| | Co-contraction of the pronator teres and extensor carpi radialis during wrist extension movements in humansReceived 10 June 2004; received in revised form 26 June 2005; accepted 18 November 2005. published online 07 March 2006. Abstract In order to elucidate the functional significance of excitatory spinal reflex arcs (facilitation) between musculus (M.) pronator teres (PT) and M. extensor carpi radialis (ECR, longus: ECRL, brevis: ECRB) in humans, activities of the muscles were studied with electromyography (EMG) and electrical neuromuscular stimulation (ENS). In EMG study, activities of PT, ECRL, ECRB, and M. flexor carpi radialis during repetitive static (isometric) wrist extension and a series of a dynamic motion of wrist flexion/extension in the prone, semiprone, and supine positions of the forearm were recorded in 12 healthy human subjects. In the prone, semiprone, and supine positions, PT and ECR showed parallel activities during the static extension in all, eight, and eight subjects, respectively, and at the extension phase during the dynamic motion in all, eight and five subjects, respectively. These findings suggest that co-contraction of PT and ECR occurs during wrist extension movements at least with the prone forearm. The facilitation must be active during the co-contraction. In ENS study, ENS to PT was examined in 11 out of the 12 and that to ECRL was in the 12 subjects. Before ENS, the forearm was in the prone, semiprone, and supine positions. In all the subjects, ENS to PT induced a motion of forearm pronation to the maximum pronation. ENS to ECRL induced motions of wrist extension to the maximum extension and abduction (radial flexion) to 5–20 degrees of abduction regardless of the positions of the forearm. Moreover, it induced 30–80 degrees supination of the forearm from the prone position. Consequently, combined ENS to PT and ECRL resulted in motions of the extension and abduction while keeping the maximum pronation. These findings suggest that the co-contraction of PT and ECR during wrist extension movements occurs to prevent supinating the forearm. Forearm supination from the prone position should be added to one of the actions of ECRL. 1. Introduction  Musculus (M.) pronator teres (PT) arises from the medial epicondyle of the humerus (humeral head) and ulnar coronoid process (ulnar head) and attaches on the lateral surface of the radial shaft [4], [29]. It belongs to forearm pronators. M. extensor carpi radialis longus (ECRL) arises mainly from the distal third of the supracondylar ridge and attaches on the radial side of the dorsal aspect of the second metacarpal base. M. extensor carpi radialis brevis (ECRB) arises mainly from the lateral epicondyle and attaches on the radial side of the third metacarpal base. However, cross-connections between the distal tendons of ECRL and ECRB are often observed [1], [30]. They belong to wrist extensors. PT is innervated by the median nerve and ECR (ECRL and ECRB) by the radial nerve. On the other hand, excitatory and inhibitory spinal reflex arcs (facilitation and inhibition) mediated by low-threshold muscle afferents (group I afferent fibers) among muscles in the human upper limb have been studied [2], [3], [6], [7], [8], [9], [10], [13], [14], [15], [16], [17], [18], [20], [21], [22], [28]. The functional significance of the facilitation and inhibition is speculated in consideration for activities of the muscles during upper limb movements [6], [7], [14], [21]. Our recent study with a post-stimulus time histogram technique has shown facilitation from PT to ECR [25]. Group Ia afferents from the muscle spindle mediate the facilitation through monosynaptic path. Facilitation in the reverse direction seems to exist [Nakano et al., unpublished results]. In the present study, therefore, in order to clarify the functional significance of the facilitation, activities of the muscles were examined using electromyography (EMG) and electrical neuromuscular stimulation (ENS). 