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A tonic vibration reflex evoked in the jaw opening muscles in man
Arctx
oral &I.
Vol. 22. pp
175 to 180 Pergaman
Press 1977. Printed
m Great Britain
A TONIC VIBRATION THE JAW OPENING
REFLEX EVOKED IN MUSCLES IN MAN
G. HELLSINC Department of Stomatognathic Physiology and EMG-laboratory, Faculty of Odontology, University of Giitegorg, Sweden, Department of Clinical Neurophysiology,
University of Uppsala,
Sweden
Summary--Motor effects induced by vibration of the mouth opening muscles were studied in eight subjects. All exhibited a tonic motor response with many characteristics in common with the tonic vibration reflex @VR) as previously studied in limb muscles and jaw elevators: an involuntary contraction appeared in the jaw openers with gradual onset and gradual decline. The contraction was accompanied by a reciprocal inhibition of the voluntarily activated jaw elevators; it was susceptible to voluntary control-when allowed visual feed-back from a torquemeter all subjects were able to suppress the TVR and keep contraction force in their jaw elevators constant. The results suggest that the jaw openers are supplied with proprioceptors functionally similar to spindle endings in that on sustained activation they can produce tonic autogenic excitation and reciprocal inhibition, i.e. the pattern of the classical tonic stretch reflex. However, the vibration-induced contraction in the jaw openers did not exhibit one of the features typical for the TVR in the jaw elevators. The marked grouping of discharges synchronous with each wave of vibration, seen in gross EMG recordings from jaw elevators, was not seen in any one of the three jaw opening muscles examined, the anterior belly of the digastric, the mylohyoid and one of the infrahyoid muscles. As the vibration-induced synchronization is considered to depend on monosynaptic projections, the results imply that the jaw openers are devoid of such projections and that the TVR is mediated through polysynaptic pa.thways.
IINTRODUCTION
TVR is probably, like the classical tonic stretch reflex (TSR), mediated predominantly by longer polysynaptic paths (Granit et al., 1957; Kanda, 1972; Homma and Kanda, 1973; Matthews, 1975; Hagbarth, Hellsing and Liifstedt, 1976b; Burke and Schiller, 1976). A previous study (Hagbarth et al., 1976b) demonstrated that in man reciprocal inhibition of the suprahyoid muscles occurs when the jaw elevators are vibrated. This finding was not regarded as contradictory to the claims of Kidokoro et al. (1968) that in the cat no short latency reciprocal inhibition of jaw openers occurs in response to electrically induced synchronized volleys in Ia afferents from the jaw elevators. We argued that the absence of short latency oligosynaptic projections to antagonistic motoneurones does not exclude the presence of longer polysynaptic projections, brought into action by sustained inflow in Ia afferents and mediating tonic inhibitory effects. By analogy, we questioned whether tonic vibration reflexes can be elicited in the jaw openers, even though short latency dynamic stretch reflexes are not present in these muscles. The present study was to test this suggestion.
Functional characteristics different from corresponding properties of limb muscles have been attributed to the masticatory muscles. In man few, if any, muscle
spindles have been recognized in the jaw opening muscles (Baum, 1900; Gregor, 1904; Voss, 1956). Attempts to evoke monosynaptic stretch reflexes in the digastric muscle in cat have been unsuccessful (Blom, 1960). It has also been assumed that the jaw elevators are not subject to reciprocal inhibitory effects of proprioc:ptive origin in the jaw openers (Godaux and Desmedt, 1975a). Furthermore, evidence indicates that proprioceptive afferents in muscle nerves of jaw-closing muscles, richly supplied with muscle spindles, do not influence digastric motoneurones (Szentagothai. 1948; Kidokoro et al., 1968). By contrast, it is ,well known that a reciprocal reflex organization exists in limb muscles, i.e. inhibition of antagonists is exerted by excitation of the Ia afferents of the agonists. Sinusoidal vibration of various muscles elicits the so-called tonic vibration reflex, TVR (Hagbarth and Eklund, 1966; de Gail, Lance and Neilson, 1966; for review, Hagbarth, 1973). This phenomenon is generally believed to result from excitation of the primary endings of the muscle spindle, end organs which are very sensitive to vibration both in cat (Bianconi and van der Meulen, 1962; Brown, Engberg and Matthews, 1967) and in man (Hagbarth et al., 1976a). Even though the TVR results from excitation of the same end organs as the tendon jerk reflex, the two reflexes are mediated through different reflex arcs; whereas the dynamic tendon jerk reflex is dependent upon monosynaptic projections, the
MATERIALS AND METHODS
Eight healthy subjects without symptoms of mandibular dysfunction and with well-preserved dentitions were used. They were seated in a comfortable chair during the trials. Jaw muscle torque was recorded during closure using a strain gauge built into a rigid, 10 mm thick mouthpiece placed between the front teeth. 175
G. Hellsing
176
Before the trial, the subjects were trained to keep a constant bite force by watching the strain gauge meter to determine the effort required to keep the pointer at 55N (about 5.4 kg). It was then checked that this constant pressure could be kept without visual feed-back. The subject was instructed to keep this effort constant during the trial whatever vibration-induced changes in torque he might perceive, i.e. he was trained not to compensate for these changes. Electromyographic (EMG) records were made from the masseter, temporalis and in three cases from the infrahyoid muscles with pairs of intracutaneous hooks 10mm apart (Ahlgren, 1967). In all subjects, EMG was recorded from the anterior belly of the digastric muscle with a coaxial needle electrode. The signals were amplified by Disa Type 14A30 and displayed on a Mingograph 800. The torque signals were amplified and displayed together with the electromyograms. The vibrator was an electric motor with an eccentric load. It was manually applied and had a contact area of about 200 mm’. Site of application was below the anterior belly of the digastric muscle, close to the midline, either contra- or ipsilateral to the side where the EMG electrodes were placed. Contralateral application was often necessary to avoid artifacts when the vibrator was applied too close to the electrodes. The vibration amplitude was 0.2mm and the vibration frequency 130Hz. In three subjects, vibration was also applied over other mouth openers, i.e. the mylohyoid and the infrahyoid muscles. To determine whether the motor-unit discharges induced by the vibration were phase-locked to the vibration cycle, the EMG recordings of 5 subjects were displayed on fast oscilloscope sweeps triggered by the
@
of an Entran EGC-240 Accelerometer output attached to the vibrator. The transverse (anterior) cutaneous nerve of the neck of one subject was blocked with 1.8 ml of 2 per cent lignocaine (Xylocaine Astra) with l/8000 Lepinephrine to exclude any reflex influence from cutaneous receptors in the vibrated region. This was done bilaterally as some cutaneous receptors, such as the Pacinian corpuscles, are extremely sensitive to vibration. In another subject, the effects of ipsilateral electrical stimulation of the mandibular alveolar nerve at the mental foramen were studied. This nerve transmits sensory impulses from the lower lip, the chin, the anterior part of the mandibular alveolar process and the lower front teeth. The duration of the stimulating pulses was varied between 0.1-1.0 msec and the stimulation frequency varied between 140 Hz. A Grass S88 stimulator with isolation unit SIUS was used. The stimulating electrodes were insulated needles with 2 mm-long bare tips. RESULTS Motor responses induced by vibrution of the supruhyoid muscles In all subjects, vibration of the contra- or ipsilateral anterior belly of the digastric muscle produced a tonic motor response which had many features in common with the TVR as studied in limb muscles and in the jaw elevators. Thus, there was a progressive augmentation of the EMG activity of the digastric muscle during vibration, an activity which slowly declined after cessation of vibration, This tonic reflex contraction was accompanied by a simultaneous decrease of
]
‘.
