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Crossed and uncrossed central effects of muscle spindle afferents from the lateral pterygoid muscle of the guinea pig
Brain Research, 302 (1984) 339-345 Elsevier
339
BRE 10069
Crossed and Uncrossed Central Effects of Muscle Spindle Afferents from the Lateral Pterygoid Muscle of the Guinea Pig SHUICHI NOZAKI*, SCOTT H. CHANDLER and LOUIS J. GOLDBERG
Departmentof Oral Biology, School of Dentistry, Departmentof Kinesiology and the Brain ResearchInstitute, Departmentof Anatomy, School of Medicine, University of California, Los Angeles, CA 90024 (U.S.A.) (Accepted November 1st, 1983)
Key words: Muscle spindle - - lateral pterygoid muscle - - zygomaticomandibularismuscle - - lateral jaw movement - trigeminal mesencephalic nucleus - - guinea pig
Physiological evidence is presented for the presence of stretch reflexes in the lateral pterygoid (Pt) muscle of the guinea pig. The central reflex effects of excitation of Pt stretch reflex afferents were also investigated. Passive lateral jaw displacement, which resulted in stretch of the Pt muscle on the side of jaw movement and stretch of the zygomatico-mandibularis(Z) muscle on the side contralateral to the movement, evoked increased EMG activity in these muscles. Stimulation of the trigeminal mesencephalic nucleus (mes V) evoked monosynaptic reflexes in both the Pt and Z nerves. Tonic stretch of the Pt muscle facilitated the monosynaptic reflex in the Pt nerve evoked by stimulation of mes V. Tonic vibration of the Pt muscle facilitated the mes V evoked monosynaptic reflex in the nerves to the ipsilateral Pt and contralateral Z muscles. Conversely, tonic vibration of the Z muscle facilitated the monosynaptic reflex evolved by mes V stimulation in the contralateral Pt and ipsilateral Z nerve. The results support the view that muscle spindles exist in the Pt and Z muscles and that there is a monosynaptic stretch reflex for both the Pt and Z muscles with cell bodies located in the mes V nucleus. It was also shown that the ipsilateral Pt muscle and the contralateral Z muscle act as synergists in the production of lateral jaw movements and that the organization of the stretch reflexes originating from the Pt and Z muscles support their synergistic action. INTRODUCTION Lateral jaw m o v e m e n t s are a p r o m i n e n t component of the masticatory chewing cycle of herbivores such as rabbits and guinea pigs, and is essential for bringing the teeth into the grinding position during mastication. L u n d et al. 20, r e p o r t e d a lateral jaw m o v e m e n t reflex in rabbits: pressing the central upper incisor in the labio-lingual direction elicits a lateral jaw m o v e m e n t t o w a r d the side opposite to that of the tooth being stimulated. T h e p r i m a r y muscles involved in this reflex were d e m o n s t r a t e d to be the ipsilateral lateral pterygoid muscle and the contralateral zygomatico-mandibularis and anterior t e m p o r a l muscles. Thus, in the rabbit, the ipsilateral lateral pterygoid (Pt) muscle and the contralateral zygomatico-mandibularis (Z) muscle are synergists in the production of lateral jaw m o v e m e n t .
In rabbits, the Pt muscle originates from the surface of the lateral p t e r y g o i d plate and inserts just below the condyle of the mandible. T h e Z muscle originates from the posterior medial surface of the zygomatic arch and inserts on the anterior and lateral surface of the ramus 6. Similar anatomical features are seen for the Pt and Z muscles of the guinea pig. Thus, it is strongly suggested that these muscles play a major role in the production of lateral jaw m o v e m e n t s in the guinea pig. The total range of activity of the Pt muscle in the production of m a n d i b u l a r m o v e m e n t s is complex and varies to some extent in different species 3A3,14,22-26. There is some discrepancy concerning anatomical reports of the distribution of muscle spindles in the Pt muscle in various animal species4,5,7-9,15,16,28,29. Muscle spindles have been anatomically d e m o n s t r a t e d in the Pt muscle of the guinea pig 31. T h e n u m b e r of spin-
* Present address: Department of Physiology, Faculty of Dentistry, Tokyo Medical and Dental University, Bunkyo-ku, Tokyo 113, Japan. Correspondence: L. J. Goldberg, Section of Oral Biology, School of Dentistry, University of California, Los Angeles, CA 90024 (U.S.A.) 0006-8993/84/$03.00 (~) 1984 Elsevier Science Publishers B.V.
