Behavior of Jaw Muscle Spindle Afferents During Cortically Induced Rhythmic Jaw Movements in the Anesthetized Rabbit

O. Hidaka,1,2 T. Morimoto,1 T. Kato,1 Y. Masuda,1 T. Inoue,1 and K. Takada2

 1Department of Oral Physiology and  2Department of Orthodontics, Osaka University Faculty of Dentistry, Suita, Osaka, 565-0871 Japan


    ABSTRACT
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ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES

Hidaka, O., T. Morimoto, T. Kato, Y. Masuda, T. Inoue, and K. Takada. Behavior of Jaw Muscle Spindle Afferents During Cortically Induced Rhythmic Jaw Movements in the Anesthetized Rabbit. J. Neurophysiol. 82: 2633-2640, 1999. The regulation by muscle spindles of jaw-closing muscle activity during mastication was evaluated in anesthetized rabbits. Simultaneous records were made of the discharges of muscle spindle units in the mesencephalic trigeminal nucleus, masseter and digastric muscle activity (electromyogram [EMG]), and jaw-movement parameters during cortically induced rhythmic jaw movements. One of three test strips of polyurethane foam, each of a different hardness, was inserted between the opposing molars during the jaw movements. The induced rhythmic jaw movements were crescent shaped and were divided into three phases: jaw-opening, jaw-closing, and power. The firing rate of muscle spindle units during each phase increased after strip application, with a tendency for the spindle discharge to be continuous throughout the entire chewing cycle. However, although the firing rate did not change during the jaw-opening and jaw-closing phases when the strip hardness was altered, the firing rate during the power phase increased in a hardness-dependent manner. In addition, the integrated EMG activity, the duration of the masseteric bursts, and the minimum gape increased with strip hardness. Spindle discharge during the power phase correlated with jaw-closing muscle activity, implying that the change in jaw-closing muscle activity associated with strip hardness was caused by increased spindle discharge produced through insertion of a test strip. The increased firing rate during the other two phases may be involved in a long-latency spindle feedback. This could contribute to matching the spatiotemporal pattern of the central pattern generator to that of the moving jaw.


    INTRODUCTION
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ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES

Masticatory movements are regulated by the texture of food, and greater activities of the jaw-closing muscles are produced when the hardness of the food increases (Lund 1991). This suggests that the control of mastication is highly dependent on sensory feedback. Experiments using cortically induced rhythmic jaw movements (CRJMs) in rabbits (Lavigne et al. 1987; Morimoto et al. 1989) have demonstrated that the integrated electromyogram (EMG) of the masseter muscle (Ma-IEMG) increases during CRJMs when a test material is chewed between the opposing cheek teeth. The effect is dramatically reduced when the periodontal and muscle spindle afferents are cut, indicating that the two sensory inputs are essential for the facilitatory effect. On the other hand, this facilitatory effect is only partially decreased when periodontal sensation alone is eliminated, and Ma-IEMG and masticatory force are still regulated according to strip hardness (Hidaka et al. 1997b). During mastication, therefore, there is the potential for muscle spindle afferents to regulate the jaw-closing muscle activity in a hardness-dependent manner. It seems that a simple reflex mechanism alone cannot explain the whole facilitatory effect (Hidaka et al. 1997b). This is because an early part of the facilitation of the masseter muscle activity sometimes occurs before the minimum latency for the masseter response to strip application (i.e., before the minimum latency [6 ms] of the monosynaptic stretch reflex). Sometimes the masseter facilitation occurs even before the onset of a load on the teeth. The early activity persists after cutting the periodontal afferents, suggesting that muscle spindle afferents play a crucial role in the production of the early facilitatory effect. In support of this proposal, a lesion of the mesencephalic trigeminal nucleus (MesV) almost abolishes the early facilitatory response (Komuro et al. 1997).

