movements by muscle vibration has been noted by several authors (Goodwin et al. 1972; Capady and Cooke 1981, 1983; Sitting et al. 1985; Bullen and Brunt 1986; Cody et al. 1990; Inglis and Frank 1990; Inglis et al. 1991). A consistent finding has been that antagonist vibration produced an undershoot of the required end-movement position whereas agonist vibration has little or no effect on the correct attainment of final position. These effects of muscle vibration during movement are consistant with the activation of the lengthsensitive muscle spindle receptors. On the other hand, although Capady and Cooke (1983) reported that when the vibrator was attached over the forearm there was no effect on the attainment o f the correct end position for either the flexion or extension movements, in the present experiment, vibration of both forearm muscles resulted in an undershoot of only elbow extension movement when vibration frequency exceeded a threshold level (Fig. 1A and B). Subthreshold vibrations (40 Hz) simultaneously applied to the forearm extensor and flexor tendon also resulted in an undershoot of elbow extension movement (Fig. 1C). Moreover, high frequency vibration (100 Hz, see Fig. 1A and B, third traces), not only produced undershoot of extension movements but also
Vibration on biceps brachii
C
50 Hz
40 Hz
50 Hz
Vibration on forearm extensor and biceps
D Vibration on forearm flexor
B
40 Hz
40 Hz
Fig. 2A-E. Effects of continuous muscle vibration Vibration on forearm flexor and biceps
E
40 Hz
50 Hz
20s
during step elbow flexion-extension movement (data from subject MK). A-C Are shown records of arm position during vibration separately applied to the forearm extensor (A), to the forearm flexor (B) and to the biceps (C). First and second traces are the same as seen in Fig. 1A, B. D, E Are shown records of arm position during subthreshold vibration simultaneously applied to the forearm extensor and the biceps (D), and to the forearm flexor and the biceps (E). Same notation as in Fig. 1
220 an overshoot of flexion movements (Fig. 1A and B, arrows in third traces). It is possible that spread of the forearm vibration wave produced direct activation of biceps or triceps spindle endings (Katz et al. 1977, 1991). However, the present results could be explained by the pattern of projections of G r o u p I afferents from forearm muscles to motoneurons supplying biceps and triceps muscles (Cavallari and K a t z 1989). T h a t is, the activation of group I afferents originating from wrist flexors and extensors would produce inhibition of the triceps brachii motoneurons and a resulting undershoot o f extensor movements. Similarly, activation of group I afferents from wrist flexors and extensors facilitates biceps brachii motoneurons, thus producing an overshoot of flexion movements during high frequency vibration. It is, however, not clear from the present results why overshoot of flexion m o v e m e n t was observed only with high frequency vibration. It is of interest that subthreshold vibration applied simultaneously either to both forearm muscles (Fig. 1C) or to the forearm and biceps muscle (Fig. 2D and E) resulted in an undershoot of elbow extensions whereas the same vibration applied to an individual muscle alone had no effect. These results suggest that group I afferents originating f r o m wrist muscles and from the biceps muscle converge onto the same inhibitory interneurons. Therefore, the present findings indicate that when the elbows are used in eating, drawing or other kinds of manual activity, the pattern of distribution of group I afferents f r o m muscles acting at the wrist onto motoneurons of muscles acting at the elbow has an important role, i.e. supporting the biceps brachii and inhibiting the triceps brachii when the reaching to a target changes into a holding movement.