340 dies, however, is rather small and their functional significance has not yet been demonstrated. It is also not known if these muscle spindles are innervated by the peripheral process of the trigeminal mesencephalic neurons as is the case for the jaw closing muscles. In this paper we will present physiological evidence for the existence of a monosynaptic stretch reflex in the Pt muscle in the guinea pig and describe the central effects of these muscle spindle afferents on the production of lateral jaw movement. MATERIALS AND METHODS Ten adult guinea pigs weighing 400-500 g were used in this study. Under ketamine HCI anesthesia (100 mg/kg, i.m.), cannulation of the trachea and the external jugular vein was performed. Anesthesia was maintained by intermittent i.v. injection of supplemental doses (20 mg/kg) of ketamine HCI during the experiment. Exposure of the Z, the Pt muscles and the Z nerve was accomplished by removal of the globe of the eye from the socket. Dissection of the fatty tissue which remained in the orbit revealed the fibers of the Z muscle which could be found on the superior surface of the muscle. The temporal muscle was also exposed; it runs inferiorly down from the temporal bone to insert on the coronoid process of the mandible. The temporal muscle was retracted with the use of a loop of thread and the fibers of the Pt muscle could be observed posterior to the temporal muscle. This dissection permitted the placement of bipolar electrodes, which consisted of a pair of fine wires (0.2 mm in diameter, enamel-coated except for 2-3 mm from the tip) directly into both the Z and Pt muscles. The mandibular movement was monitored with the use of a light sensitive transducer placed 3-4 cm in front of a small tungsten light bulb that was fixed to the inferior surface of the mandible near the mental symphasis2,1°,lL The transducer provided two outputs; one was proportional to the vertical, and the other to the lateral displacement of the jaw. Stimulating electrodes were stereotaxically placed in both the right and left trigeminal mesencephalic nuclei (mes V). Pairs of fine wire electrodes for recording E M G were placed in the right and left Pt muscles. The nerves to the left Z and superficial masseter muscles were dissected, the peripheral ends
cut, and central ends mounted on silver wire electrodes in an oil pool in the left orbit. In 6 animals, the left condyle was severed from the ramus of the mandible along with the insertion of the left Pt muscle for selective stretch of the left Pt muscle. The sensory innervation of the temporomandibular joint was previously removed by section of the auriculotemporal nerve, to exclude the central effects of the joint afferents evoked by movement of the condyle in the fossa. A string was tied around the condyle and the Pt muscle was tonically stretched in the natural direction of its fibers with a weight of 50 g. In two animals, vibratory stimuli (60 Hz sinusoidal vibration of 200/~m in amplitude) of the Pt and Z muscles was delivered. In these animals, the left Pt muscle was prepared as in the case of tonic stretch of the muscle as described above. In addition, the left zygoma was dissected free with the insertion of the Z muscle intact, and the mandible was sectioned at the midline and the right and left halves kept separate. One string was tied around the left condyle, and another around the left zygoma. The string was attached to a vibrator which provided the above mentioned vibratory stimuli. The left Pt and Z muscles were held in the natural direction of their fibers, and were kept on stretch by applying 50 g of tension. RESULTS
Jaw movements induced by direct stimulation of the lateral pterygoid and zygomatico-mandibularis muscles Fig. 1 is a schematic illustration of the anatomy of the jaw of the guinea pig and the muscles of mastication which were studied. The lateral pterygoid muscle is innervated by lateral pterygoid motoneurons (Pt). This muscle originates on the pterygoid process of the sphenoid bone (p) and inserts on the neck, articular capsule, and disc of the condyle of the mandible (c). The zygomatico-mandibularis muscle is innervated by zygomatico-mandibularis motoneurons (Z) and originates from the lateral surface of the body of the mandible (m) and inserts on the inner surface of the zygoma (z). In the oscilloscopic tracings at the bottom of Fig. 1, the results of electrical stimulation through wire electrodes placed directly into the right Z and left Pt muscles on the position of the man-
341 Passive Jaw Movement Lateral J a w ~ Movement - - r [
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...................... --~ . . . . . . . . . . . . / . . . . . . . . . .
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Fig. 2. EMG activity of the ipsi- and contralateral Pt and Z muscles evoked by passive lateral displacement of the jaw. Top trace: lateral jaw movement; upward deflection of the trace indicates left lateral movement and downward deflection, right lateral movement. The dotted line indicates the control midline position of the mandible. RZ, LZ, EMG of right and left Z muscles; RPt, LPt, EMG of right and left Pt muscles. Time base applies to all records. LZ calibration bar applies to all EMG records.
0.4 mm Fig. 1, Schematic illustration of the origin and insertion of the lateral pterygoid (Pt) and zygomaticomandibularis (Z) muscles. Pt, lateral pterygoid motoneuron; Z, zygomaticomandibularis motoneuron; Me, trigeminal mesencephalic cell body; p, pterygoid fossa; c, condyle of the mandible; z, zygoma; m, mandible. The bottom oscilloscope traces illustrate the mandibular movements induced by stimulation (50 Hz, 0.3 ms in duration, 5.0 V, 10 pulses) of either the right Z muscle (upper trace, denoted as RZ) or the left Pt muscle (lower trace, denoted as LPt). Dotted line indicates the midline of the mandible; L and R show the direction of jaw movement to the left and right sides, respectively. The calibration bar at the bottom applies to the jaw movement records. Each oscilloscopic record is the result of the superimposition of traces made by 10 separate stimulation trials. The vertical output of the transducer was placed in the vertical input of the oscilloscope and the horizontal output was placed in the Z input.
dible in the frontal plane is shown. These muscles act as synergists for lateral jaw m o v e m e n t s since it can be seen that contraction of the right Z muscle elevates and moves the jaw to the ipsilateral (right) side, whereas contraction of the left Pt muscle both opens and moves the jaw to the contralateral (right) side.
Responses of the lateral pterygoid and zygomaticomandibularis muscles to passive horizontal jaw movement It can be seen in Fig. 2 that passive displacement of
the m a n d i b l e (top trace) to the left side induces E M G activity in the right Z and left Pt muscles and, conversely, passive displacement of the m a n d i b l e to the right side activates the right Pt and left Z muscles. Displacement of the jaw to the left stretches the right Z and the left Pt muscle (Fig. 1). Notice that the muscles which are stretched are the ones that show increased E M G activity. The o t h e r pair of muscles (left Z and right Pt) are stretched when the jaw is m o v e d to the right. F u r t h e r m o r e , it was o b s e r v e d that selective stretch of the Pt and Z muscles by pulling the isolated insertions increased the excitability of the stretch reflex of the respective muscles (Fig. 4). Stretch of these muscles was accomplished after section of the auriculotemporal nerve to exclude the central effects of t e m p o r o m a n d i b u l a r joint afferents activated by m o v e m e n t of the condyle. Thus, the results indicate the presence of stretch receptors in the Pt and Z muscles. These results d e m o n s t r a t e that passive displacement of the m a n d i b l e in the lateral direction evokes E M G activity in the contralateral Z and ipsilateral Pt muscles which then act synergistically to resist the displacement. This can be thought of as a lateral stretch reflex of the jaw.