The behavior of spindle afferents during fictive mastication induced by cortical stimulation has been reported by other investigators (Kolta et al. 1990). But the activity of muscle spindle afferents during CRJMs has only been noted in two brief reports (Morimoto et al. 1995a,b). How muscle spindles are involved in the regulation of jaw-closing muscle activity therefore remains an unanswered question.

In the present study we sought to provide an insight into the neural mechanism for mastication by analyzing how jaw muscle spindle afferents behave, according to the hardness of a chewed material, during CRJMs. The use of CRJMs in studies of mastication enables measurement of the effect of the chewed material alone on parameters relating to mastication. The texture of the material can be controlled, and CRJMs obtained during chewing can be compared with those obtained when not chewing. Some data from this study have been reported briefly (Hidaka et al. 1997a).


    METHODS
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ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES

All surgical procedures were approved by the Osaka University Faculty of Dentistry Intramural Animal Care and Use Committee and were almost the same as those described previously (Liu et al. 1993). In this investigation, 24 male rabbits weighing 2.5-3.5 kg were used. Each animal was anesthetized with ketamine (16 mg/kg, Ketalar 10, Sankyo) and thiamylal sodium (20 mg/kg) injected in an auricular vein. The trachea was cannulated, and anesthesia was maintained during surgery by a mixture of halothane and oxygen so that a corneal reflex and spontaneous eye movements were not present. A photo diode was attached to the mentum, and jaw movements were monitored with an optoelectronic recording apparatus (C2399, Hamamatsu Photonics, Hamamatsu City, Japan). The animal's head was fixed in a stereotaxic apparatus so that the lambda was 1.5 mm below the bregma (Sawyer et al. 1954). The cortical surface was exposed (1-7 mm anterior and 3-8 mm lateral of the bregma) for electrical stimulation of the cerebral masticatory area (CMA). The rectal temperature was maintained between 36 and 38°C with a heating pad. The EMGs were recorded with pairs of Teflon-coated stainless steel wires (with bared tips 1.0 mm in length) inserted into the left masseter and digastric muscles on the side contralateral to the cortical stimulation. On the basis of the results of our previous study (Morimoto et al. 1989), masseteric activity was recorded from the deep anterior part of the muscle.

Cortical stimulation

Intracortical microstimulation was achieved with square pulses (0.2 ms, <80 µA, 30 Hz) delivered through glass-coated metal electrodes with an impedance of 1-2 MOmega at 1 kHz, and crescent-shaped jaw movements were induced. The anesthesia during the experiment was controlled at a level slightly lighter than that during surgery. The heart rate was ~230 beats/min. The lowest arterial pressure of the femoral artery was ~75 mmHg, and the highest pressure ranged between 110 and 130 mmHg. Pupillary constriction appeared when a light was directed into the animal's eye. No obvious changes in the heart rate, respiration, pupillary size, or arterial pressure were induced by CMA stimulation.

Intraoral stimulation

During CRJMs, a thin test strip of polyurethane foam was held with forceps by an experimenter and placed between the animal's opposing left molar teeth. Three test strips, each 2-mm thick, 5-mm wide, and 15-mm long were used, and each strip was designated as soft, medium, and hard, respectively (hardness: 27, 67, and 91 respectively; Japanese Industrial Standard, K 6301).

Recording from muscle spindle afferents

A craniotomy was performed to allow access to the left MesV (11-16 mm posterior and 0-4 mm lateral of the bregma), and a small cylinder was fixed to the skull at the defect and filled with liquid paraffin. Passive movements were applied to the lower jaw with a servo-controlled stretcher (EMIC 513A) attached to screws at the symphysis menti. During sinusoidal and ramp-and-hold stretches, spikes were recorded from the MesV neurons with a glass-coated tungsten microelectrode (15-µm-diam tip, 1-3 MOmega impedance at 1 kHz). The spindle responses were recorded at least 6 hours after the administration of thiamylal sodium. The following criteria (see also Masuda et al. 1997) were used for identification of MesV spindle units: histological identification of the recording sites in the MesV, a low threshold for unit discharge to passive jaw opening; neuronal firing rates >100 Hz during mastication, absence of response to occlusal contact of the upper and lower teeth, and absence of response to pressure applied to the teeth, gingiva, or vibrissae. In addition, we identified masseteric units by the following features: a response to gentle palpation of the masseter surface (Fig. 1A) and a decrease or elimination of any preexisting discharges in response to weak electrical stimulation of the muscle belly (Fig. 1B). For the nonmasseteric units, we confirmed a response to gentle palpation of a small superficial portion of the temporal muscle and a response to a brief pressure applied to the eyeball.