Acknowledgements. The authors wish to express their gratitude to Professor J.D. Cooke for reading and commenting upon the manuscript and also for scrutinizing the English. References Bullen AR, Brunt D (1986) Effect of tendon vibration on unimanual and bimanual movement accuracy. Exp Neurol 93 : 311-319
Burke D, Hagbarth K-E, Lofstedt L, Wallin BG (1976a) The responses of human muscle spindle endings to vibration of noncontracting muscles. J Physiol (London) 261 : 673-693 Burke D, Hagbarth K-E, Lofstedt L, Wallin BG (1976b) The responses of human muscle spindle endings to vibration of contracting muscles. J Physiol (London) 261:695-711 Capady C, Cooke JD (1981) The effects of muscle vibration on the attainment of intended final position during voluntary human arm movements. Exp Brain Res 42:228-230 Capady C, Cooke JD (1983) Vibration-induced changes in movement-related EMG activity in humans. Exp Brain Res 52:139-146 Cavallari P, Katz R (1989) Pattern of projections of group ! afferents from forearm muscles to motoneurones supplying biceps and triceps muscles in man. Exp Brain Res 78:465-478 Cody FWJ, Schwartz MP, Smit GP (1990) Propfioceptive guidance of human voluntary wrist movements studied using muscle vibration. J Physiol (London) 427:455-470 Gilhodes JC, Roll JP, Tardy-Gervet MF (1986) Perceptual and motor effects of agonist-antagonist muscle vibration in man. Exp Brain Res 61 : 395-402 Goodwin GM, McCloskey DI, Mathews PBC (1982) The contribution of muscle afferents to kinesthesia shown by vibration induced illusions of movement and by the effects of paralyzing joint afferents. Brain 95:705-748 Inglis JT, Frank JS (1990) The effect of agonist/antagonist muscle vibration on human position sense. Exp Brain Res 81 : 573-580 Inglis JT, Frank JS, Inglis B (1991) The effect of muscle vibration on human position sense during movements controlled by lengthening muscle contraction. Exp Brain Res 84:631-634 Kasai T (1991) An empirical note on tonic neck reflexes: control of the upper limb's proprioceptive sensation. Percept Mot Skills 72: 955-960 Katz R, Morin C, Pierrot-Deseilligny E, Hibino R (1977) Conditioning of H-reflex by a preceding subthreshold tendon reflex stimulus. J Neurol Neurosurg Psychiat 40:575-580 Katz R, Penicaud A, Rossi A (1991) Reciprocal Ia inhibition between elbow flexors and extensors in the human. J Physiol (London) 437:269-286 Roll JP, Vedel JP (1982) Kinesthetic role of muscle afferents in man, studies by tendon vibration and rnicroneurography. Exp Brain Res 47:177-190 Roll JP, Vedel JP, Ribot E (1989) Alteration of proprioceptive messages induced by tendon vibration in man. Exp Brain Res 76: 213-222 Sitting AC, Denier vander Gon JJ, Gielen CCAM, van Wijk AJM (1985) The attainment of target position during step-tracking movements despite a shift of initial position. Exp Brain Res 60: 407-410
Experimental BrainResearch 9 Springer-Verlag1992
Research Note The effects of wrist muscle vibration on human voluntary elbow flexion-extension movements T. Kasai 1, M. Kawanishi 2, and S. Yahagi 3 t Department of Human Movement Studies, Faculty of Integrated Arts and Sciences, HiroshimaUniversity, 1-1-89, Higashisendamachi, Naka-ku, Hiroshima 730, Japan 2 Department of Sports Science, Hiroshima BunkyoWomen's College, 1-2-1, Kabehigashi,Asakita-ku, Hiroshima 731-02, Japan 3 Department of Sports Science, Hiroshima Syudo University, 1717, Ohtsuka, Numata-cho, Asaminami-ku,Hiroshima 731-31, Japan Received September 27, 1991 / Accepted March 16, 1992
Summary. The effect of forearm muscle tendon vibration during alternating step flexion-extension movements about the elbow was studied in normal humans. In one experiment, a vibrator was mounted over either the forearm flexor or the extensor muscle. In a second experiment, a vibrator was mounted over either the forearm muscle or the biceps muscle. In both experiments, vibration was applied either to a single muscle or simultaneously to both muscles during elbow flexion-extension movements. After a period of practice, subjects learned the required movements and were able to make them with their eyes closed. Application of vibration to the forearm and the biceps muscle during extension movements produced an undershoot of the required endmovement position. Moreover, application of highfrequency vibration (100 Hz) to the forearm extensor and flexor muscle produced an overshoot of the required end-movement position. The observed results are consistent with vibration induced activation of muscle spindle receptors not only in the lengthening muscle during movement but also in the forearm muscles. It is suggested that the pattern of distribution of muscle spindle afferent from the forearm muscle onto a-motoneurons of muscles acting at the elbow has played an important role of alternating step flexion-extension movements. Key words: Muscle vibration - Spindle afferents - Elbow movement - Forearm muscle - Human
In a number of studies of goal-directed elbow movements, a general finding has been that vibration of the antagonist, i.e. passively lengthening muscle, produces an undershoot of the intended target position whereas vibration of the actively shortening agonist has relatively little effect upon accuracy (Capady and Cooke 1981, 1983; Bullen and Brunt 1986; Sitting et al. 1985). This evidence suggests that muscle receptors such as muscle Correspondence to .' T. Kasai