Potentials evoked in the lateral pterygoid nerve and muscle by stimulation of the trigeminal mesencephalic nucleus It has been well established both anatomically and physiologically in various animal species that p r i m a r y afferents from the muscle spindles in the jaw closing muscles are the p e r i p h e r a l processes of neurons with
342 A R Pt -~
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Fig. 3. Potentials evoked by simultaneous stimulation of the left and right mes V as recorded from the nerves supplying the left zygomatico-mandibularis (LZ) and left masseter (LM) muscles and from fine wire electrodes placed in the right and left lateral pterygoid muscles (RPt and LPt) prior to and during muscle paralysis• Traces in columns A and B were obtained before and after paralysis of the animal, respectively• Traces in A 1 and B 1 are the averaged responses to single shocks applied to mes V bilaterally (1 Hz, 0.1 ms duration, 6.4 V). In A 2 and B 2 two shocks to mes V were delivered at an interval of 2 ms and in A 3 and B 3 3 shocks were delivered. Arrows indicate the location of stimulus application. In A, all traces are the averaged response to 32 trials, and in B to 256 trials. The voltage calibration of 20/~V in B 3 applies to the R P T and L P T traces in B; the voltage calibration of 250/~V in B 3 applies to the L Z and LM nerve recordings in A and B, and to the R P T and L P T E M G recordings in A. Time base in B 3 applies to all records•
their cell bodies in mes V; the central processes of these neurons make monosynaptic excitatory contact with trigeminal motoneurons innervating the jaw closing muscles 11,27,30. Simultaneous stimulation of both left and right mes V with one shock, at a low stimulus intensity, produced no EMG response in the Pt muscles, and only an antidromic response in the spindle afferent fibers as recorded from the left Z and masseter (M) nerves (Fig. 3A1). The antidromic response is the result of direct activation of the peripheral process of the mes V neurons. Stimulation with 2 shocks produced two antidromic volleys in the LZ and M nerves and a small monosynaptic response following the last antidromic volley (Fig. 3A2). An EMG response can also be seen in the RPT and LPT EMG records. When 3 shocks
were given the monosynaptic response was significantly increased in both the nerve and muscle records (Fig. 3A3). The latency of the anti- and orthodromic responses in both the left Z and M nerves are nearly identical. Short pulse train stimulation of the mes V of the guinea pig has been shown to produce summation of monosynaptic EPSPs in jaw closer motoneurons such as those innervating the masseter muscle u. Since the response in the masseter nerve is known to be monosynaptic and originate from the spindle afferent fibers located in the jaw closing muscles it, a similar monosynaptic reflex can postulated to be responsible for the response in the Z nerve. After paralysis of the animal with gallamine triethiodide, the same stimuli were delivered to the right and left mes V with the animal artificially respired (Fig. 3B). Use of the averaging technique demonstrates that in the paralyzed preparation nerve potentials from the Pt and Z muscle nerves can be recorded with fine wire electrodes (Fig. 3B2,3). In Fig. 3B2,3 it can be seen that averaged responses to mes V stimuli resulting from action potentials in afferent and efferent fibers were recorded from the fine wire electrodes placed directly into the right and left Pt muscles. The records from the RPt and LPt muscles show the same antidromic, followed by orthodromic response (Fig. 3B2,3 upper two traces) as seen in the Z and M nerve recordings (Fig. 3B2,3 lower two traces). Note the increased gain in the records obtained from RPT and LPT muscles after paralysis. The similar latencies in all records, and the augmented responses to a train of shocks indicate that both Pt and Z motoneurons are monosynaptically activated by stimulation of mes V. It also supports the view that there are muscle spindles in the Pt muscle and that they are innervated by peripheral processes of mes V neurons, the central processes of which project monosynaptically to the Pt motoneurons.
Effects of stretch and vibratory stimulation of the PT muscle on monosynaptic responses of the PT, Z and M motoneurons. The effects of tonically stretching the left Pt muscle were tested on the monosynaptic responses in the nerves supplying the left and right Pt, left Z and left M muscles in 5 paralyzed animals• Recordings from the Pt muscles were obtained as described for Fig. 3B; and from the Z and M muscle nerves as described for Fig. 3A, B. During stretch,
343 A
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Fig. 4. Effects of stretch of the left Pt muscle on the monosynaptic reflexes of the right Pt (RPt), left Pt (LPt), left Z (LZ), and left M (LM) nerves evoked by 3 shocks applied to mes V bilaterally (1 Hz, 0.1 ms duration, 4.0 V, 500 pps). All traces were obtained in the paralyzed preparation and each record is the averaged response of 256 trials. A, was obtained before, and B, during tonic stretch of the left Pt muscle with a load of 50 g. Calibration of 20/~V and 250/~V apply to upper and lower pairs of traces, respectively. Time base applies to all records.
the averaged monosynaptic response to mes V stimulation in the left Pt nerve (Fig. 4B second trace) was increased above the control level (Fig. 4A, second trace). The antidromic responses in Fig. 4A, B were not changed and only the left Pt record showed a change in the monosynaptic response. The data demA Control
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Fig. 5. Effects of vibratory stimuli applied to the left Pt and left Z muscles on the monosynaptic reflex evoked bilaterally in the Z and Pt muscles by bilateral simultaneous stimulation of mes V (1 Hz, 0.1 ms duration, 500 pps) at arrows shown in A. B and E were obtained during vibration of the left Pt and Z muscles, respectively. A and C, and D and F were recorded before and after application of the vibratory stimuli to LPt and LZ. All records are the averaged responses of 32 trials. Voltage calibration and time base in F apply to all records.