m. temporalis
I I+.
Fig. 1. Changes in jaw muscle EMG and bite force induced by vibration of the digastric muscle. Bar at bottom of figure = duration of vibration at 130 Hz. Drop of mouthpiece indicated on the bar. Note gradual onset of the digastric contraction and simultaneous decrease of the masseter muscle EMG activity.
Vibration reflex in jaw opening muscles the EMG activity in the jaw elevators, e.g. the masseter (Fig. 1). On cessation of vibration, the masseter activity slowly recovered to or even exceeded the previbration level. As a consequence of these motor phenomena, the bite force was diminished to such an extent that, after a mean latency of .3.8 s (S.D. 2.0) all subjects dropped the strain gauge. In five subjects, this produced immediate activation of the masseter muscle causing rebound jaw closure. On continued vibration, the masseter EMG-activity was inhibited again. When allowed visual feed-back, all subjects were able to suppress the vibration-induced effects, i.e. to maintain constant pressure. Subjectively, the vibration-induced contraction of the mouth openers was strong. The subjects reported the corresponding effects upon vibration of the masseter muscle to be weaker. Cutaneous anaesthesia of both sides of the neck did not change the vibration-induced motor responses.
a
I
177
5ms
[
100 pv
b Fig. 3. Electrical stimulation of the mandibular alveolar nerve. Upper trace: masseter EMG; lower trace: digastric muscle EMG. Stimulus frequency lOimp/s. a. Subject relaxed. No responses visible in either muscle; b. Sustained voluntary contraction of the digastric muscle. No further activation induced by stimulation. The masseter muscle remains silent.
a
Motor responses induced by vibration of the infrahyoid muscles
b -5mS
loo@!
When the vibrator was applied below the hyoid bone to stimulate the infrahyoid musculature, the subjective experiences, as well as the EMG- and torque changes, were much the same as when the suprahyoid musculature was vibrated. Progressive increase of EMG activity of the infrahyoid muscles as well as reciprocal inhibition of the elevators developed and the subject dropped the strain gauge after a few seconds. Effects of electrical
C
Fig. 2. Electrical stimulation of the mandibular alveolar nerve during sustained voluntary contraction of the masseter muscle. As in Figs. 4 and 5. 25 consecutive sweeps, triggered by the electrical pulses, are superimposed. Stimulus duration 0.1 msec. a. Upper trace: masseter muscle EMG; lower trace: digastric muscle EMG. Impulses delivered at l/s cause inhibition of the masseter muscle EMG-activity with a latency of about 7.5 msec. Duration of silent period about 17 msec. No EMG activity induced in the digasttic muscle; b. Masseter muscle EMG. Stimulation frequency lOimp/s. The silent period is shortened compared with a; c. Masseter muscle EMG. Stimulation frequency 40imp/s. The silent period still present.
stimulation of the alveolar
nerve
Electrical stimulation of the ipsilateral mandibular alveolar nerve applied to one subject with a stimulus just above pain-threshold intensity caused mucosal dysaesthesia and an ache in the ipsilateral anterior teeth of the lower jaw, indicating that the stimulus was adequately applied. The duration of the impulses was varied between O.l-l.Omsec during the trials without any noticeable change in the response. Single pulses delivered while the subject was clenching his teeth resulted in transient inhibition of the masseter muscle, i.e. a silent period, with a latency of about 17 msec (Fig. 2). On increasing stimulation frequency, the duration of the silent period was shortened but remained clearly visible even at a frequency of 40 Hz. No activation of the anterior belly of the digastric muscle could be seen at any frequency (Fig. 2). When the subject was completely relaxed, no activation of either muscle could be seen during stimulation. Stimulation produced no change in the gross EMG pattern when applied during sustained contraction of the digastric muscle (Fig. 3).
178
Lack TVR
G. Hellsing
of motor
synchronization
in the jaw-opening
As shown by Godaux and Desmedt (1975b) and confirmed by Hagbarth et al. (1976b), the TVR of the human jaw elevators is characterized by a marked grouping of the EMG-potentials in synchrony with the vibration waves, a phenomenon attributed to monosynaptic timing of the discharges from the firing motoneurone pool (Desmedt and Godaux, 1975). This timing phenomenon was absent in the vibrationinduced contractions of the jaw openers. Marked grouping of the EMG potentials in the masseter muscle occurred during jaw elevator vibration, both when the masseter contraction was maintained voluntarily and when it was reflexly induced by the vibratory stimulus (Fig. 4). By contrast. vibration of the jaw openers did not cause similar synchronization of the EMG potentials in the digastric, mylohyoid or infrahyoid muscles, whether the contraction in these muscles was maintained voluntarily or the EMG activity had developed as a result of the vibration (Fig. 5).