2. Subjects and methods  Activities of PT and ECR (ECRL and ECRB) were studied in 12 healthy human subjects (9 males and 3 females, age range 20–40 years) with EMG and ENS [19], [23], [24]. All of the subjects gave their informed consent to the experimental procedure, which was approved by the Ethics Committee of Yamagata University School of Medicine, Yamagata, Japan. The subject sat on a chair and put the forearm on a table with the shoulder flexed to 0–20 degrees of flexion and the elbow flexed to 70–90 degrees of flexion. The hand was put in the air. 2.1. EMG and goniometry EMGs of PT, ECRL, ECRB and M. flexor carpi radialis (FCR) were recorded with bipolar intramuscular electrodes made of teflon-coated stainless steel wire (75 μm in diameter, SUS 316, AM system) with distance of about 4 mm [5], [23]. The electrodes were implanted percutaneously into the muscles with 25 gauge-injection needles [25], [26], [27]. Wet carbasus absorbens was put round the shoulder and used as reference. EMGs were amplified, band pass filtered (10–1000 Hz), sampled at 2048 Hz, and fed into a data recorder (XR-50, TEAC, Tokyo) and pen recorder (RECTI-HORIZ-8K, San-ei, Tokyo). Then they were integrated (rectified and averaged) with an EMG integration program (Multi-Computer System, Giga Tex Co., Furukawa). For standardization, contraction level of the muscle was indicated by expressing the amplitude of integrated EMG as a percentage of that produced by the maximum contraction (%Max). Movements tested were repetitive static (isometric) wrist extension and a series of a dynamic motion of wrist flexion/extension in the prone (about 80 degrees of pronation), semiprone (neutral position), and supine positions (about 80 degrees of supination) of the forearm. In the static extension, the subject made an effort to extend the wrist in the position of 0–20 degrees of extension against resistance for about 5 s. The resistance was produced by the experimenter’s hand. The hand pressed the dorsum of the subject’s hand to prevent the wrist from extending. The effort was performed 3–5 times at interval of about 5 s. In the dynamic motion, the subject performed a to-and-fro motion from the maximum flexion to the maximum extension of the wrist 5 times for about 25 s. EMGs of the muscles during the maximum contraction were recorded last. The subject made the maximum effort to extend and flex the wrist, and pronate the forearm against resistance produced by the experimenter’s hand. Angular changes of a motion of the wrist in flexion/extension direction were measured using an electrogoniometer with a strain gauge (PH510, Denkikeisoku-hanbai Co., Tokyo). Data of the angular changes were fed into the data recorder and pen recorder with EMGs. 2.2. ENS study For electrical stimulation, monopolar electrodes made of teflon-coated stainless steel wire (above-mentioned product) were implanted percutaneously into each motor point of ECRL and PT with 27 gauge injection-needles [19], [24]. A guide needle of a 25 gauge spinal-needle (length: 89 mm, Top Co., Tokyo) was percutaneously inserted into the subcutaneous tissue along to the lateral intermuscular septum of the arm and used as reference. Before the implantation, locations of the motor points were examined by electrical stimulation with surface electrodes. During the implantation, electrical rectangular pulses (duration: 0.2 ms, amplitude: −20 to 0 V, frequency: 1 or 20 Hz) were occasionally delivered to the muscles through the wire electrodes and contraction of individual muscles was confirmed by inspecting and palpating the tendon or belly of them [1], [4], [29], [30]. Also it was carefully checked that no contraction of any other muscles was induced by the stimulation. For ENS study, electrical rectangular pulses (duration: 0.2 ms, amplitude: −20 to 0 V, frequency: 20 Hz) were delivered using a computer-controlled multi-channel functional electrical stimulation (FES) system which we had developed to restore motor functions of paralyzed extremities with intramuscular wire electrodes [11], [12]. EMGs of ECRL and PT were recorded with two pairs of surface electrodes (Ag/AgCl Paste Applied with PVC Tape, Vitrode, NIHON KODEN, Tokyo), which were put on the central part of the contracted muscle belly longitudinally with the distance of about 1 cm. EMGs were amplified and band pass filtered (10–350 Hz). Wet carbasus absorbens put round the shoulder was used as reference. Stimulation intensities (voltage) for the motor threshold (MT) and maximum contraction (MC) in individual muscles were determined by monitoring EMGs (motor wave) of the muscles and by palpating the belly and tendon of them. In order to stimulate each of the muscles with the intensity between MT and MC, the voltage data for MT and MC were put into the FES system. Before ENS, the examined forearm was in the prone, semiprone, and supine positions. Then motions of the forearm and wrist induced by ENS were taken video with a digital video system (NV-MX2500, Panasonic, Tokyo). Angular changes of the motions of the wrist in flexion/extension direction and the forearm in pronation/supination direction were measured with the electrogoniometers mentioned above. A motion of the wrist in abduction/adduction direction was checked with video pictures. During ENS, EMGs of PT and ECRL were recorded with the pairs of the surface electrodes mentioned above. Data of the angular changes and EMGs were fed into the data recorder and pen recorder. 3. Observations  3.1. EMG and goniometry During the static wrist extension, ECRL showed activities of 16–30, 12–32, and 13–25 %Max and ECRB those of 50–70, 42–66, and 44–61 %Max in the prone, semiprone, and supine positions of the forearm, respectively, in the 12 subjects (Table 1, Fig. 1). Slight or no activities (0–3 %Max) were seen in FCR in all the subjects. PT showed activities of 15–70, 2–30, and 17–27 %Max in the prone, semiprone, and supine positions in all, eight, and eight subjects, respectively. The activities were parallel with those of ECRL and ECRB. In the remainders, PT showed no activities (0 %Max) during the movement. | | |  | Subject | Prone | Semiprone | Supine |  |
|---|
 | ECRL (%Max) | ECRB (%Max) | PT (%Max) | FCR (%Max) | ECRL (%Max) | ECRB (%Max) | PT (%Max) | FCR (%Max) | ECRL (%Max) | ECRB (%Max) | PT (%Max) | FCR (%Max) |  |
|---|
 | K.Sa. | + | + | + | − | + | + | + | + | + | + | − | − |  |  | (20) | (68) | (38) | (0) | (19) | (62) | (2) | (3) | (15) | (55) | (0) | (0) |  |  | Y.E. | + | + | + | − | + | + | − | − | + | + | − | − |  |  | (25) | (70) | (70) | (0) | (25) | (42) | (0) | (0) | (18) | (50) | (0) | (0) |  |  | H.F. | + | + | + | − | + | + | − | − | + | + | − | − |  |  | (21) | (65) | (44) | (0) | (24) | (55) | (0) | (0) | (18) | (51) | (0) | (0) |  |  | M.S. | + | + | + | − | + | + | − | − | + | + | − | − |  |  | (25) | (62) | (35) | (0) | (28) | (52) | (0) | (0) | (21) | (48) | (0) | (0) |  |  | K.Su. | + | + | + | − | + | + | + | − | + | + | + | − |  |  | (30) | (67) | (34) | (0) | (25) | (50) | (28) | (0) | (19) | (56) | (22) | (0) |  |  | S.Y. | + | + | + | + | + | + | + | − | + | + | + | − |  |  | (28) | (65) | (35) | (2) | (32) | (55) | (30) | (0) | (21) | (52) | (27) | (0) |  |  | H.T. | + | + | + | − | + | + | + | + | + | + | + | − |  |  | (17) | (60) | (24) | (0) | (15) | (55) | (21) | (3) | (18) | (57) | (19) | (0) |  |  | Y.K. | + | + | + | − | + | + | − | + | + | + | + | − |  |  | (27) | (68) | (55) | (0) | (24) | (66) | (0) | (2) | (25) | (61) | (23) | (0) |  |  | A.M. | + | + | + | − | + | + | + | − | + | + | + | + |  |  | (16) | (54) | (27) | (0) | (15) | (55) | (24) | (0) | (13) | (50) | (18) | (3) |  |  | Y.U. | + | + | + | − | + | + | + | − | + | + | + | − |  |  | (22) | (50) | (28) | (0) | (24) | (55) | (18) | (0) | (19) | (44) | (17) | (0) |  |  | S.K. | + | + | + | + | + | + | + | + | + | + | + | − |  |  | (18) | (55) | (15) | (3) | (12) | (48) | (20) | (2) | (13) | (55) | (21) | (0) |  |  | Y.W. | + | + | + | − | + | + | + | − | + | + | + | − |  |  | (24) | (58) | (30) | (0) | (21) | (51) | (27) | (0) | (23) | (50) | (22) | (0) |  | | | |