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Fig. 1. Muscle spindle responses to various mechanical stimuli. A: palpation; jaw was held fully closed. B: twitch contraction; jaw was held at an opened position of 5 mm. C: ramp stretch; jaw was opened to 5 mm from a starting position of 2 mm. Bottom: records with expanded time base. Ma, masseter muscle EMG; Vert, vertical jaw movements.

At the finish of the experiments, electrolytic lesions were made at the recording sites to permit identification of their locations. Each rabbit was given a fatal dose of thiamylal sodium and perfused intracardially with saline and then with buffered formalin. The brains were extracted, sectioned at the thickness of 50 µm in the frontal plane, and stained with cresyl violet.

Data analysis

An eight-channel digital audio tape data recorder (PC-208 M, Sony-Magnescale, Tokyo, Japan) was used to record the jaw movements, EMGs, and spindle discharges. The data were transferred to a computer (Power Macintosh 9500/200), digitized at 500 Hz for the jaw movements, 2 kHz for the EMGs, and 20 kHz for the spindle discharges. Spindle units were discriminated and identified as single units on the basis of shape (including amplitude) of the units by software (Spike2, Cambridge Electronic Design, Cambridge, UK). The EMG data were software rectified and smoothed by a 9-point moving average, and the area under the smoothed EMG record was denoted as integrated EMG (IEMG).

The CRJMs were recorded before and during the strip application, and these periods were designated as control cycles and experimental cycles, respectively. The interval between two consecutive maximum jaw-openings was defined as a chewing cycle, and its length was designated as a total cycle length (TCL). A chewing cycle was composed of three phases: The jaw-opening phase was defined as the time from the most closed position to the most opened position, the jaw-closing phase was the most opened position to the lateralmost position, and the power phase was the phase between the first two phases.

The mean values were calculated for each of the following variables from five successive chewing cycles, and the mean value was used as a representative value for the chewing cycles: the minimum gape, the mean frequency of spindle discharge, IEMG, and the EMG burst duration.

The EMG burst duration was determined in the following way. The mean ± SD of the digitized EMG during one-tenth of the TCL immediately before the maximum jaw opening was first calculated for the masseteric EMG. Each burst was then identified by when the muscle activity exceeded the mean level by 3 SD for >= 30 ms.

Statistical analysis

In each group, each variable was tested for a normal distribution with a chi 2 test, and the homogeneity of all variances was tested with a Bartlett test. The results of these tests determined which statistical analysis was performed next. A one-way ANOVA or the Kruskal-Wallis test was used to examine for differences among the three groups classified by strip hardness. A Wilcoxon signed-rank test was used to determine significant differences between control cycles and experimental cycles. Scheffé's F test was used for multiple comparisons when a statistically significant difference was found among the three groups. P < 0.05 was assumed to be statistically significant. The data were presented as the mean ± SE.


    RESULTS
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INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES

We examined data, including 43 spindle afferents, from 13 rabbits. Twenty-one of the spindle afferents were from the masseter muscle, 3 were from the temporalis, and the muscle of origins for the remaining 19 spindle afferents were not clearly identified. In the masseter, the spindles were located in the anterior or central region. Forty-three stable units were recorded during chewing of the soft test strip and during chewing of the medium strip. However, only 36 stable units were recorded when the hard test strip was applied. The weakness of the rabbit skull (in comparison with other animals, e.g., cats) sometimes prevented a rigid fixation to the stereotaxic frame and hampered stable recording conditions. Consequently, fewer stable units were obtained during chewing of the hard test strip.