-
2 ms
[
IOO~V
DISCUSSION
All subjects experienced difficulty in following the instruction to keep constant effort when vibration was applied over the jaw openers. It was hard to concentrate upon the task, especially when they were about to drop the strain gauge, but it was carefully checked that the subjects tried not to compensate for any vibration-induced changes on torque that they might perceive. Fig. 5. Vibration of different contralateral jaw openers. 130 Hz, 0.2 mm. 15 superimposed sweeps triggered by vibration wave; a. Subject relaxed at start of vibration. Upper trace: vibration wave; second trace: masseter EMG; third, forth and fifth traces: EMG recordings from the digastric, the mylohyoid and the infrahyoid muscles, respectively. The vibration-induced EMG-activny in the jaw openers is asynchronous in nature, i.e. the EMG discharges are not phase-locked to the vibration wave; b. Vibration of the same muscles during sustained voluntary contraction of the mouth openers does not cause any grouping of the motor unit discharges or any activation of the masseter muscle.
a -22s
[ 100 /Lv
b Fig. 4. Marked synchronization to vibration wave (upper trace) of the motor unit discharges in the masseter muscle (middle traces) during jaw elevator vibration. Digastric EMG-lower trace. 130Hz, 0.2 mm. 15 superimposed sweeps triggered by vibration wave. a. The subject relaxed at the start of vibration, i.e. the EMG activity induced by the vibratory stimuli; b. The vibration applied during sustained voluntary contraction of the masseter muscle.
The fact that all subjects dropped the strain gauge approximately 4s after the start of vibration cannot be explained merely in terms of reduced contraction force in the jaw elevators. To the initial bite force of 55 N exerted by the subject, there was an additional upward pressure of 10-20 N when the vibrator was applied and the tonic reflex contraction in the jaw opener was powerful enough to overcome this pressure. The results indicate that there are proprioceptors in the jaw opening muscles which are sensitive to vibration and on sustained activation produce the wellknown pattern of the tonic vibration reflex and the classical stretch reflex, i.e. tonic autogenic excitation and reciprocal inhibition. It may be objected that the reflex contractions were not strictly autogenic as they also occurred in the contralateral jaw opening muscles. However, there was probably a mechanical spread of the vibration waves across the midline, suffi-
Vibration reflex in jaw opening cient to activate receptors in the contralateral muscles. The possibility that the reflex response resulted from vibration-induced excitation of skin receptors is excluded by the test during skin anaesthesia. If vibration-sensitive mechanoreceptors around the mandibular teeth or in the mandibular mucosa were responsible for the reflex high-frequency tetanic stimulation of the mandibular alveolar nerve would have been expected to cause a similar tonic jaw opening reflex. The results show that the phasic jaw opening reflex resulting from single shocks at l/s to the alveolar nerve is accompanied, not by contraction in the jaw openers, but by a lransient inhibition of the jaw elevators (Yemm, 1972; Gillings and Klineberg, 197.5; Desmedt and Godaux, 1976) and sustained tetanic stimulation of this nerve did not produce a tonic contraction in the jaw opening muscles similar to that induced by vibration. Furthermore, it seems unlikely that vibration applied as far down as over the infrahyoid muscles could spread to receptors in the mouth, supplied by the alveolar or lingual nerves, but such vibration was efficient in eliciting a tonic contraction in the jaw openers. Another possibility which is difficult to exclude experimentally would be that submandibular vibration causes excitation of receptors in the deep fascia. If that were the case, it would be true for other muscles. The different motor response from the jaw elevators (synchronization) and the lack of motor response from the facial muscle (Eklund and Hagbarth, 1966) would then be hard to explain. It could be argued that afferent impulses from platysma might be responsible for the motor response. As platysma belongs to the facial muscles this is probably not so. What is the nature of the vibration-sensitive proprioceptors in the jaw-openers responsible for the observed tonic reflex? Some reports indicate that tonic vibration reflexes cannot be elicited in the facial muscles, and this has been attributed the lack of spindle end organs in these muscles (Eklund and Hagbarth, 1966). In view of the lack of histological evidence of muscle Ispindles in the jaw openers (Baum, 1900; Gregor, 1904; Voss, 1956), no TVR and no dynamic stretch rellexes would be expected in these muscles. However, it is possible that these muscles contain receptors differing in shape from ordinary spindle endings but with similar functional characteristics, in the sense that they are vibration-sensitive stretch receptors whose sustained activation is capable of producing .a tonic stretch reflex, presumably mediated through polysynaptic paths. Nevertheless, the jaw openers differ from the jaw elevators in that they do not exhibit any short latency, phasic stretch reflexes. That vibration of jaw openers produced a tonic reflex contraction with no evidence of monosynaptically induce’d EMG-synchronization supports the view that the TVR is not critically dependent on monosynaptic projections (Homma and Kanda, 1973; Hagbarth rt a/., 19’76b; Burke and Schiller, 1976). Lamarre and Lund (1975) showed that monosynaptic load compensation is prominent in the jawclosing muscles. During mastication, a load was applied to the mandible, resulting in an increase in the EMG activity of the masseter muscle after a delay comparable to that of the jaw-jerk reflex (mean
179
muscles