spindles in the antagonist are a particularly important source of proprioceptive input during normal movements (Goodwin et al. 1972). The vibration-induced undershoot was associated with increased EMG activity of the vibrated (antagonist) muscle and a resultant increase in the ratio of the antagonist to agonist EMG activity (Capady and Cooke 1983). Cody et al. (1990) reported that vibration-induced undershoot of extension movements resulted largely from a reduction in activity in the prime-mover rather than increased antagonist activity. Furthermore, microneurographic recordings demonstrated that spindle primaries are powerfully excited by vibration of both relaxed and contracting muscles and are relatively more sensitive than spindle secondaries or tendon organs (Burke et al. 1976a, b; Roll and Vedel 1982; Gilholdes et al. 1986; Roll et al. 1989). These reports support the above mentioned view that proprioceptive sensory input from the passively lengthening antagonist muscle, arising mainly from muscle spindle Ia afferents, plays an important role. Recently, Cavallari and Katz (1989) reported the pattern of distribution of Ia afferents from muscles acting at the wrist onto motoneurons of muscles acting at the elbow. Activation of group I afferents contained in the median nerves and originating from wrist flexors and pronators, resulted in a strong, short latency facilitation of biceps brachii motoneurons. A similar effect was also produced by stimulation of group I afferents in the radial nerve. The latency of both median and radial-induced facilitation was compatible with a monosynaptic linkage. Stimulation of group I afferents in the median or the radial nerves produced inhibition of triceps motoneurons, with a latency compatible with a disynaptic linkage. We, therefore, hypothesized that vibration of the forearm flexor or extensor tendons should affect elbow flexion-extension movements through these median and radial nerve group I projections to biceps and triceps motoneurons. Two experimental procedures were used to estimate the effects of forearm muscle vibration on elbow flexionextension movements. (1) The amplitude of elbow
218
flexion-extension movements made without vibration at the forearm was compared to that with vibration. (2) The amplitude of elbow flexion-extension movements without excitatory and inhibitory convergence was compared to that with convergence. Experiments were made with eight normal humans who gave informed consent. To ensure the reproducibility of the results and to check the spread of the vibration wave, each experimental condition was repeated several times with each subject. During the experiment the subject was seated in a chair and grasped a manipulandum handle whose proximal end supported the elbow. The handle was connected to the shaft of a linear potentiometer and could be moved in the horizontal plane by either flexion or extension movements about the elbow joint (Kasai 1991). Subjects made alternate flexion and extension movements about the elbow cued by an acoustic signal given once every second. Target positions were not mechanically detectable and were not bounded by mechanical stops. Subjects were instructed to move "briskly and accurately" between the targets (Capady and Cooke 1981, 1983). After practice with visual guidance, subjects performed the task without visual guidance, i.e. with their eyes closed. All subjects were well practiced at the task and could move between the target position (flexion/ extension angle is about 40 ~) equally well without visual guidance. After 30 trials have passed since the experimental trial started, vibration was provided to muscle tendon during 20 trials. Subsequently, the subject was instructed to continue alternating step flexion-extension movements as same as initial trials in spite of vibration being stopped.
Vibration on forearm flexor
Vibration on forearm extensor
A
40 Hz
In the first experiment, vibrators were mounted over the forearm extensor and flexor tendons using adjustable velcro straps. Vibration could be applied to each tendon either separately or simultaneously during flexion and extension movements. In the second experiment, one vibrator was mounted over the forearm extensor or flexor tendon and another was mounted over the biceps tendon. Vibration could thus be applied to either of the forearm extensor or flexor tendons and to the biceps tendon either separately or simultaneously. Vibration frequency was varied between 30-100 Hz. Experimental sequences were controlled by a personal computer system (NEC model PC-9801vm2) which was specially modified for the present study. The position of the handle and thus of the forearm (derived from a precision potentiometer) was recorded and displayed on a rectigraph (SANEI-8K 13) together with a signal indicating the time of application of vibration. This made it possible to determine the effect of the relevant phenomena. Vibration of either or both forearm muscles resulted in an undershoot of elbow extension movements with vibration frequencies of 50 Hz or greater. The degree of undershoot depended on the vibration frequency being greatest with 100 Hz vibration (Fig. 1A and B, second traces). During 100 Hz subjects also showed a slight overshoot of the flexion target (Fig. 1A and B, arrows in third traces). Subjects verbally reported that vibration separately applied to the individual forearm muscles induced "easier" flexion movements. Vibration simultaneously applied to both forearm muscles also produced an undershoot of elbow extension movements (Fig. 1C). Such undershoot occurred at vibration frequencies which were ineffective when applied to the individual tendons.