onstrate that stretch of the left Pt muscle results in a facilitation of the homonymous monosynaptic reflex evoked by stimulation of mes V. The effects of vibratory stimuli applied to the Pt and Z muscles is illustrated in Fig. 5. In this case EMG recordings were obtained with fine wire electrodes from the left and right Pt and Z muscles. The test stimuli were 3 shocks at 500 Hz delivered simultaneously to the left and right mes V. The effects of vibration at 60 Hz and 200 mm to the left Pt and Z muscles was observed. It can be seen that vibration of the left Pt muscle increased the monosynaptic reflex both in the left Pt and right Z muscles (Fig. 5B). Conversely, vibration of the left Z muscle increased the monosynaptic reflex in the left Z and in the right Pt muscle (Fig. 5E) when compared to control responses (Fig. 5A, C, D, F). DISCUSSION
The existence of muscle spindles has been demonstrated anatomically in the Pt muscle of the guinea pig 31 but the central projections of these muscle spindle afferents from the Pt muscle has not yet been determined. The present study provides physiological evidence that spindle afferents of the Pt as well as the Z muscle have their cell bodies in mes V with their central processes making homonymous monosynaptic excitatory contact with Pt and Z motoneurons, respectively. This pattern is similar to that of spindle afferents from the jaw closing muscles of the cat 27, and guinea pig n. Tonic stretch and vibratory stimulation of the Pt and Z muscles were used to activate possible muscle spindle stretch receptors located therein. Longitudinal vibration of muscles is most effective in activating primary endings of muscle spindles; secondary endings and tendon organ receptors are much less sensitive to such stimulation, especially in the high frequency range of vibration used in the present experiments 1. Thus, the facilitatory effects of longitudinal vibration of the Pt and Z muscles on the homonymous monosynaptic reflex, and the monosynaptic reflex of the contralateral synergists can be attributed to the activation of muscles spindle primary endings in Pt and Z muscles. A summary of the results of these experiments is shown in graphic form in Fig. 6. Afferents from the
344 sus vertical jaw movements acts independently. Further studies are needed to test this possibility and its implications for the role of these reflexes in jaw
'
"4-
movement control. The results suggest that the synergistic action of the Pt and Z m o t o n e u r o n s in producing lateral jaw movements is influenced to some degree by the stretch reflex system of their muscles. Simultaneous contraction of the left Pt and right Z muscles moves the mandible to the right side and simultaneously passively stretches the right Pt and left Z muscles.
Fig. 6. Schematic summary of the results obtained in this study.
The results presented here indicate that stretch of the right Pt and left Z muscles evokes h o m o n y m o u s excitation of right Pt and left Z m o t o n e u r o n s through a monosynaptic pathway and excitation of the contralateral synergist through an u n k n o w n pathway. This
muscle spindles in Pt muscles have their cell bodies in mes V; the central processes of these neurons make monosynaptic excitatory contact with ipsilateral Pt motoneurons and exert a facilitatory influence
would produce resistance to the right lateral movement and eventually return the jaw to a central position. One might also expect such stimuli to inhibit the antagonist muscles, however, under the conditions of
through an u n k n o w n pathway to contralateral Z mo-
these experiments no such inhibition could be dem-
toneurons. Conversely, Z spindle afferents excite ipsilateral Z m o t o n e u r o n s and contralateral Pt motoneurons. We did not observe either excitatory or in-
onstrated.
hibitory effects on the monosynaptic reflex to the jaw closing M m o t o n e u r o n s during stretch of the Pt muscle. This indicates the possibility that the stretch reflex system involving muscles producing lateral verREFERENCES 1 Brown, M. C., Engberg, I. and Matthews, P. B. C., The relative sensitivity to vibration of muscle receptors of the cat, J. Physiol. (Lond.), 192 (1976) 773-800. 2 Byrd, K. E., Milberg, D. J. and Luschei, E. S., Human and macaque mastication: a quantitative study, J. dent. Res., 57 (1978) 834-843. 3 Carlsoo, S., An electromyographic study of the activity, and an analysis of the mechanics of the lateral pterygoid muscle, Acta anat., 26 (1956) 339-351. 4 Christensen, L. V., Muscle spindles in the lateral pterygoid muscle of miniature swine, Arch. Oral Biol., 12 (1967) 1203-1204. 5 Cooper, S., Muscle spindles and other muscle receptors. In G. H. Bourne (Ed.), The Structure and Function o f Muscle, Vol. 1, New York, Academic Press, 1960, pp. 381-420. 6 Fox, S. S., Lateral jaw movements in mammalian dentitions, J. Prosth. Dent., 15 (1965) 810-825. 7 Franks, A. S. T., Studies on the innervation of the temporomandibular joint and lateral pterygoid muscle in animals, J. dent. Res., 43 (1964) 497-498. 8 Freimann, R., Untersuchungen fiber Zahl und Anordnung der Muskelspindeln in den Kaumuskeln des Menschen, Anat. Ariz., 100 (1954) 258-264.
ACKNOWLEDGEMENTS This research was supported in whole by the National Institute of Dental Research, NIH, Research Grant RO1 D E 4166. 9 Gill, H. L., Neuromuscular spindles in human lateral pterygoid muscles, J. Anat. (Lond.), 109 (1971) 15%167. 10 Goldberg, L. J. and Chandler, S. H., Evidence for pattern generator control of the effects of spindle afferent input during rhythmical jaw movements, Canad. J. Physiol. Pharmacol., 59 (1981) 707-712. 11 Goldberg, L. J. and Tal, M., Intracellular recording in trigeminal motoneurons of the anesthetized guinea pig during rhythmic jaw movements, Exp. Neurol., 58 (1978) 102-111. 12 Goldberg, L. J., Chandler, S. H. and Tal, M., Relationship between jaw movements and trigeminal motoneuron membrane potential fluctuations during cortically induced rhythmical jaw movements in the guinea pig, J. Neurophysiol., 48 (1982) 110-125. 13 Hickey, J. C., Stacy, R. W. and Rinear, L. L., Electromyographic studies of mandibular muscles in basic jaw movements, J. Prosth. Dent., 7 (1957) 565-570. 14 Kamiyama, M., Study on activity of the lateral pterygoid muscles. J. Stomatol. Soc. Japan, 25 (1958) 164-183. 15 Karlsen, K., The location of motor endplates and the distribution and histological structure of muscle spindles in jaw muscles of the rat. Acta Odont. Scand., 23 (1965) 521-547. 16 Karlsen, K., Fibre calibre spectra of nerves to masticatory muscles in the cat, Acta Odont. Scand., 27 (1969) 263-270.