7.2 msec). EMG recordings from the digastric muscle when loads were applied in closing direction as well as when this muscle was loaded directly during opening movements demonstrated a long latency (24-34msec) response. This infers the existence of a polysynaptic load compensating reflex in the digastric muscle in agreement with the results of the present study. Horseradish peroxidase (HRP) injected into muscle is taken up by nerve terminals and transported to the bodies of the neurones (Kristensson and Olsson, 1971). After injection of HRP in the anterior belly of the digastric and the mylohyoid in the cat, Alvarado-Mallart et al. (1975) found labelled neurones in the ipsilateral posterior half of the mesencephalic nucleus V. This agrees with the present findings and suggests that jaw opening muscles have afferent projections to the mesencephalic nucleus, a nucleus considered to be proprioceptive. Acknowledgements-1 wish to thank Dr Karl-Erik Hagbarth, the department of Clinical Neurology, Academic Hospital, Uppsala, for generously letting me use the facilities of his department and also for constructive criticism and guidance. I am also indebted to Ing. Lars Llifstedt for technical assistance and Dr David Burke for valuable advice during the preparation of this paper. REFERENCES
Ahlgren J. 1967. An intracutaneous
needle electrode for kinesiologic EMG studies. Acta odont. stand. 25, 15-19. Alvarado-Mallart M. R., Batini C., Buisseret-Delmas C. and Corvisier J. 1975. Trigeminal reoresentations of the masticatory and extraocular propriiceptors as revealed by horseradish peroxidase retrograde transport. Expl. Brain Res. 23, 167-179. Baum J. 1900. BeitrHge zur Kenntnis der Muskelspindeln. Anat. Heffe, 1. Abt. 13, 249-305. Bianconi R. and van der Meulen J. P. 1963. The response to vibration of the end organs of mammalian muscle spindles. J. Neurophysiol. 26, 177-190. Blom S. 1960. Afferent influences on tongur muscle activity. Acta physiol. stand. 49 (Supplement 170), l-97. Brown M. C., Engberg I. and Matthews P. B. C. 1967. The relative sensitivity to vibration of muscle receptors of the cat. J. Physiol. 192, 773-800. Burke D. and Schiller H. 1976. The discharge pattern of single motor units in the tonic vibration reflex of human triceps surae. J. Neural. Neurosurg. Psychiat. 39, 729-741. Desmedt J. E. and Godaux E. 1975. Vibration-induced discharge patterns of single motor units in the masseter muscle in man. J. Physiol. 253, 429-442. Desmedt J. E. and Godaux E. 1976. Habituation of exteroceptive suppression and of exteroceptive reflexes in man as influenced by voluntary contraction. Brain Rex 106, 21-29. Eklund G. and Hagbarth K.-E. 1966. Normal variability of tonic vibration reflexes in man. Expl. Neural. 16, 8&92. de Gail P., Lance J. W. and Neilson P. D. 1966. DitTerential effects on tonic and phasic reflex machanisms produced by vibration of muscles in man. J. Neural. Neurosurg. Psychiat. 29, l-11. Gillings B. R. D. and Klineberg I. J. 1975. Latency and inhibition of human masticatory muscles following stimuli. J. dent. Res. 54, 269-279. Godaux E. and Desmedt J. E. 1975a. Human masseter muscle: H- and tendon reflexes. Their paradoxical potentiation by muscle vibration. Archs Neural., Chicago 32, 229-234.
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G. Hellsing
Godaux E. and Desmedt J. E. 1975b. Evidence for a monosynaptic mechanism in the tonic vibration reflex of the human masseter muscle. J. Neural. Neurosurg. Psychiat. 38, 161-169. Granit R., Phillips C. G., Skoglund S. and Steg G. 1957. Differentiation of tonic from phasic alpha ventral horn cells by stretch, pinna and crossed extensor reflexes. J. Neurophysiol. 29, 47@481. Gregor A. 1904. Ueber die Vertheilung der Muskelspindeln in der Muskulatur des menschlichen FGtus. Arch. Anat. Physiol. Anat. Abt. Jahrg. 1904, 112-196. Hagbarth K.-E. 1973. The effect of muscle vibration in normal man and in patients with motor disorders. In: New Developments in Electromyography and Clinicul NeuroDhvsioloav (Edited bv Desmedt J. E.). Vol. 3. vv. _. 428-443.’ Kar&, ‘Base]. I Hagbarth K.-E., Burke D., Wallin G. and LGfstedt L. 1976a. Single unit spindle responses to muscle vibration in man. In: Undorsranding the Stretch Reflex. Progress in Brain Research (Edited by Homma S.), Elsevier. Amsterdam. Hagbarth K.-E. and Eklund G. 1966. Motor effects of vibratory stimuli in man. In: Muscular Affrrents and Motor Conrrol. Nobel Symposium I (Edited by Granit R.). p. 177. Almqvist & Wiksell, Stockholm. Hagbarth K.-E.. Hellsing G. and Liifstedt L. 197613. The TVR and vibration-induced timing of motor impulses in the human jaw elevators. J. Neural. Neurosurg. Psq‘chiat. 39, 719-728. Hirayama K., Homma S., Mizote M., Nakajima Y. and Watanabe S. 1974. Separation of the contributions of voluntary and vibratory activation of motor units in man by cross-correlograms. Jap. J. Physiol. 24, 293-304. Homma S., Kanda K. and Watanabe S. 1971 Tonic vibration reflex in human and monkey subjects. Jap. J. Physiol. 21. 419430.
Homma S., Kanda K. and Watanabe S. 1972. Preferred spike intervals in the vibration reflex. Jap. J. Physiol. 22, 421432. Hufschmidt H. J. 1958. Wird durch Muskelvibration eine Eigenreflexreihe erzeugt? Pjiigers Arch. ges Physiol. 267, 508-516. Kanda K. 1972. Contributions of polysynaptic pathways to the tonic vibration reflex. Jap. J. Physiol. 221, 367-377. Kidokoro Y., Kubota K., Shuto S. and Sumino R. 1968. Reflex organization of cat masticatory muscles. J. Neurophysiol. 31, 6955708. Kristensson K. and Olsson Y. 1971. Retrograde axonal transport of protein. Brain Res. 29, 363-365. Lamarre Y. and Lund J. P. 1975. Load compensation in human masseter muscles. J. Physiol. 253, 21-35. Matthews P. B. C. 1975. The relative unimportance of the temporal pattern of the primary afferent input in determinating the mean level of motor firing in the tonic vibration reflex. J. Physiol. 251, 333-361. Sherrington C. S. 1917. Reflexes elicitable in the cat from pinna vibrissiae and jaws. J. Physiol. 51, 404431. Sommer J. 1941. Synchronisierung motorischer Impulse und ihre Bedeutung fir die Neurophysiologische Forschung. 2. ges Neural. Psychiat. 172, 501S530. Szentagothai J. 1948. Anatomical considerations of monosynaptic reflex arcs. J. Neurophysiol. 11, 445-454. Voss H. 1956. Zahl und Anordnung der Muskelspindeln in den oberen Zungenbeinmuskeln im M. trapezius und M. latissimus dorse. Anat. Anz. 103, 443446. Yemm R. 1972. Reflex jaw opening following electrical stimulation of oral mucous membrane in man. Archs oral Biol. 17. 513-523.
oral &I.