B
40 Hz
50 Hz
50 Hz
100Hz
100Hz
Vibration on both forearms
C
30 Hz
40 Hz
20s
Fig. 1A-C. Effects of continuous muscle vibration during step elbow flexion-extension movement (data from subject SY). A, B Show records of arm position during vibration separately applied to the forearm extensor (A) and forearm flexor (B). First and second traces are records of arm position during subthreshold (40 Hz) and suprathreshold (50 Hz) vibration, respectively. Third traces are records of arm position during high frequency (100 Hz) vibration. Arrows
I E 40 ~ F
show overshoot of flexion movement. C Shows records of arm position during vibration simultaneously applied to both forearms. Tendon vibration was applied during the period indicated by the solid bar over each position record. E; elbow extension movement, F; elbow flexion movement. The horizontal calibration represents 20 s and the vertical calibration for position are 40 deg
2]9 Similar results were obtained in seven of the 8 subjects. One subject was discarded from the study as vibration produced no consistent effect on the end-movement position. In the early stage of the first experiment, under the condition where vibration was applied to the forearm extensor, we could not obtain an undershoot of elbow extension movements, but rather an undershoot of elbow flexion movements. The results indicated that the spread of the forearm vibration wave produced direct activation of triceps brachii spindle endings. Therefore, we changed the location or reduced the frequency of the vibrator, and checked the spread of the vibration wave to see whether the results were modified or not. Furthermore, we examined the reproducibility of the results. This procedure was used with every subject. Furthermore, when vibration was applied to the forearm flexor, the same procedure was used to check the spread of the vibration wave to muscle spindle of other muscles. Figure 2 shows results when one vibration was applied to the forearm muscle and another was applied to the biceps muscle. Vibration separately applied to the forearm extensor, flexor or biceps muscles resulted in an undershoot of elbow extension movements with vibration frequencies o f 50 Hz. However, vibration frequencies of 40 Hz were ineffective, similar to the result shown in Fig. 1A and B (Fig. 2A-C). Vibration simultaneously applied to the forearm extensor and biceps muscles with vibration frequencies of 40 Hz produced an undershoot Vibration on forearm extensor
A
40 Hz
of elbow extension movements (Fig. 2D). Such undershoot occurred when vibration was applied to the forearm flexor and biceps muscles (Fig. 2E). A similar results was found in six subjects in spite of individual differences in the amount of undershoot. Modification of active movements by muscle vibration has been noted by several authors (Goodwin et al. 1972; Capady and Cooke 1981, 1983; Sitting et al. 1985; Bullen and Brunt 1986; Cody et al. 1990; Inglis and Frank 1990; Inglis et al. 1991). A consistent finding has been that antagonist vibration produced an undershoot of the required end-movement position whereas agonist vibration has little or no effect on the correct attainment of final position. These effects of muscle vibration during movement are consistant with the activation of the lengthsensitive muscle spindle receptors. On the other hand, although Capady and Cooke (1983) reported that when the vibrator was attached over the forearm there was no effect on the attainment o f the correct end position for either the flexion or extension movements, in the present experiment, vibration of both forearm muscles resulted in an undershoot of only elbow extension movement when vibration frequency exceeded a threshold level (Fig. 1A and B). Subthreshold vibrations (40 Hz) simultaneously applied to the forearm extensor and flexor tendon also resulted in an undershoot of elbow extension movement (Fig. 1C). Moreover, high frequency vibration (100 Hz, see Fig. 1A and B, third traces), not only produced undershoot of extension movements but also
Vibration on biceps brachii
C
50 Hz
40 Hz
50 Hz
Vibration on forearm extensor and biceps
D Vibration on forearm flexor
B
40 Hz
40 Hz
Fig. 2A-E. Effects of continuous muscle vibration Vibration on forearm flexor and biceps
E
40 Hz
50 Hz
20s
during step elbow flexion-extension movement (data from subject MK). A-C Are shown records of arm position during vibration separately applied to the forearm extensor (A), to the forearm flexor (B) and to the biceps (C). First and second traces are the same as seen in Fig. 1A, B. D, E Are shown records of arm position during subthreshold vibration simultaneously applied to the forearm extensor and the biceps (D), and to the forearm flexor and the biceps (E). Same notation as in Fig. 1