During the series of the dynamic motion of the wrist flexion/extension, activities of ECRL and ECRB increased at the extension phase and those of FCR at the flexion phase in all the subjects (Fig. 2). Therefore peaks of the activities of ECRL and ECRB appeared at the extension phase and those of FCR at the flexion phase (Table 2). In the prone, semiprone, and supine positions, the peaks were 10–18, 10–15, and 10–14 %Max in ECRL, 21–38, 19–28, and 19–23 %Max in ECRB, and 12–17, 12–19, and 19–25 %Max in FCR, respectively. Activities of PT increased at the extension phase in all, eight and five subjects, respectively, and at the flexion phase in zero, four, and five subjects, respectively, in the prone, semiprone, and supine positions. In three subjects (YE, SY, SK in Table 2), the activities increased at both the extension and flexion phases in the semiprone and supine positions. The peaks of the activities at the extension phase were 8–17, 3–10, and 2–10 %Max, respectively, and those at the flexion phase 0, 2–3, and 8–9 %Max, respectively, in the prone, semiprone, and supine positions. The activities of PT at the extension and flexion phases were parallel with those of ECRL and ECRB (Fig. 2), and FCR (Fig. 2A), respectively. | | |  | Subject | Prone | Semiprone | Supine |  |
|---|
 | ECRL (%Max) | ECRB (%Max) | PT (%Max) | FCR (%Max) | ECRL (%Max) | ECRB (%Max) | PT (%Max) | FCR (%Max) | ECRL (%Max) | ECRB (%Max) | PT (%Max) | FCR (%Max) |  |
|---|
 | K.Sa. | E | E | E | F | E | E | | | F | E | E | | | F |  |  | (10) | (33) | (8) | (16) | (12) | (25) | (0) | (17) | (13) | (20) | (0) | (23) |  |  | Y.E. | E | E | E | F | E | E | E | F | F | E | E | E | F | F |  |  | (12) | (32) | (10) | (14) | (11) | (28) | (3) | (2) | (17) | (10) | (21) | (3) | (8) | (19) |  |  | H.F. | E | E | E | F | E | E | | | F | E | E | | | F |  |  | (15) | (28) | (12) | (12) | (13) | (20) | (0) | (15) | (11) | (19) | (0) | (21) |  |  | M.S. | E | E | E | F | E | E | E | F | F | E | E | | F | F |  |  | (11) | (24) | (8) | (13) | (10) | (21) | (8) | (3) | (12) | (12) | (19) | | (8) | (19) |  |  | K.Su. | E | E | E | F | E | E | E | | F | E | E | | | F |  |  | (15) | (26) | (9) | (13) | (10) | (22) | (9) | | (13) | (14) | (19) | (0) | (22) |  |  | S.Y. | E | E | E | F | E | E | E | F | F | E | E | E | F | F |  |  | (18) | (32) | (17) | (14) | (12) | (25) | (3) | (3) | (16) | (10) | (21) | (3) | (9) | (25) |  |  | H.T. | E | E | E | F | E | E | | | F | E | E | | F | F |  |  | (12) | (27) | (14) | (15) | (14) | (19) | (0) | (18) | (13) | (19) | | (8) | (22) |  |  | Y.K. | E | E | E | F | E | E | E | | F | E | E | E | | F |  |  | (16) | (22) | (15) | (17) | (14) | (20) | (10) | | (14) | (10) | (23) | (10) | | (25) |  |  | A.M. | E | E | E | F | E | E | E | | F | E | E | | | F |  |  | (10) | (38) | (10) | (14) | (10) | (23) | (9) | | (15) | (10) | (21) | (0) | (19) |  |  | Y.U. | E | E | E | F | E | E | | | F | E | E | | | F |  |  | (13) | (22) | (15) | (17) | (15) | (19) | (0) | (19) | (11) | (19) | (0) | (24) |  |  | S.K. | E | E | E | F | E | E | E | F | F | E | E | E | F | F |  |  | (14) | (35) | (12) | (12) | (12) | (27) | (10) | (3) | (15) | (14) | (20) | (3) | (9) | (20) |  |  | Y.W. | E | E | E | F | E | E | E | | F | E | E | E | | F |  |  | (15) | (21) | (14) | (12) | (13) | (19) | (8) | | (13) | (11) | (19) | (2) | | (19) |  | | | |
3.2. ENS study ENS to ECRL was examined in all the 12 subjects. Since ENS to PT resulted in activation of PT and the other muscles innervated by the median nerve, i.e. FCR, M. palmaris longus, in one subject, it was examined in the remaining 11 subjects. The stimulus intensity was increased linearly from MT to MC for 4–5 s. In all the 11 subjects, ENS to PT induced a motion of forearm pronation from the three positions to the maximum pronation (90 degrees of pronation). In all the 12 subjects, ENS to ECRL induced motions of wrist extension to the maximum extension (70 degrees of extension) and abduction (radial