Vol. 22. pp
175 to 180 Pergaman
Press 1977. Printed
m Great Britain
A TONIC VIBRATION THE JAW OPENING
REFLEX EVOKED IN MUSCLES IN MAN
G. HELLSINC Department of Stomatognathic Physiology and EMG-laboratory, Faculty of Odontology, University of Giitegorg, Sweden, Department of Clinical Neurophysiology,
University of Uppsala,
Sweden
Summary--Motor effects induced by vibration of the mouth opening muscles were studied in eight subjects. All exhibited a tonic motor response with many characteristics in common with the tonic vibration reflex @VR) as previously studied in limb muscles and jaw elevators: an involuntary contraction appeared in the jaw openers with gradual onset and gradual decline. The contraction was accompanied by a reciprocal inhibition of the voluntarily activated jaw elevators; it was susceptible to voluntary control-when allowed visual feed-back from a torquemeter all subjects were able to suppress the TVR and keep contraction force in their jaw elevators constant. The results suggest that the jaw openers are supplied with proprioceptors functionally similar to spindle endings in that on sustained activation they can produce tonic autogenic excitation and reciprocal inhibition, i.e. the pattern of the classical tonic stretch reflex. However, the vibration-induced contraction in the jaw openers did not exhibit one of the features typical for the TVR in the jaw elevators. The marked grouping of discharges synchronous with each wave of vibration, seen in gross EMG recordings from jaw elevators, was not seen in any one of the three jaw opening muscles examined, the anterior belly of the digastric, the mylohyoid and one of the infrahyoid muscles. As the vibration-induced synchronization is considered to depend on monosynaptic projections, the results imply that the jaw openers are devoid of such projections and that the TVR is mediated through polysynaptic pa.thways.
IINTRODUCTION
TVR is probably, like the classical tonic stretch reflex (TSR), mediated predominantly by longer polysynaptic paths (Granit et al., 1957; Kanda, 1972; Homma and Kanda, 1973; Matthews, 1975; Hagbarth, Hellsing and Liifstedt, 1976b; Burke and Schiller, 1976). A previous study (Hagbarth et al., 1976b) demonstrated that in man reciprocal inhibition of the suprahyoid muscles occurs when the jaw elevators are vibrated. This finding was not regarded as contradictory to the claims of Kidokoro et al. (1968) that in the cat no short latency reciprocal inhibition of jaw openers occurs in response to electrically induced synchronized volleys in Ia afferents from the jaw elevators. We argued that the absence of short latency oligosynaptic projections to antagonistic motoneurones does not exclude the presence of longer polysynaptic projections, brought into action by sustained inflow in Ia afferents and mediating tonic inhibitory effects. By analogy, we questioned whether tonic vibration reflexes can be elicited in the jaw openers, even though short latency dynamic stretch reflexes are not present in these muscles. The present study was to test this suggestion.
Functional characteristics different from corresponding properties of limb muscles have been attributed to the masticatory muscles. In man few, if any, muscle
spindles have been recognized in the jaw opening muscles (Baum, 1900; Gregor, 1904; Voss, 1956). Attempts to evoke monosynaptic stretch reflexes in the digastric muscle in cat have been unsuccessful (Blom, 1960). It has also been assumed that the jaw elevators are not subject to reciprocal inhibitory effects of proprioc:ptive origin in the jaw openers (Godaux and Desmedt, 1975a). Furthermore, evidence indicates that proprioceptive afferents in muscle nerves of jaw-closing muscles, richly supplied with muscle spindles, do not influence digastric motoneurones (Szentagothai. 1948; Kidokoro et al., 1968). By contrast, it is ,well known that a reciprocal reflex organization exists in limb muscles, i.e. inhibition of antagonists is exerted by excitation of the Ia afferents of the agonists. Sinusoidal vibration of various muscles elicits the so-called tonic vibration reflex, TVR (Hagbarth and Eklund, 1966; de Gail, Lance and Neilson, 1966; for review, Hagbarth, 1973). This phenomenon is generally believed to result from excitation of the primary endings of the muscle spindle, end organs which are very sensitive to vibration both in cat (Bianconi and van der Meulen, 1962; Brown, Engberg and Matthews, 1967) and in man (Hagbarth et al., 1976a). Even though the TVR results from excitation of the same end organs as the tendon jerk reflex, the two reflexes are mediated through different reflex arcs; whereas the dynamic tendon jerk reflex is dependent upon monosynaptic projections, the
MATERIALS AND METHODS
Eight healthy subjects without symptoms of mandibular dysfunction and with well-preserved dentitions were used. They were seated in a comfortable chair during the trials. Jaw muscle torque was recorded during closure using a strain gauge built into a rigid, 10 mm thick mouthpiece placed between the front teeth. 175
G. Hellsing
176
Before the trial, the subjects were trained to keep a constant bite force by watching the strain gauge meter to determine the effort required to keep the pointer at 55N (about 5.4 kg). It was then checked that this constant pressure could be kept without visual feed-back. The subject was instructed to keep this effort constant during the trial whatever vibration-induced changes in torque he might perceive, i.e. he was trained not to compensate for these changes. Electromyographic (EMG) records were made from the masseter, temporalis and in three cases from the infrahyoid muscles with pairs of intracutaneous hooks 10mm apart (Ahlgren, 1967). In all subjects, EMG was recorded from the anterior belly of the digastric muscle with a coaxial needle electrode. The signals were amplified by Disa Type 14A30 and displayed on a Mingograph 800. The torque signals were amplified and displayed together with the electromyograms. The vibrator was an electric motor with an eccentric load. It was manually applied and had a contact area of about 200 mm’. Site of application was below the anterior belly of the digastric muscle, close to the midline, either contra- or ipsilateral to the side where the EMG electrodes were placed. Contralateral application was often necessary to avoid artifacts when the vibrator was applied too close to the electrodes. The vibration amplitude was 0.2mm and the vibration frequency 130Hz. In three subjects, vibration was also applied over other mouth openers, i.e. the mylohyoid and the infrahyoid muscles. To determine whether the motor-unit discharges induced by the vibration were phase-locked to the vibration cycle, the EMG recordings of 5 subjects were displayed on fast oscilloscope sweeps triggered by the
@
of an Entran EGC-240 Accelerometer output attached to the vibrator. The transverse (anterior) cutaneous nerve of the neck of one subject was blocked with 1.8 ml of 2 per cent lignocaine (Xylocaine Astra) with l/8000 Lepinephrine to exclude any reflex influence from cutaneous receptors in the vibrated region. This was done bilaterally as some cutaneous receptors, such as the Pacinian corpuscles, are extremely sensitive to vibration. In another subject, the effects of ipsilateral electrical stimulation of the mandibular alveolar nerve at the mental foramen were studied. This nerve transmits sensory impulses from the lower lip, the chin, the anterior part of the mandibular alveolar process and the lower front teeth. The duration of the stimulating pulses was varied between 0.1-1.0 msec and the stimulation frequency varied between 140 Hz. A Grass S88 stimulator with isolation unit SIUS was used. The stimulating electrodes were insulated needles with 2 mm-long bare tips. RESULTS Motor responses induced by vibrution of the supruhyoid muscles In all subjects, vibration of the contra- or ipsilateral anterior belly of the digastric muscle produced a tonic motor response which had many features in common with the TVR as studied in limb muscles and in the jaw elevators. Thus, there was a progressive augmentation of the EMG activity of the digastric muscle during vibration, an activity which slowly declined after cessation of vibration, This tonic reflex contraction was accompanied by a simultaneous decrease of
]
‘.
