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J Dent Res 85(9):849-853, 2006
© 2006 International and American Associations for Dental Research

RESEARCH REPORT
Biological

Functional Adaptability of Jaw-muscle Spindles after Bite-raising

T. Yabushita1,2,*, J.L. Zeredo2, K. Fujita1,2, K. Toda2, and K. Soma1

1 Orthodontic Science, Department of Orofacial Development and Function, Division of Oral Health Sciences, Graduate School, Tokyo Medical and Dental University, 1-5-45 Yushima, Bunkyo-ku, Tokyo 113-8549, Japan; and
2 Division of Integrative Sensory Physiology, Department of Developmental and Reconstructive Medicine, Graduate School of Biomedical Sciences, Nagasaki University, Nagasaki 852-8588, Japan

* corresponding author, yabushita-t.orts{at}tmd.ac.jp


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS & METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
In a previous experiment, we found that masseter muscle spindles show functional plasticity after 5 to 15 days under increased occlusal vertical dimension (iOVD). In the present study, we hypothesized that spindle function would eventually recover if longer observation periods were allowed. Therefore, in this study we investigated changes in masseter muscle spindle function over periods of 1 day to 8 weeks. Masseter muscle-spindle responses to ramp-and-hold jaw stretches were recorded from the mesencephalic trigeminal nucleus in 35 barbiturate-anesthetized female Wistar rats. The rats were previously divided into Control and iOVD groups, and those in the iOVD group received a 2.0-mm composite resin build-up to the maxillary molars. In this condition, there were no statistically significant differences in masseter muscle spindle sensitivity between Control and iOVD in the six- and eight-week subgroups. Our results further indicate a high degree of adaptability in masseter muscle spindle function following changes in OVD.

KEY WORDS: masseter muscle • muscle spindle • occlusal vertical dimension • adaptation • rat


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS & METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Dentists have long been interested in the vertical changes caused by prosthodontic or orthodontic treatments (Hellsing, 1990). An intentional increase in facial height can be produced by raising the bite in removable and fixed prosthodontics (Dahlström and Haraldson, 1985; Mays, 2003), or by the orthodontic extrusion of posterior teeth when deep overbite and some Angle class III malocclusions are corrected. Therefore, a better understanding of post-treatment stability of increased occlusal vertical dimension in adult patients is important, because some adult patients would benefit from an increase in vertical occlusal height.

Muscle spindles play a role in maintaining the posture of the mandible (Brill and Tryde, 1974; Broekhuijsen and van Willigen, 1983). Under dynamic conditions, the input from the muscle spindles has been shown as important in stabilizing the position of the mandible during movements of the body (Lund and Olsson, 1983). Therefore, jaw-muscle spindles could be the receptors responsible for the perception and maintenance of the occlusal vertical dimension (OVD). In addition, jaw-muscle spindles play an important role in the control of jaw movements during normal masticatory function (Lund, 1991).

Although some studies suggest the OVD to be strictly controlled (Yagi et al., 2003), and that this control would be exerted, at least in part, by inputs from jaw-muscle spindles (Zhang et al., 2003), we have recently demonstrated that masseter muscle spindles already start to show some degree of functional plasticity 5 days after the establishment of an increased OVD (iOVD) condition (Yabushita et al., 2005); i.e., some parameters of muscle-spindle function, particularly those related to the receptor’s sensitivity, were affected by changes in OVD. In this study, we tested for the possibility of functional recovery in masseter muscle spindles following longer periods of observation after iOVD.


   MATERIALS & METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS & METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
The experimental procedures described here are in agreement with the Animal Care Standards of the Tokyo Medical and Dental University and Nagasaki University, and were carried out with the approval from their respective Animal Welfare Committees.

Animal Preparation
Thirty-five female Wistar albino rats (13 wks old) were used. Rats were randomly divided into Control (n = 10) and iOVD (n = 25) groups. All rats were lightly anesthetized with thiamylal sodium (Isozol®, Yoshitomi Pharmaceutical, Osaka, Japan; 60 mg/kg i.p.), and those in the iOVD group had the dimension between the maxillary and mandibular molars increased by 2.0 mm with a resin build-up to the maxillary molars. The occlusal surfaces of lower molars were coated with fluid resin to prevent reduction of molar height due to abrasive movement of the mandible. The animals were then returned to their cages and allowed to recover from anesthesia. Electrophysiological recordings were obtained 1 day, 2, 4, 6, and 8 wks later (n = 5, in each group). The body weights of rats in both the Control and iOVD groups were monitored during the entire experimental period, for assessment of general health status.