345 17 Kubota, K., Masegi, T. and Osanai, K., Muscle spindle in masticatory muscle and its trigeminal mesencephalic nucleus, Bull. Tokyo Med. Dent. Univ., Suppl, 21 (1974) 3-6. 18 Lehr, R. P., Jr. and Owens, S. E., Jr., An electromyographic study of the human lateral pterygoid muscles. Anat. Rec., 196 (1980) 441448. 19 Lennartsson, B., Number and distribution of muscle spindles in the masticatory muscles of the rat, J. Anat. (Lond.), 130 (1980) 279-288. 20 Lund, J. P., McLachlan, R. S. and Deilow, P. G., A lateral jaw movement reflex, Exp. Neurol., 31 (1971) 189-199. 21 Maier, A., Occurrence and distribution of muscle spindles in masticatory and suprahyoid muscles of the rat, Amer. J. Anat., 155 (1979) 483-505. 22 McNamara, J. A., Jr., The independent functions of the two heads of the lateral pterygoid muscle, Amer. J. Anat., 138 (1973) 197-206. 23 McNamara, J. A., Jr., The electromyography of the mandibular postural position in the rhesus monkey (Macaca mulatta), J. dent. Res., 53 (1974) 949. 24 McNamara, J. A., Jr., An electromyographic study of mastication in the rhesus monkey (Macaca mulatta), Arch. Oral Biol., 19 (1974) 821-823. 25 McNamara, J. A., Jr. and Moyers, R. E., Electromyography of the oral phase of deglutition in the rhesus monkey (Macaca mulatta), Arch. Oral Biol., 18 (1973) 995-1002.
26 Molin, C., An electromyographic study of the function of the lateral pterygoid muscle, Swed. dent. J., 66 (1973) 203-208. 27 Nakamura, Y., Goldberg, L. J. and Clemente, C. D., Nature of suppression of the trigeminal monosynaptic reflex induced by stimulation of the orbital gyrus of the cat, Brain Research, 6 (1967) 184-198. 28 Rakhawy, M. T., Shehata, S. H. and Badawy, Z. H., The proprioceptive innervation of the lateral pterygoid muscle in man and some other muscles, Acta anat., 79 (1971) 581-598. 29 Smith, R. D. and Marcarian, H. Q., The neuromuscular spindles of the lateral pterygoid muscle, Anat. Anz., 120 (1967) 47-53. 30 Szentagothai, J., Anatomical considerations of monosynaptic reflex arcs, J. Neurophysiol., 11 (1948) 445-453. 31 Tsaknakis, A. and Karakasis, D., Neuromuscular spindles in the lateral pterygoid muscle of the guinea pig, Arch. Oral Biol., 17 (1972) 1265-1268. 32 Voss, H., Zahl und Anordnung der Muskelspindeln in den oberen Zungenbeinmuskeln, im M. trapezius und M. latissimus dorsi, Anat. Anz., 103 (1956) 443-446. 33 Woelfel, J. B., Hickey, J. C., Stacy, R. W. and Rinear, L., Electromyographic analysis of jaw movement, J. Prosth. Dent., 10 (1960) 688-697.
339
BRE 10069
Crossed and Uncrossed Central Effects of Muscle Spindle Afferents from the Lateral Pterygoid Muscle of the Guinea Pig SHUICHI NOZAKI*, SCOTT H. CHANDLER and LOUIS J. GOLDBERG
Departmentof Oral Biology, School of Dentistry, Departmentof Kinesiology and the Brain ResearchInstitute, Departmentof Anatomy, School of Medicine, University of California, Los Angeles, CA 90024 (U.S.A.) (Accepted November 1st, 1983)
Key words: Muscle spindle - - lateral pterygoid muscle - - zygomaticomandibularismuscle - - lateral jaw movement - trigeminal mesencephalic nucleus - - guinea pig
Physiological evidence is presented for the presence of stretch reflexes in the lateral pterygoid (Pt) muscle of the guinea pig. The central reflex effects of excitation of Pt stretch reflex afferents were also investigated. Passive lateral jaw displacement, which resulted in stretch of the Pt muscle on the side of jaw movement and stretch of the zygomatico-mandibularis(Z) muscle on the side contralateral to the movement, evoked increased EMG activity in these muscles. Stimulation of the trigeminal mesencephalic nucleus (mes V) evoked monosynaptic reflexes in both the Pt and Z nerves. Tonic stretch of the Pt muscle facilitated the monosynaptic reflex in the Pt nerve evoked by stimulation of mes V. Tonic vibration of the Pt muscle facilitated the mes V evoked monosynaptic reflex in the nerves to the ipsilateral Pt and contralateral Z muscles. Conversely, tonic vibration of the Z muscle facilitated the monosynaptic reflex evolved by mes V stimulation in the contralateral Pt and ipsilateral Z nerve. The results support the view that muscle spindles exist in the Pt and Z muscles and that there is a monosynaptic stretch reflex for both the Pt and Z muscles with cell bodies located in the mes V nucleus. It was also shown that the ipsilateral Pt muscle and the contralateral Z muscle act as synergists in the production of lateral jaw movements and that the organization of the stretch reflexes originating from the Pt and Z muscles support their synergistic action. INTRODUCTION Lateral jaw m o v e m e n t s are a p r o m i n e n t component of the masticatory chewing cycle of herbivores such as rabbits and guinea pigs, and is essential for bringing the teeth into the grinding position during mastication. L u n d et al. 20, r e p o r t e d a lateral jaw m o v e m e n t reflex in rabbits: pressing the central upper incisor in the labio-lingual direction elicits a lateral jaw m o v e m e n t t o w a r d the side opposite to that of the tooth being stimulated. T h e p r i m a r y muscles involved in this reflex were d e m o n s t r a t e d to be the ipsilateral lateral pterygoid muscle and the contralateral zygomatico-mandibularis and anterior t e m p o r a l muscles. Thus, in the rabbit, the ipsilateral lateral pterygoid (Pt) muscle and the contralateral zygomatico-mandibularis (Z) muscle are synergists in the production of lateral jaw m o v e m e n t .