Behavior of muscle spindle afferents during CRJMs

Records of the discharges of a spindle neuron are shown in Fig. 2A. The receptive field for this neuron was in the ventral anterior part of the masseter muscle. When rhythmic jaw movements were induced by rubbing the hard palate (a chewing strip was not applied), spindle discharges were absent at the end of the jaw-closing phase (Fig. 2A, Palatal stimulation). This period of silence was also apparent in records obtained during CRJMs when a chewing-strip was absent (Fig. 2A, No strip) although the regularity of the spindle discharge in a jaw movement cycle was different. Spindle discharges continued throughout the jaw closure, however, when a chewing strip was applied. Changes in the number of discharges of the unit, according to strip hardness, are shown in Fig. 2B. The activity of the masseter muscle increased with strip hardness.



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Fig. 2. The behavior of a muscle spindle afferent during reflexively evoked rhythmic jaw movements and during CRJMs. A: modification of spindle unit firing. The leftmost records (Palatal stimulation) are from rhythmic jaw movements induced by rubbing the hard palate, with no strip applied. The other records (No strip, Soft strip, Medium strip) refer to CRJMs and the hardness of the test strip. For spindle discharge, small vertical lines represent unit discharges, and larger vertical lines at regular intervals represent artifacts of cortical stimulation; B: the phase relationship of unit discharges to the jaw movement cycle. Five cycles of each trial were aligned at the point of minimum jaw opening (indicated by the dotted line). Spikes are represented as raster records, and histograms showing mean spike counts per bin (binwidth: 5 ms). Frequency, the instantaneous neuronal discharge frequency; Hor, horizontal jaw movements. Ma-IEMG, the integrated masseter muscle EMG (the area under the software-rectified and -smoothed EMG of the masseter muscle).

We compared the discharge frequency of this unit during CRJMs with and without chewing strips after normalizing the latter so that the time course matched (Fig. 3). When a test strip was applied, the minimum gape increased, and the muscles were at a longer length during the power phase with the test strip in place than during this phase in control cycles (i.e., the muscles were not shortened to the same degree). The discharge pattern in control cycles (Fig. 3, +) was similar to the pattern in experimental cycles (Fig. 3, open circle ) during the jaw-opening and jaw-closing phases. The discharge patterns were very different, however, during the power phase, when discharges were observed only when a chewing-strip was applied.



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Fig. 3. Neuronal discharge frequency during control cycles and experimental cycles. Unit is the same as in Fig. 2. The time axis of control cycles has been normalized to match the time of the experimental cycles. (+), the interspike interval in control cycles (test strip not applied); (open circle ), the interspike interval experimental cycles (soft test strip applied). In the lower part of the diagram, jaw movements of control cycles are shown by a thin line and those of experimental cycles by a thick line.

Discharges of a different unit are illustrated in Fig. 4A. The muscle of origin for this afferent discharge was not the masseter muscle and could not be clearly identified. This unit is likely to be a muscle spindle afferent (see DISCUSSION). When a test strip was absent, neuronal activity was observed during the jaw-opening phase; during the remaining part of the chewing cycle the unit did not discharge. A different spindle discharge pattern was observed, however, after application of a soft chewing strip. Discharges were then observed mainly in the latter half of the jaw-opening phase and the period around the minimum jaw opening. A similar pattern of discharge activity was observed during the chewing of the medium strip, but the firing rate in the power phase was higher. The increased rate of spindle discharge was further pronounced when the hard strip was chewed, and the discharge became continuous throughout the chewing cycles. The discharge pattern displaying an increased frequency around the time of minimum gape (i.e., around maximum jaw closure) was observed in 7 (including 3 masseteric) of the 43 units.