flexion) to 5–20 degrees of abduction regardless of the positions of the forearm. When the forearm was pronated before ENS, 30–80 degrees supination of the forearm from the prone position was induced in all the subjects (Fig. 3, Fig. 4). Combined ENS to PT and ECRL was examined in the 11 subjects. An increase of the stimulus intensity of ENS to PT from MT to MC fixed the forearm in the maximum pronation (Fig. 5, Fig. 6). Then an increase for ENS to ECRL from MT to MC resulted in motions of wrist extension to the maximum extension and abduction to 5–20 degrees of abduction without a motion of supination in all the 11 subjects. In this situation, a decrease of the intensity of ENS to PT from MC to MT resulted in a motion of 40–90 degrees supination from the maximum pronation while holding the wrist extension and abduction. Then the increase of the intensity of ENS to PT from MT to MC resulted in a motion of pronation to the maximum pronation while holding the extension and abduction (Fig. 6C). 4. Discussion  Observations of activities of two muscles during repetitive movements must reveal activation of facilitation or inhibition between the muscles. The facilitation must be active during co-contraction of the muscles and the inhibition must be during reciprocal or alternating contraction between the muscles. Among PT, ECR, and FCR, inhibition between ECR and FCR [2], [3], [9], and facilitation between PT and ECR [25, Nakano et al., unpublished results] have been studied. In the present EMG study, during the series of the dynamic motion of flexion/extension ECR (ECRL and ECRB) and FCR showed increments of activities at the extension and flexion phases, respectively, regardless of the positions of the forearm in all the subjects. Therefore alternating contraction between the muscles occurred during the motion. The inhibition between the muscles must be active during the alternating contraction. In the present EMG study, in the prone, semiprone, and supine positions of the forearm, PT and ECR showed parallel activities during the static extension in all, eight, and eight subjects, respectively, and at the extension phase during the dynamic motion in all, eight and five subjects, respectively. Therefore co-contraction of the muscles occurred during wrist extension movements at least with the prone forearm. The facilitation between the muscles must be active during the co-contraction. In the present EMG study, during the series of the dynamic motion parallel activities of PT and FCR were seen at the flexion phase in the semiprone and supine positions in four and five subjects, respectively. This observation of co-contraction seems to indicate existence of facilitation between PT and FCR. Therefore it seems likely that the facilitation between PT and ECR is activated with pronating the forearm and that between PT and FCR is with supinating the forearm. Textbooks of the anatomy describe that PT acts as a forearm pronator and ECR as a wrist extensor and abductor [4], [29]. In the present ENS study, ENS to PT induced a motion of forearm pronation to the maximum pronation in all the 11 subjects. This result agrees with the action of PT. In the present study, ENS to ECRL induced motions of wrist extension to the maximum extension and abduction to 5–20 degrees of abduction regardless of the positions of the forearm in all the 12 subjects. This result also agrees with the actions of ECRL. Usually wrist abduction is achieved by co-contraction of ECRL, ECRB, and FCR [4], [5], [29]. Furthermore, during supination movements the weight of the hand works to adduct the wrist. Probably the force in abduction direction produced by ECRL contraction is not enough to abduct the wrist to the maximum abduction. In the present study, ENS to ECRL induced a motion of 30–80 degrees supination from the prone position in all the 12 subjects. There seem to be no publications describing such action of ECRL in healthy human subjects. Since the distal tendon of ECRL tunnels together with that of