220 an overshoot of flexion movements (Fig. 1A and B, arrows in third traces). It is possible that spread of the forearm vibration wave produced direct activation of biceps or triceps spindle endings (Katz et al. 1977, 1991). However, the present results could be explained by the pattern of projections of G r o u p I afferents from forearm muscles to motoneurons supplying biceps and triceps muscles (Cavallari and K a t z 1989). T h a t is, the activation of group I afferents originating from wrist flexors and extensors would produce inhibition of the triceps brachii motoneurons and a resulting undershoot o f extensor movements. Similarly, activation of group I afferents from wrist flexors and extensors facilitates biceps brachii motoneurons, thus producing an overshoot of flexion movements during high frequency vibration. It is, however, not clear from the present results why overshoot of flexion m o v e m e n t was observed only with high frequency vibration. It is of interest that subthreshold vibration applied simultaneously either to both forearm muscles (Fig. 1C) or to the forearm and biceps muscle (Fig. 2D and E) resulted in an undershoot of elbow extensions whereas the same vibration applied to an individual muscle alone had no effect. These results suggest that group I afferents originating f r o m wrist muscles and from the biceps muscle converge onto the same inhibitory interneurons. Therefore, the present findings indicate that when the elbows are used in eating, drawing or other kinds of manual activity, the pattern of distribution of group I afferents f r o m muscles acting at the wrist onto motoneurons of muscles acting at the elbow has an important role, i.e. supporting the biceps brachii and inhibiting the triceps brachii when the reaching to a target changes into a holding movement.
Acknowledgements. The authors wish to express their gratitude to Professor J.D. Cooke for reading and commenting upon the manuscript and also for scrutinizing the English. References Bullen AR, Brunt D (1986) Effect of tendon vibration on unimanual and bimanual movement accuracy. Exp Neurol 93 : 311-319
Burke D, Hagbarth K-E, Lofstedt L, Wallin BG (1976a) The responses of human muscle spindle endings to vibration of noncontracting muscles. J Physiol (London) 261 : 673-693 Burke D, Hagbarth K-E, Lofstedt L, Wallin BG (1976b) The responses of human muscle spindle endings to vibration of contracting muscles. J Physiol (London) 261:695-711 Capady C, Cooke JD (1981) The effects of muscle vibration on the attainment of intended final position during voluntary human arm movements. Exp Brain Res 42:228-230 Capady C, Cooke JD (1983) Vibration-induced changes in movement-related EMG activity in humans. Exp Brain Res 52:139-146 Cavallari P, Katz R (1989) Pattern of projections of group ! afferents from forearm muscles to motoneurones supplying biceps and triceps muscles in man. Exp Brain Res 78:465-478 Cody FWJ, Schwartz MP, Smit GP (1990) Propfioceptive guidance of human voluntary wrist movements studied using muscle vibration. J Physiol (London) 427:455-470 Gilhodes JC, Roll JP, Tardy-Gervet MF (1986) Perceptual and motor effects of agonist-antagonist muscle vibration in man. Exp Brain Res 61 : 395-402 Goodwin GM, McCloskey DI, Mathews PBC (1982) The contribution of muscle afferents to kinesthesia shown by vibration induced illusions of movement and by the effects of paralyzing joint afferents. Brain 95:705-748 Inglis JT, Frank JS (1990) The effect of agonist/antagonist muscle vibration on human position sense. Exp Brain Res 81 : 573-580 Inglis JT, Frank JS, Inglis B (1991) The effect of muscle vibration on human position sense during movements controlled by lengthening muscle contraction. Exp Brain Res 84:631-634 Kasai T (1991) An empirical note on tonic neck reflexes: control of the upper limb's proprioceptive sensation. Percept Mot Skills 72: 955-960 Katz R, Morin C, Pierrot-Deseilligny E, Hibino R (1977) Conditioning of H-reflex by a preceding subthreshold tendon reflex stimulus. J Neurol Neurosurg Psychiat 40:575-580 Katz R, Penicaud A, Rossi A (1991) Reciprocal Ia inhibition between elbow flexors and extensors in the human. J Physiol (London) 437:269-286 Roll JP, Vedel JP (1982) Kinesthetic role of muscle afferents in man, studies by tendon vibration and rnicroneurography. Exp Brain Res 47:177-190 Roll JP, Vedel JP, Ribot E (1989) Alteration of proprioceptive messages induced by tendon vibration in man. Exp Brain Res 76: 213-222 Sitting AC, Denier vander Gon JJ, Gielen CCAM, van Wijk AJM (1985) The attainment of target position during step-tracking movements despite a shift of initial position. Exp Brain Res 60: 407-410