m. temporalis
I I+.
Fig. 1. Changes in jaw muscle EMG and bite force induced by vibration of the digastric muscle. Bar at bottom of figure = duration of vibration at 130 Hz. Drop of mouthpiece indicated on the bar. Note gradual onset of the digastric contraction and simultaneous decrease of the masseter muscle EMG activity.
Vibration reflex in jaw opening muscles the EMG activity in the jaw elevators, e.g. the masseter (Fig. 1). On cessation of vibration, the masseter activity slowly recovered to or even exceeded the previbration level. As a consequence of these motor phenomena, the bite force was diminished to such an extent that, after a mean latency of .3.8 s (S.D. 2.0) all subjects dropped the strain gauge. In five subjects, this produced immediate activation of the masseter muscle causing rebound jaw closure. On continued vibration, the masseter EMG-activity was inhibited again. When allowed visual feed-back, all subjects were able to suppress the vibration-induced effects, i.e. to maintain constant pressure. Subjectively, the vibration-induced contraction of the mouth openers was strong. The subjects reported the corresponding effects upon vibration of the masseter muscle to be weaker. Cutaneous anaesthesia of both sides of the neck did not change the vibration-induced motor responses.
a
I
177
5ms
[
100 pv
b Fig. 3. Electrical stimulation of the mandibular alveolar nerve. Upper trace: masseter EMG; lower trace: digastric muscle EMG. Stimulus frequency lOimp/s. a. Subject relaxed. No responses visible in either muscle; b. Sustained voluntary contraction of the digastric muscle. No further activation induced by stimulation. The masseter muscle remains silent.
a
Motor responses induced by vibration of the infrahyoid muscles
b -5mS
loo@!
When the vibrator was applied below the hyoid bone to stimulate the infrahyoid musculature, the subjective experiences, as well as the EMG- and torque changes, were much the same as when the suprahyoid musculature was vibrated. Progressive increase of EMG activity of the infrahyoid muscles as well as reciprocal inhibition of the elevators developed and the subject dropped the strain gauge after a few seconds. Effects of electrical
C
Fig. 2. Electrical stimulation of the mandibular alveolar nerve during sustained voluntary contraction of the masseter muscle. As in Figs. 4 and 5. 25 consecutive sweeps, triggered by the electrical pulses, are superimposed. Stimulus duration 0.1 msec. a. Upper trace: masseter muscle EMG; lower trace: digastric muscle EMG. Impulses delivered at l/s cause inhibition of the masseter muscle EMG-activity with a latency of about 7.5 msec. Duration of silent period about 17 msec. No EMG activity induced in the digasttic muscle; b. Masseter muscle EMG. Stimulation frequency lOimp/s. The silent period is shortened compared with a; c. Masseter muscle EMG. Stimulation frequency 40imp/s. The silent period still present.
stimulation of the alveolar
nerve
Electrical stimulation of the ipsilateral mandibular alveolar nerve applied to one subject with a stimulus just above pain-threshold intensity caused mucosal dysaesthesia and an ache in the ipsilateral anterior teeth of the lower jaw, indicating that the stimulus was adequately applied. The duration of the impulses was varied between O.l-l.Omsec during the trials without any noticeable change in the response. Single pulses delivered while the subject was clenching his teeth resulted in transient inhibition of the masseter muscle, i.e. a silent period, with a latency of about 17 msec (Fig. 2). On increasing stimulation frequency, the duration of the silent period was shortened but remained clearly visible even at a frequency of 40 Hz. No activation of the anterior belly of the digastric muscle could be seen at any frequency (Fig. 2). When the subject was completely relaxed, no activation of either muscle could be seen during stimulation. Stimulation produced no change in the gross EMG pattern when applied during sustained contraction of the digastric muscle (Fig. 3).
178
Lack TVR
G. Hellsing
of motor
synchronization
in the jaw-opening
As shown by Godaux and Desmedt (1975b) and confirmed by Hagbarth et al. (1976b), the TVR of the human jaw elevators is characterized by a marked grouping of the EMG-potentials in synchrony with the vibration waves, a phenomenon attributed to monosynaptic timing of the discharges from the firing motoneurone pool (Desmedt and Godaux, 1975). This timing phenomenon was absent in the vibrationinduced contractions of the jaw openers. Marked grouping of the EMG potentials in the masseter muscle occurred during jaw elevator vibration, both when the masseter contraction was maintained voluntarily and when it was reflexly induced by the vibratory stimulus (Fig. 4). By contrast. vibration of the jaw openers did not cause similar synchronization of the EMG potentials in the digastric, mylohyoid or infrahyoid muscles, whether the contraction in these muscles was maintained voluntarily or the EMG activity had developed as a result of the vibration (Fig. 5).