In rabbits, the Pt muscle originates from the surface of the lateral p t e r y g o i d plate and inserts just below the condyle of the mandible. T h e Z muscle originates from the posterior medial surface of the zygomatic arch and inserts on the anterior and lateral surface of the ramus 6. Similar anatomical features are seen for the Pt and Z muscles of the guinea pig. Thus, it is strongly suggested that these muscles play a major role in the production of lateral jaw m o v e m e n t s in the guinea pig. The total range of activity of the Pt muscle in the production of m a n d i b u l a r m o v e m e n t s is complex and varies to some extent in different species 3A3,14,22-26. There is some discrepancy concerning anatomical reports of the distribution of muscle spindles in the Pt muscle in various animal species4,5,7-9,15,16,28,29. Muscle spindles have been anatomically d e m o n s t r a t e d in the Pt muscle of the guinea pig 31. T h e n u m b e r of spin-
* Present address: Department of Physiology, Faculty of Dentistry, Tokyo Medical and Dental University, Bunkyo-ku, Tokyo 113, Japan. Correspondence: L. J. Goldberg, Section of Oral Biology, School of Dentistry, University of California, Los Angeles, CA 90024 (U.S.A.) 0006-8993/84/$03.00 (~) 1984 Elsevier Science Publishers B.V.
340 dies, however, is rather small and their functional significance has not yet been demonstrated. It is also not known if these muscle spindles are innervated by the peripheral process of the trigeminal mesencephalic neurons as is the case for the jaw closing muscles. In this paper we will present physiological evidence for the existence of a monosynaptic stretch reflex in the Pt muscle in the guinea pig and describe the central effects of these muscle spindle afferents on the production of lateral jaw movement. MATERIALS AND METHODS Ten adult guinea pigs weighing 400-500 g were used in this study. Under ketamine HCI anesthesia (100 mg/kg, i.m.), cannulation of the trachea and the external jugular vein was performed. Anesthesia was maintained by intermittent i.v. injection of supplemental doses (20 mg/kg) of ketamine HCI during the experiment. Exposure of the Z, the Pt muscles and the Z nerve was accomplished by removal of the globe of the eye from the socket. Dissection of the fatty tissue which remained in the orbit revealed the fibers of the Z muscle which could be found on the superior surface of the muscle. The temporal muscle was also exposed; it runs inferiorly down from the temporal bone to insert on the coronoid process of the mandible. The temporal muscle was retracted with the use of a loop of thread and the fibers of the Pt muscle could be observed posterior to the temporal muscle. This dissection permitted the placement of bipolar electrodes, which consisted of a pair of fine wires (0.2 mm in diameter, enamel-coated except for 2-3 mm from the tip) directly into both the Z and Pt muscles. The mandibular movement was monitored with the use of a light sensitive transducer placed 3-4 cm in front of a small tungsten light bulb that was fixed to the inferior surface of the mandible near the mental symphasis2,1°,lL The transducer provided two outputs; one was proportional to the vertical, and the other to the lateral displacement of the jaw. Stimulating electrodes were stereotaxically placed in both the right and left trigeminal mesencephalic nuclei (mes V). Pairs of fine wire electrodes for recording E M G were placed in the right and left Pt muscles. The nerves to the left Z and superficial masseter muscles were dissected, the peripheral ends
cut, and central ends mounted on silver wire electrodes in an oil pool in the left orbit. In 6 animals, the left condyle was severed from the ramus of the mandible along with the insertion of the left Pt muscle for selective stretch of the left Pt muscle. The sensory innervation of the temporomandibular joint was previously removed by section of the auriculotemporal nerve, to exclude the central effects of the joint afferents evoked by movement of the condyle in the fossa. A string was tied around the condyle and the Pt muscle was tonically stretched in the natural direction of its fibers with a weight of 50 g. In two animals, vibratory stimuli (60 Hz sinusoidal vibration of 200/~m in amplitude) of the Pt and Z muscles was delivered. In these animals, the left Pt muscle was prepared as in the case of tonic stretch of the muscle as described above. In addition, the left zygoma was dissected free with the insertion of the Z muscle intact, and the mandible was sectioned at the midline and the right and left halves kept separate. One string was tied around the left condyle, and another around the left zygoma. The string was attached to a vibrator which provided the above mentioned vibratory stimuli. The left Pt and Z muscles were held in the natural direction of their fibers, and were kept on stretch by applying 50 g of tension. RESULTS
Jaw movements induced by direct stimulation of the lateral pterygoid and zygomatico-mandibularis muscles Fig. 1 is a schematic illustration of the anatomy of the jaw of the guinea pig and the muscles of mastication which were studied. The lateral pterygoid muscle is innervated by lateral pterygoid motoneurons (Pt). This muscle originates on the pterygoid process of the sphenoid bone (p) and inserts on the neck, articular capsule, and disc of the condyle of the mandible (c). The zygomatico-mandibularis muscle is innervated by zygomatico-mandibularis motoneurons (Z) and originates from the lateral surface of the body of the mandible (m) and inserts on the inner surface of the zygoma (z). In the oscilloscopic tracings at the bottom of Fig. 1, the results of electrical stimulation through wire electrodes placed directly into the right Z and left Pt muscles on the position of the man-
341 Passive Jaw Movement Lateral J a w ~ Movement - - r [
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Fig. 2. EMG activity of the ipsi- and contralateral Pt and Z muscles evoked by passive lateral displacement of the jaw. Top trace: lateral jaw movement; upward deflection of the trace indicates left lateral movement and downward deflection, right lateral movement. The dotted line indicates the control midline position of the mandible. RZ, LZ, EMG of right and left Z muscles; RPt, LPt, EMG of right and left Pt muscles. Time base applies to all records. LZ calibration bar applies to all EMG records.
0.4 mm Fig. 1, Schematic illustration of the origin and insertion of the lateral pterygoid (Pt) and zygomaticomandibularis (Z) muscles. Pt, lateral pterygoid motoneuron; Z, zygomaticomandibularis motoneuron; Me, trigeminal mesencephalic cell body; p, pterygoid fossa; c, condyle of the mandible; z, zygoma; m, mandible. The bottom oscilloscope traces illustrate the mandibular movements induced by stimulation (50 Hz, 0.3 ms in duration, 5.0 V, 10 pulses) of either the right Z muscle (upper trace, denoted as RZ) or the left Pt muscle (lower trace, denoted as LPt). Dotted line indicates the midline of the mandible; L and R show the direction of jaw movement to the left and right sides, respectively. The calibration bar at the bottom applies to the jaw movement records. Each oscilloscopic record is the result of the superimposition of traces made by 10 separate stimulation trials. The vertical output of the transducer was placed in the vertical input of the oscilloscope and the horizontal output was placed in the Z input.
dible in the frontal plane is shown. These muscles act as synergists for lateral jaw m o v e m e n t s since it can be seen that contraction of the right Z muscle elevates and moves the jaw to the ipsilateral (right) side, whereas contraction of the left Pt muscle both opens and moves the jaw to the contralateral (right) side.