ECRB through the second compartment of the extensor retinaculum [4], [29], contraction of the muscle must pull the distal end of the radius via the retinaculum in supination direction. Therefore forearm supination from the prone position should be added to one of the actions of ECRL. In the present ENS study, combined ENS to PT and ECRL could produce motions of wrist extension and abduction while holding the maximum pronation of the forearm in all the 11 subjects. Then a decrease of the stimulus intensity of ENS to PT resulted in forearm supination while maintaining the extension and abduction. This finding suggests that contraction of PT during wrist extension movements prevents supinating the forearm. The present EMG study actually showed co-contraction of PT and ECR during the movements. 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[28]. [28]Sato T, Fujii H, Naito A, Tonosaki A, Kobayashi S, Shinozaki K, et al. Inhibition of muscle afferents from the brachioradialis to triceps brachii motoneurones in humans: central pathway. Acta Anat Nippon. 2002;77:H511. [29]. [29]Williams PL, Bannister LH, Berry MM, Collins P, Dyson M, Dussek JE, et al. Gray’s anatomy. 38th ed.. New York, Edinburgh, London, Tokyo, Madrid, Melbourne: Churchill Livingstone; 1995;. [30]. [30]Yoshida Y. Anatomical studies on the extensor carpi radialis longus and brevis muscles in Japanese. Okajima’s Folia Anat Jpn. 1994;71:123–136.  Hiromi Fujii was born in 1961 in Nishigo-Village, Nishishirakawa-Gun, Japan. He received the O.T. degree from School of Allied Medical Sciences, Hirosaki University, Hirosaki, Japan, in 1983 and the Ph.D. degree from Yamagata University, Yamagata, Japan, in 2005. Currently, he is a Professor of the Department of Occupational Therapy, Yamagata Prefectural University of Health Sciences. His research interests are in the area of human motor control.  Shinji Kobayashi was born in 1960 in Shimobe-town, Nishiyatsushiro-Gun, Japan. He graduated from Yamagata University School of Medicine in 1987 and received his Ph.D. degree from Yamagata University, Yamagata, Japan, in 2003. Currently, he is an Assistant Professor of the Department of Orthopedics, Yamagata University School of Medicine. His research interests are in neural connections of the human upper limb and biomechanics of the human hip joint.  Toshiaki Sato was born in 1967 in Kutchan-twon, Abuta-Gun, Japan. He received the O.T. degree from School of Allied Medical Sciences, Hirosaki University, Hirosaki, Japan, in 1989 and the Ph.D. degree from Yamagata University, Yamagata, Japan, in 2005. Currently, he is an Assistant Professor of the Department of Occupational Therapy, Yamagata Prefectural University of Health Sciences. His research interests are in the area of human motor control.  Katsuhiro Shinozaki was born in 1964 in Moka, Japan. He graduated from Yamagata University School of Medicine in 1992 and received his Ph.D. degree from Yamagata University, Yamagata, Japan, in 2003. Currently, he is a Head of the Division of Anesthesiology, Yamagata Prefectural-Nihonkai-Hospital, Sakata, Japan. His research interests are in neural connections of the human upper limb.  Akira Naito was born in 1957 in Kofu, Japan. He received the M.D. degree from Yamagata University School of Medicine, Yamagata, Japan, in 1982 and the Ph.D. degree from Shinshu University, Matsumoto, Japan, in 1986. Currently, he is a Professor of the Department of Anatomy and Structural Science, Course of Biological Structure and Cognitive Integration Science, Yamagata University School of Medicine. His research interests are in the area of human motor control. a Department of Anatomy, Yamagata University School of Medicine, 2-2-2 Iida-Nishi, Yamagata 990-9585, Japan b Department of Rehabilitation Medicine, Yamagata University School of Medicine, 2-2-2 Iida-Nishi, Yamagata 990-9585, Japan c Yamagata-Prefectural-Nihonkai Hospital, Sakata, Japan Corresponding author. Fax: +81 23 628 5205.
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