-
2 ms
[
IOO~V
DISCUSSION
All subjects experienced difficulty in following the instruction to keep constant effort when vibration was applied over the jaw openers. It was hard to concentrate upon the task, especially when they were about to drop the strain gauge, but it was carefully checked that the subjects tried not to compensate for any vibration-induced changes on torque that they might perceive. Fig. 5. Vibration of different contralateral jaw openers. 130 Hz, 0.2 mm. 15 superimposed sweeps triggered by vibration wave; a. Subject relaxed at start of vibration. Upper trace: vibration wave; second trace: masseter EMG; third, forth and fifth traces: EMG recordings from the digastric, the mylohyoid and the infrahyoid muscles, respectively. The vibration-induced EMG-activny in the jaw openers is asynchronous in nature, i.e. the EMG discharges are not phase-locked to the vibration wave; b. Vibration of the same muscles during sustained voluntary contraction of the mouth openers does not cause any grouping of the motor unit discharges or any activation of the masseter muscle.
a -22s
[ 100 /Lv
b Fig. 4. Marked synchronization to vibration wave (upper trace) of the motor unit discharges in the masseter muscle (middle traces) during jaw elevator vibration. Digastric EMG-lower trace. 130Hz, 0.2 mm. 15 superimposed sweeps triggered by vibration wave. a. The subject relaxed at the start of vibration, i.e. the EMG activity induced by the vibratory stimuli; b. The vibration applied during sustained voluntary contraction of the masseter muscle.
The fact that all subjects dropped the strain gauge approximately 4s after the start of vibration cannot be explained merely in terms of reduced contraction force in the jaw elevators. To the initial bite force of 55 N exerted by the subject, there was an additional upward pressure of 10-20 N when the vibrator was applied and the tonic reflex contraction in the jaw opener was powerful enough to overcome this pressure. The results indicate that there are proprioceptors in the jaw opening muscles which are sensitive to vibration and on sustained activation produce the wellknown pattern of the tonic vibration reflex and the classical stretch reflex, i.e. tonic autogenic excitation and reciprocal inhibition. It may be objected that the reflex contractions were not strictly autogenic as they also occurred in the contralateral jaw opening muscles. However, there was probably a mechanical spread of the vibration waves across the midline, suffi-
Vibration reflex in jaw opening cient to activate receptors in the contralateral muscles. The possibility that the reflex response resulted from vibration-induced excitation of skin receptors is excluded by the test during skin anaesthesia. If vibration-sensitive mechanoreceptors around the mandibular teeth or in the mandibular mucosa were responsible for the reflex high-frequency tetanic stimulation of the mandibular alveolar nerve would have been expected to cause a similar tonic jaw opening reflex. The results show that the phasic jaw opening reflex resulting from single shocks at l/s to the alveolar nerve is accompanied, not by contraction in the jaw openers, but by a lransient inhibition of the jaw elevators (Yemm, 1972; Gillings and Klineberg, 197.5; Desmedt and Godaux, 1976) and sustained tetanic stimulation of this nerve did not produce a tonic contraction in the jaw opening muscles similar to that induced by vibration. Furthermore, it seems unlikely that vibration applied as far down as over the infrahyoid muscles could spread to receptors in the mouth, supplied by the alveolar or lingual nerves, but such vibration was efficient in eliciting a tonic contraction in the jaw openers. Another possibility which is difficult to exclude experimentally would be that submandibular vibration causes excitation of receptors in the deep fascia. If that were the case, it would be true for other muscles. The different motor response from the jaw elevators (synchronization) and the lack of motor response from the facial muscle (Eklund and Hagbarth, 1966) would then be hard to explain. It could be argued that afferent impulses from platysma might be responsible for the motor response. As platysma belongs to the facial muscles this is probably not so. What is the nature of the vibration-sensitive proprioceptors in the jaw-openers responsible for the observed tonic reflex? Some reports indicate that tonic vibration reflexes cannot be elicited in the facial muscles, and this has been attributed the lack of spindle end organs in these muscles (Eklund and Hagbarth, 1966). In view of the lack of histological evidence of muscle Ispindles in the jaw openers (Baum, 1900; Gregor, 1904; Voss, 1956), no TVR and no dynamic stretch rellexes would be expected in these muscles. However, it is possible that these muscles contain receptors differing in shape from ordinary spindle endings but with similar functional characteristics, in the sense that they are vibration-sensitive stretch receptors whose sustained activation is capable of producing .a tonic stretch reflex, presumably mediated through polysynaptic paths. Nevertheless, the jaw openers differ from the jaw elevators in that they do not exhibit any short latency, phasic stretch reflexes. That vibration of jaw openers produced a tonic reflex contraction with no evidence of monosynaptically induce’d EMG-synchronization supports the view that the TVR is not critically dependent on monosynaptic projections (Homma and Kanda, 1973; Hagbarth rt a/., 19’76b; Burke and Schiller, 1976). Lamarre and Lund (1975) showed that monosynaptic load compensation is prominent in the jawclosing muscles. During mastication, a load was applied to the mandible, resulting in an increase in the EMG activity of the masseter muscle after a delay comparable to that of the jaw-jerk reflex (mean
179
muscles