Responses of the lateral pterygoid and zygomaticomandibularis muscles to passive horizontal jaw movement It can be seen in Fig. 2 that passive displacement of
the m a n d i b l e (top trace) to the left side induces E M G activity in the right Z and left Pt muscles and, conversely, passive displacement of the m a n d i b l e to the right side activates the right Pt and left Z muscles. Displacement of the jaw to the left stretches the right Z and the left Pt muscle (Fig. 1). Notice that the muscles which are stretched are the ones that show increased E M G activity. The o t h e r pair of muscles (left Z and right Pt) are stretched when the jaw is m o v e d to the right. F u r t h e r m o r e , it was o b s e r v e d that selective stretch of the Pt and Z muscles by pulling the isolated insertions increased the excitability of the stretch reflex of the respective muscles (Fig. 4). Stretch of these muscles was accomplished after section of the auriculotemporal nerve to exclude the central effects of t e m p o r o m a n d i b u l a r joint afferents activated by m o v e m e n t of the condyle. Thus, the results indicate the presence of stretch receptors in the Pt and Z muscles. These results d e m o n s t r a t e that passive displacement of the m a n d i b l e in the lateral direction evokes E M G activity in the contralateral Z and ipsilateral Pt muscles which then act synergistically to resist the displacement. This can be thought of as a lateral stretch reflex of the jaw.
Potentials evoked in the lateral pterygoid nerve and muscle by stimulation of the trigeminal mesencephalic nucleus It has been well established both anatomically and physiologically in various animal species that p r i m a r y afferents from the muscle spindles in the jaw closing muscles are the p e r i p h e r a l processes of neurons with
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Fig. 3. Potentials evoked by simultaneous stimulation of the left and right mes V as recorded from the nerves supplying the left zygomatico-mandibularis (LZ) and left masseter (LM) muscles and from fine wire electrodes placed in the right and left lateral pterygoid muscles (RPt and LPt) prior to and during muscle paralysis• Traces in columns A and B were obtained before and after paralysis of the animal, respectively• Traces in A 1 and B 1 are the averaged responses to single shocks applied to mes V bilaterally (1 Hz, 0.1 ms duration, 6.4 V). In A 2 and B 2 two shocks to mes V were delivered at an interval of 2 ms and in A 3 and B 3 3 shocks were delivered. Arrows indicate the location of stimulus application. In A, all traces are the averaged response to 32 trials, and in B to 256 trials. The voltage calibration of 20/~V in B 3 applies to the R P T and L P T traces in B; the voltage calibration of 250/~V in B 3 applies to the L Z and LM nerve recordings in A and B, and to the R P T and L P T E M G recordings in A. Time base in B 3 applies to all records•
their cell bodies in mes V; the central processes of these neurons make monosynaptic excitatory contact with trigeminal motoneurons innervating the jaw closing muscles 11,27,30. Simultaneous stimulation of both left and right mes V with one shock, at a low stimulus intensity, produced no EMG response in the Pt muscles, and only an antidromic response in the spindle afferent fibers as recorded from the left Z and masseter (M) nerves (Fig. 3A1). The antidromic response is the result of direct activation of the peripheral process of the mes V neurons. Stimulation with 2 shocks produced two antidromic volleys in the LZ and M nerves and a small monosynaptic response following the last antidromic volley (Fig. 3A2). An EMG response can also be seen in the RPT and LPT EMG records. When 3 shocks
were given the monosynaptic response was significantly increased in both the nerve and muscle records (Fig. 3A3). The latency of the anti- and orthodromic responses in both the left Z and M nerves are nearly identical. Short pulse train stimulation of the mes V of the guinea pig has been shown to produce summation of monosynaptic EPSPs in jaw closer motoneurons such as those innervating the masseter muscle u. Since the response in the masseter nerve is known to be monosynaptic and originate from the spindle afferent fibers located in the jaw closing muscles it, a similar monosynaptic reflex can postulated to be responsible for the response in the Z nerve. After paralysis of the animal with gallamine triethiodide, the same stimuli were delivered to the right and left mes V with the animal artificially respired (Fig. 3B). Use of the averaging technique demonstrates that in the paralyzed preparation nerve potentials from the Pt and Z muscle nerves can be recorded with fine wire electrodes (Fig. 3B2,3). In Fig. 3B2,3 it can be seen that averaged responses to mes V stimuli resulting from action potentials in afferent and efferent fibers were recorded from the fine wire electrodes placed directly into the right and left Pt muscles. The records from the RPt and LPt muscles show the same antidromic, followed by orthodromic response (Fig. 3B2,3 upper two traces) as seen in the Z and M nerve recordings (Fig. 3B2,3 lower two traces). Note the increased gain in the records obtained from RPT and LPT muscles after paralysis. The similar latencies in all records, and the augmented responses to a train of shocks indicate that both Pt and Z motoneurons are monosynaptically activated by stimulation of mes V. It also supports the view that there are muscle spindles in the Pt muscle and that they are innervated by peripheral processes of mes V neurons, the central processes of which project monosynaptically to the Pt motoneurons.