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Fig. 4. Modification of the phase relationship of unit discharges to the jaw movement cycle, according to strip hardness. A: nonmasseteric unit showing a clear cessation of firing before strip application. During strip application, this neuron actively fired, and the firing rate in the power phase became higher when harder strips were placed between the molar teeth. The masseteric EMG activity also increased progressively with strip hardness. B: masseteric unit showing no clear cessation of firing during the power phase of control cycles.

The behavior of another masseteric unit is shown in Fig. 4B. During the power phase of control cycles, a clear cessation of firing was not observed. In experimental cycles, however, spindle discharge showed behavior similar to that shown in Fig. 4A, according to strip hardness.

A clear cessation of spindle discharge during the power phase of control cycles (e.g., as shown in Figs. 2 and 4A) was observed in 26 (60%) of the 43 units. These 26 units included 14 masseteric units and 12 nonmasseteric. No distinct relation was found between the receptive field and the presence or absence of a clear cessation of firing. The mean spindle discharge rate increased significantly in a hardness-dependent manner during the power phase (one-way ANOVA, P < 0.001; Fig. 5A). In addition, the mean firing rate during each phase was significantly greater in experimental cycles than in control cycles (Wilcoxon signed-rank test; P < 0.01; Fig. 5, A, B, and C). However, the mean firing rates during the jaw-opening and jaw-closing phases did not significantly change, according to strip hardness (Fig. 5, B and C).



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Fig. 5. Quantitative analysis of spindle responses, masseter EMG responses, and the minimum gape according to strip hardness. A: spindle responses during the power phase. B: spindle responses during the jaw-opening phase. C: spindle responses during the jaw-closing phase. D: Ma-IEMG responses. E: changes in masseter EMG duration. F: changes in minimum gape. Minimum gape was measured at the mentum, where a photodiode was attached, and was expressed as the moved vertical distance from the most jaw-closed position. Data are presented as means ± SE. *, P < 0.05; **, P < 0.01; ***, P < 0.001.

Changes in masseter activity and the minimum intermaxillary distance related to strip hardness

The masseteric IEMG activity and the mean duration of the masseteric EMG bursts increased significantly in a hardness-dependent manner (Kruskal-Wallis test, P < 0.001, Fig. 5D; one-way ANOVA, P < 0.001, Fig. 5E). The minimum gape was increased by insertion of a test strip and became wider significantly with increasing strip hardness (one-way ANOVA, P < 0.001; Fig. 5F). On the other hand, the horizontal component of chewing in experimental cycles did not change significantly with strip hardness.


    DISCUSSION
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ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES

Twenty-one (49%) of the spindle afferents examined were from the masseter muscle. Within the MesV of the cat, no difference has been found in the relative distribution of spindle afferent somata from the masseter, temporalis, and medial pterygoid muscles (Cody et al. 1972; Jerge 1963). During fictive mastication in the rabbit, central modulation (a phasic inhibition in most units) of afferent discharge has been recognized, and neurons showing modulated and unmodulated characteristics have been encountered at all levels of the MesV (Kolta et al. 1990). These findings suggest that there was little bias in the sampling of the units that were recorded from the MesV. The recording sites of the units were confirmed histologically. These units responded to the jaw opening, but did not respond to pressure applied to the teeth, gingiva, or vibrissae. Furthermore, the first-order neurons of Golgi tendon organs are located in gasserian ganglia rather than in the MesV (Lund et al. 1978). Accordingly, all units examined in the current study were thought to be muscle spindle units.

The receptive fields of the masseteric units of the present investigation were located in the anterior or middle part of the muscle, which accords well with anatomic findings (Bredman et al. 1991). The temporal muscle of a rabbit is divided into a small superficial portion and a much larger part originating from the posterior wall of the orbit (Weijs and Dantuma 1981). In the present study, we restricted palpation of the temporal muscle to the small superficial portion because of the difficulty in reaching the larger part. Three units were observed in the small portion. In the rabbit, the number of the spindles in the lateral pterygoid muscle, if any are present, is extremely small (Smith and Marcarian 1967). We believe therefore that the spindles of the remaining 19 units are in the deep portion of the temporal muscle or in the medial pterygoid muscle.