7.2 msec). EMG recordings from the digastric muscle when loads were applied in closing direction as well as when this muscle was loaded directly during opening movements demonstrated a long latency (24-34msec) response. This infers the existence of a polysynaptic load compensating reflex in the digastric muscle in agreement with the results of the present study. Horseradish peroxidase (HRP) injected into muscle is taken up by nerve terminals and transported to the bodies of the neurones (Kristensson and Olsson, 1971). After injection of HRP in the anterior belly of the digastric and the mylohyoid in the cat, Alvarado-Mallart et al. (1975) found labelled neurones in the ipsilateral posterior half of the mesencephalic nucleus V. This agrees with the present findings and suggests that jaw opening muscles have afferent projections to the mesencephalic nucleus, a nucleus considered to be proprioceptive. Acknowledgements-1 wish to thank Dr Karl-Erik Hagbarth, the department of Clinical Neurology, Academic Hospital, Uppsala, for generously letting me use the facilities of his department and also for constructive criticism and guidance. I am also indebted to Ing. Lars Llifstedt for technical assistance and Dr David Burke for valuable advice during the preparation of this paper. REFERENCES
Ahlgren J. 1967. An intracutaneous
needle electrode for kinesiologic EMG studies. Acta odont. stand. 25, 15-19. Alvarado-Mallart M. R., Batini C., Buisseret-Delmas C. and Corvisier J. 1975. Trigeminal reoresentations of the masticatory and extraocular propriiceptors as revealed by horseradish peroxidase retrograde transport. Expl. Brain Res. 23, 167-179. Baum J. 1900. BeitrHge zur Kenntnis der Muskelspindeln. Anat. Heffe, 1. Abt. 13, 249-305. Bianconi R. and van der Meulen J. P. 1963. The response to vibration of the end organs of mammalian muscle spindles. J. Neurophysiol. 26, 177-190. Blom S. 1960. Afferent influences on tongur muscle activity. Acta physiol. stand. 49 (Supplement 170), l-97. Brown M. C., Engberg I. and Matthews P. B. C. 1967. The relative sensitivity to vibration of muscle receptors of the cat. J. Physiol. 192, 773-800. Burke D. and Schiller H. 1976. The discharge pattern of single motor units in the tonic vibration reflex of human triceps surae. J. Neural. Neurosurg. Psychiat. 39, 729-741. Desmedt J. E. and Godaux E. 1975. Vibration-induced discharge patterns of single motor units in the masseter muscle in man. J. Physiol. 253, 429-442. Desmedt J. E. and Godaux E. 1976. Habituation of exteroceptive suppression and of exteroceptive reflexes in man as influenced by voluntary contraction. Brain Rex 106, 21-29. Eklund G. and Hagbarth K.-E. 1966. Normal variability of tonic vibration reflexes in man. Expl. Neural. 16, 8&92. de Gail P., Lance J. W. and Neilson P. D. 1966. DitTerential effects on tonic and phasic reflex machanisms produced by vibration of muscles in man. J. Neural. Neurosurg. Psychiat. 29, l-11. Gillings B. R. D. and Klineberg I. J. 1975. Latency and inhibition of human masticatory muscles following stimuli. J. dent. Res. 54, 269-279. Godaux E. and Desmedt J. E. 1975a. Human masseter muscle: H- and tendon reflexes. Their paradoxical potentiation by muscle vibration. Archs Neural., Chicago 32, 229-234.
180
G. Hellsing
Godaux E. and Desmedt J. E. 1975b. Evidence for a monosynaptic mechanism in the tonic vibration reflex of the human masseter muscle. J. Neural. Neurosurg. Psychiat. 38, 161-169. Granit R., Phillips C. G., Skoglund S. and Steg G. 1957. Differentiation of tonic from phasic alpha ventral horn cells by stretch, pinna and crossed extensor reflexes. J. Neurophysiol. 29, 47@481. Gregor A. 1904. Ueber die Vertheilung der Muskelspindeln in der Muskulatur des menschlichen FGtus. Arch. Anat. Physiol. Anat. Abt. Jahrg. 1904, 112-196. Hagbarth K.-E. 1973. The effect of muscle vibration in normal man and in patients with motor disorders. In: New Developments in Electromyography and Clinicul NeuroDhvsioloav (Edited bv Desmedt J. E.). Vol. 3. vv. _. 428-443.’ Kar&, ‘Base]. I Hagbarth K.-E., Burke D., Wallin G. and LGfstedt L. 1976a. Single unit spindle responses to muscle vibration in man. In: Undorsranding the Stretch Reflex. Progress in Brain Research (Edited by Homma S.), Elsevier. Amsterdam. Hagbarth K.-E. and Eklund G. 1966. Motor effects of vibratory stimuli in man. In: Muscular Affrrents and Motor Conrrol. Nobel Symposium I (Edited by Granit R.). p. 177. Almqvist & Wiksell, Stockholm. Hagbarth K.-E.. Hellsing G. and Liifstedt L. 197613. The TVR and vibration-induced timing of motor impulses in the human jaw elevators. J. Neural. Neurosurg. Psq‘chiat. 39, 719-728. Hirayama K., Homma S., Mizote M., Nakajima Y. and Watanabe S. 1974. Separation of the contributions of voluntary and vibratory activation of motor units in man by cross-correlograms. Jap. J. Physiol. 24, 293-304. Homma S., Kanda K. and Watanabe S. 1971 Tonic vibration reflex in human and monkey subjects. Jap. J. Physiol. 21. 419430.
Homma S., Kanda K. and Watanabe S. 1972. Preferred spike intervals in the vibration reflex. Jap. J. Physiol. 22, 421432. Hufschmidt H. J. 1958. Wird durch Muskelvibration eine Eigenreflexreihe erzeugt? Pjiigers Arch. ges Physiol. 267, 508-516. Kanda K. 1972. Contributions of polysynaptic pathways to the tonic vibration reflex. Jap. J. Physiol. 221, 367-377. Kidokoro Y., Kubota K., Shuto S. and Sumino R. 1968. Reflex organization of cat masticatory muscles. J. Neurophysiol. 31, 6955708. Kristensson K. and Olsson Y. 1971. Retrograde axonal transport of protein. Brain Res. 29, 363-365. Lamarre Y. and Lund J. P. 1975. Load compensation in human masseter muscles. J. Physiol. 253, 21-35. Matthews P. B. C. 1975. The relative unimportance of the temporal pattern of the primary afferent input in determinating the mean level of motor firing in the tonic vibration reflex. J. Physiol. 251, 333-361. Sherrington C. S. 1917. Reflexes elicitable in the cat from pinna vibrissiae and jaws. J. Physiol. 51, 404431. Sommer J. 1941. Synchronisierung motorischer Impulse und ihre Bedeutung fir die Neurophysiologische Forschung. 2. ges Neural. Psychiat. 172, 501S530. Szentagothai J. 1948. Anatomical considerations of monosynaptic reflex arcs. J. Neurophysiol. 11, 445-454. Voss H. 1956. Zahl und Anordnung der Muskelspindeln in den oberen Zungenbeinmuskeln im M. trapezius und M. latissimus dorse. Anat. Anz. 103, 443446. Yemm R. 1972. Reflex jaw opening following electrical stimulation of oral mucous membrane in man. Archs oral Biol. 17. 513-523.