Effects of stretch and vibratory stimulation of the PT muscle on monosynaptic responses of the PT, Z and M motoneurons. The effects of tonically stretching the left Pt muscle were tested on the monosynaptic responses in the nerves supplying the left and right Pt, left Z and left M muscles in 5 paralyzed animals• Recordings from the Pt muscles were obtained as described for Fig. 3B; and from the Z and M muscle nerves as described for Fig. 3A, B. During stretch,
343 A
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Fig. 4. Effects of stretch of the left Pt muscle on the monosynaptic reflexes of the right Pt (RPt), left Pt (LPt), left Z (LZ), and left M (LM) nerves evoked by 3 shocks applied to mes V bilaterally (1 Hz, 0.1 ms duration, 4.0 V, 500 pps). All traces were obtained in the paralyzed preparation and each record is the averaged response of 256 trials. A, was obtained before, and B, during tonic stretch of the left Pt muscle with a load of 50 g. Calibration of 20/~V and 250/~V apply to upper and lower pairs of traces, respectively. Time base applies to all records.
the averaged monosynaptic response to mes V stimulation in the left Pt nerve (Fig. 4B second trace) was increased above the control level (Fig. 4A, second trace). The antidromic responses in Fig. 4A, B were not changed and only the left Pt record showed a change in the monosynaptic response. The data demA Control
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Fig. 5. Effects of vibratory stimuli applied to the left Pt and left Z muscles on the monosynaptic reflex evoked bilaterally in the Z and Pt muscles by bilateral simultaneous stimulation of mes V (1 Hz, 0.1 ms duration, 500 pps) at arrows shown in A. B and E were obtained during vibration of the left Pt and Z muscles, respectively. A and C, and D and F were recorded before and after application of the vibratory stimuli to LPt and LZ. All records are the averaged responses of 32 trials. Voltage calibration and time base in F apply to all records.
onstrate that stretch of the left Pt muscle results in a facilitation of the homonymous monosynaptic reflex evoked by stimulation of mes V. The effects of vibratory stimuli applied to the Pt and Z muscles is illustrated in Fig. 5. In this case EMG recordings were obtained with fine wire electrodes from the left and right Pt and Z muscles. The test stimuli were 3 shocks at 500 Hz delivered simultaneously to the left and right mes V. The effects of vibration at 60 Hz and 200 mm to the left Pt and Z muscles was observed. It can be seen that vibration of the left Pt muscle increased the monosynaptic reflex both in the left Pt and right Z muscles (Fig. 5B). Conversely, vibration of the left Z muscle increased the monosynaptic reflex in the left Z and in the right Pt muscle (Fig. 5E) when compared to control responses (Fig. 5A, C, D, F). DISCUSSION
The existence of muscle spindles has been demonstrated anatomically in the Pt muscle of the guinea pig 31 but the central projections of these muscle spindle afferents from the Pt muscle has not yet been determined. The present study provides physiological evidence that spindle afferents of the Pt as well as the Z muscle have their cell bodies in mes V with their central processes making homonymous monosynaptic excitatory contact with Pt and Z motoneurons, respectively. This pattern is similar to that of spindle afferents from the jaw closing muscles of the cat 27, and guinea pig n. Tonic stretch and vibratory stimulation of the Pt and Z muscles were used to activate possible muscle spindle stretch receptors located therein. Longitudinal vibration of muscles is most effective in activating primary endings of muscle spindles; secondary endings and tendon organ receptors are much less sensitive to such stimulation, especially in the high frequency range of vibration used in the present experiments 1. Thus, the facilitatory effects of longitudinal vibration of the Pt and Z muscles on the homonymous monosynaptic reflex, and the monosynaptic reflex of the contralateral synergists can be attributed to the activation of muscles spindle primary endings in Pt and Z muscles. A summary of the results of these experiments is shown in graphic form in Fig. 6. Afferents from the
344 sus vertical jaw movements acts independently. Further studies are needed to test this possibility and its implications for the role of these reflexes in jaw
'
"4-
movement control. The results suggest that the synergistic action of the Pt and Z m o t o n e u r o n s in producing lateral jaw movements is influenced to some degree by the stretch reflex system of their muscles. Simultaneous contraction of the left Pt and right Z muscles moves the mandible to the right side and simultaneously passively stretches the right Pt and left Z muscles.
Fig. 6. Schematic summary of the results obtained in this study.
The results presented here indicate that stretch of the right Pt and left Z muscles evokes h o m o n y m o u s excitation of right Pt and left Z m o t o n e u r o n s through a monosynaptic pathway and excitation of the contralateral synergist through an u n k n o w n pathway. This
muscle spindles in Pt muscles have their cell bodies in mes V; the central processes of these neurons make monosynaptic excitatory contact with ipsilateral Pt motoneurons and exert a facilitatory influence
would produce resistance to the right lateral movement and eventually return the jaw to a central position. One might also expect such stimuli to inhibit the antagonist muscles, however, under the conditions of
through an u n k n o w n pathway to contralateral Z mo-
these experiments no such inhibition could be dem-
toneurons. Conversely, Z spindle afferents excite ipsilateral Z m o t o n e u r o n s and contralateral Pt motoneurons. We did not observe either excitatory or in-
onstrated.
hibitory effects on the monosynaptic reflex to the jaw closing M m o t o n e u r o n s during stretch of the Pt muscle. This indicates the possibility that the stretch reflex system involving muscles producing lateral verREFERENCES 1 Brown, M. C., Engberg, I. and Matthews, P. B. C., The relative sensitivity to vibration of muscle receptors of the cat, J. Physiol. (Lond.), 192 (1976) 773-800. 2 Byrd, K. E., Milberg, D. J. and Luschei, E. S., Human and macaque mastication: a quantitative study, J. dent. Res., 57 (1978) 834-843. 3 Carlsoo, S., An electromyographic study of the activity, and an analysis of the mechanics of the lateral pterygoid muscle, Acta anat., 26 (1956) 339-351. 4 Christensen, L. V., Muscle spindles in the lateral pterygoid muscle of miniature swine, Arch. Oral Biol., 12 (1967) 1203-1204. 5 Cooper, S., Muscle spindles and other muscle receptors. In G. H. Bourne (Ed.), The Structure and Function o f Muscle, Vol. 1, New York, Academic Press, 1960, pp. 381-420. 6 Fox, S. S., Lateral jaw movements in mammalian dentitions, J. Prosth. Dent., 15 (1965) 810-825. 7 Franks, A. S. T., Studies on the innervation of the temporomandibular joint and lateral pterygoid muscle in animals, J. dent. Res., 43 (1964) 497-498. 8 Freimann, R., Untersuchungen fiber Zahl und Anordnung der Muskelspindeln in den Kaumuskeln des Menschen, Anat. Ariz., 100 (1954) 258-264.
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