Behavior of muscle spindle afferents during CRJMs

The activity patterns of muscle spindle afferents were divided into two types, depending on the presence or absence of a clear cessation of discharge during the power phase before strip application. We cannot clarify what caused the different spindle discharge patterns, but possible explanations include the type of ending of the spindle afferent and the location and direction of the spindle. Because jaw muscle spindles cannot be classified reliably by their conduction velocity (Inoue et al. 1981), a distinction between the two types of afferents, primary and secondary, was not made in the present investigation. Moreover, it seemed inappropriate in the present study to use the more reliable way of classifying spindle afferents by using ramp-and-hold stretches and a depolarizing neuromuscular blocking agent (succinylcholine). This is because the agent may cause such an unfavorable condition that the output from motoneurons is not transferred to muscles in a physiological manner, thereby causing an unfavorable effect on the behavior of EMG activity according to strip hardness. Furthermore, it is uncertain whether the test with succinylcholine is valid for the rabbit. The test has been used exclusively on the cat. Consequently, which type of afferents contribute to the regulation of jaw-closing muscle activity remains uncertain at present. However, we believe that both primary and secondary afferents are involved in the regulation, because both types are activated by static fusimotor drive during the jaw-closing and power phases, and because both afferents project to trigeminal motoneurons monosynaptically (Appenteng et al. 1978; Dessem et al. 1997) and may also be involved in polysynaptic jaw muscle stretch reflexes (Dessem et al. 1997). The topographic distributions of the two types of afferents, however, are different (rat: Dessem et al. 1997; cat: Kishimoto et al. 1998), implying that the afferents play different functional roles.

The spindle afferent firing showed less regularity in CRJMs than in rhythmic jaw movements induced by palatal stimulation. Although the possibility remains that these different discharge patterns were caused by the dissimilar jaw movements induced, the firing patterns could also result from a difference in fusimotor activity. In support of this proposal, a very irregular discharge of the spindle afferents was noted during active movements, whereas spindle firing was more regular when the same movements were reproduced passively (Taylor et al. 1997). It seems therefore that the fusimotor drive is more active in CRJMs than in reflexively evoked rhythmic jaw movements.

A clear cessation of spindle discharge during the power phase was observed before strip application but was absent in most units after strip application. The discharge during shortening of the jaw-closing muscles could result from the static fusimotor drive that would prevent unloading of sensory endings (Taylor and Appenteng 1981). It has been proposed that the static fusimotor fibers are activated principally during muscle shortening to help keep both primary and secondary endings active and take up slack in the intrafusal fiber. In contrast, during the whole cycle of chewing, the dynamic fusimotor system acts tonically to set the incremental sensitivity of primary endings to stretch (Appenteng et al. 1980). In the present study the discharge increased coincidentally with the transition from fast closing (jaw-closing phase) to slow closing (power phase), which is in agreement with previous reports (Cody et al. 1975; Goodwin and Luschei 1975; Taylor and Cody 1974; Taylor and Davey 1968; Taylor et al. 1981). The discharge often persisted throughout the power phase, especially when a tougher strip was applied. During the power phase the spindle discharge increased with strip hardness, which seemed to parallel jaw-closing muscle activity. The increased spindle discharge during the power phase could effectively raise the excitability of trigeminal motoneurons (Chase and McGinty 1970) and thus is most likely involved in the facilitatory effects on jaw-closing muscle activity. The increased firing rate for a tougher strip is probably caused by a greater intermaxillary distance throughout the power phase (Morimoto et al. 1995a) and by an increased slowing of muscle shortening. Any loading that slowed the expected shortening would cause an increase in spindle afferent firing, which would reflexively compensate for the loading. In this manner, the patterned discharge of the static fusimotor drive may represent a temporal template of the intended movement (Taylor and Appenteng 1981). In this concept, the secondary spindle afferents would tend to display more firing, because the greater dynamic sensitivity of the b1b2c afferents (afferents with the predominant influences of the bagl, bag2 and chain intrafusal fibers; primary) would make it more difficult for the static fusimotor burst to prevent unloading than for the b2c afferents (afferents with the predominant influences of the bag2 and chain intrafusal fibers; probably secondary).

During the jaw-opening phase, excitatory inputs from spindle afferents are inhibited in trigeminal motoneurons by hyperpolarizing inputs from the pattern generator (Goldberg and Chandler 1981; Nakamura and Kubo 1978). However, the spindle firing during the jaw-opening phase could be concerned with the regulation of jaw-closing muscle activity. It has been noted by other investigators (Dessem et al. 1997; Donga and Dessem 1993) that jaw-muscle spindle afferents project directly to the cerebellum. These direct projections could provide reliable signals for the comparison of peripheral movements with centrally generated motor commands and thereby produce a long-latency spindle feedback that might contribute to matching the central commands with peripheral movements. For this function secondary spindle afferents may be particularly important (Perreault et al. 1995). The early facilitatory EMG response to strip chewing (Hidaka et al. 1997b), which was almost abolished by deafferentation of muscle spindle afferents (Komuro et al. 1997), may be produced by the increased firing rate during the jaw-opening phase.

During the jaw-closing phase, the discharge increased when any strip was applied. A perturbation in a strip-chewing cycle starts approximately at the end of the jaw-closing phase (Hidaka et al. 1997b). Gellman et al. (1985) have proposed that it is the climbing fiber system that signals unexpected events to a normal movement pattern. According to their study, a climbing fiber response is consistently elicited if an unexpected displacement or contact occurs. We propose that for the trigeminal system, a trigeminally evoked climbing fiber response may signal a perturbation (i.e., an event outside the programmed chewing pattern) during mastication, thereby triggering a corrective movement or modulating the cerebellar output to alter movement commands. The cerebellum may modulate masticatory rhythmic jaw movements by exerting its effects on the masticatory central rhythm generator as well as trigeminal motoneurons (Nakamura and Katakura 1995).

Hardness-dependent changes in EMGs of the masticatory muscles

Both periodontal sensory receptors and jaw muscle spindles are primarily responsible for the facilitatory effects on masseteric EMGs during mastication (Hidaka et al. 1997b; Morimoto et al. 1989). However, these sensory receptors have different physiological properties (Appenteng et al. 1982; Inoue et al. 1981) and different regulatory actions on masticatory force (Hidaka et al. 1997b). The facilitatory masseteric response, including the early EMG response before a loading on the teeth, almost remains even after deprivation of periodontal sensation by cutting the maxillary and inferior alveolar nerves to the teeth (Hidaka et al. 1997b), implying that spindle afferents contribute to the remaining facilitation of the masseteric EMG. Chase and McGinty (1970) electrically stimulated the MesV and recorded the resultant H-reflex of the masseter muscle. They noted that during CRJMs in the freely moving cat, the H-reflex was facilitated during jaw closure and inhibited during jaw opening. Nakamura et al. (1976) reported that in immobilized cats, tonic jaw depression increased the amplitude of cortically induced rhythmical masseteric nerve activity. It could be stated from these results that the increased spindle discharges, at least during the jaw-closing and power phases, could raise the excitability of motoneurons and lead to a facilitatory EMG response during CRJMs, according to the hardness of the material that was chewed.


    ACKNOWLEDGMENTS

This study was partly supported by Grants 10307045 and 10771010 from the Japanese Ministry of Education.


    FOOTNOTES

Address for reprint requests: O. Hidaka, Department of Oral Physiology, Osaka University, Faculty of Dentistry, 1-8 Yamadaoka, Suita, Osaka 565-0871 Japan.

The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

Received 21 December 1998; accepted in final form 2 August 1999.


    REFERENCES
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ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES

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