Stimulation and Recording
For electrophysiological recordings, the animals were again anesthetized with thiamylal sodium (80 mg/kg i.p.). We monitored the level of anesthesia by checking pupil size, flexion and corneal reflexes, and heart rate. Additional thiamylal sodium (5 mg/kg i.p.) was administered when a firm pinch applied between the toe pads resulted in increased respiration and heart rate. With their bodies in a prone position, the animals were placed in a stereotaxic apparatus (models SN-2 and SM-15M, Narishige Scientific Instruments, Tokyo, Japan). For masseter muscle stimulation, one extreme of the cotton thread was fixed to the mandibular symphysis and the other to an automatic pulling machine. The maximum jaw-opening distance was set at 7.0 mm (ramp duration of 4.5 sec and hold duration of 4.0 sec) (Yabushita et al., 2005).

To allow for the introduction of the recording electrode, the scalp was incised at the midline, and a small aperture about 3 mm wide was prepared in the skull with a stereotaxic microengine. Monopolar tungsten microelectrodes (250-µm-diameter shaft with 8° tapered tip, 5 M{Omega} of AC impedance; A-M Systems, Inc., Carlsborg, WA, USA) were used to record single-unit activities of the masseter muscle-spindle afferents. Recording electrodes were inserted into the caudal, triangular part of the mesencephalic trigeminal nucleus following stereotaxic coordinates as previously reported (Paxinos and Watson, 1998). This nucleus contains the cell bodies of two types of neurons, i.e., primary muscle-spindle afferents of ipsilateral jaw-closing muscles and mechanoreceptor afferents of ipsilateral maxillary and mandibular teeth (reviewed in Lund, 1991). The caudal part of the mesencephalic trigeminal nucleus holds 60% of the nucleus cells (Rakhawy et al., 1972). Afferent units responding to gentle surface pressure applied with a rod to different areas of the masseter, but not to pushing of the teeth with the mandible fixed, were identified as masseter muscle spindle afferents. Identification of muscle afferent was complemented by electrical stimulation of the masseter nerve. The masseter nerve was exposed in the infratemporal fossa by lateral reflection of the temporalis muscle. The unit responses evoked in the mesencephalic trigeminal nucleus followed high-frequency stimulation (> 200 Hz) (Ro and Capra, 1999). Spike signals were amplified by a differential amplifier (DAM-80, WPI, Sarasota, FL, USA; x1000 gain, 300 Hz and 3 KHz for low and high filters, respectively). The responses were averaged after three consecutive trials.

Spindle afferents were classified as primary and secondary based on the response to stretch stimulation (Edin and Vallbo, 1990). In our pilot study, after standardized ramp-and-hold stretches (7.0 mm amplitude at 3.0 mm/sec speed), two types of response were observed. One type, characteristic of primary endings, exhibited a high dynamic peak (the discharge frequency at the end of the ramp phase) (73 ± 3.7 Hz) and a pause in the discharge during the stretch release. The other type of response, characteristic of secondary endings, exhibited a lower dynamic peak value (38 ± 6.5 Hz) and a continuous discharge during the stretch release.

After each unit was recorded, the electrode position was marked (50 µA negative current for 10 sec), and at the end of the experiment, the rat’s brain was removed under deep anesthesia for histological sectioning (50-µm frozen sections, cresyl violet staining). The electrode positioning was checked histologically, based on the electrolytic markings and signs of electrode penetration (Fig. 1Go).


Figure 1
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  		Figure 1. Schematic representation of the trigeminal mesencephalic nucleus drawn from coronal sections of the brainstem over a template form (Paxinos and Watson, 1998), –9.1 mm posterior to the bregma. An asterisk indicates the recording site. 4V, fourth ventricle; IRt, intermediate reticular nucleus; LC, locus coeruleus; Me5, trigeminal mesencephalic nucleus; Pr5, principal sensory trigeminal nucleus; py, pyramidal tract; sp5, spinal trigeminal tract; ts, tectospinal tract.

 
Data Analysis
All data were captured by means of a CED 1401 interface (Cambridge Electronic Design, Cambridge, UK) and stored in a computer hard disc. The data were later analyzed off-line with the Spike2 software for Windows, Version 4.02a (Cambridge Electronic Design, Cambridge, UK).

For units showing an initial burst of response at the onset of stretch, we assessed the dynamic index to examine speed-sensitivity, and the static index to examine length-sensitivity. The dynamic index was calculated as the difference between the peak instantaneous frequency of the ramp-stretch and the frequency at 0.5 sec of the hold phase of stimulation (Crowe and Matthews, 1964). The static index was calculated as the average firing frequency in the interval of 0.5 to 1 sec during the hold phase of stimulation.

Statistical Analysis
Data from all groups and subgroups were compared with repeated-measures ANOVA, followed by Scheffé’s post hoc test (5% significance level). The software Statview for Windows, version 5.0 (SAS Institute, Cary, NC, USA), aided in statistical analysis.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS & METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
The mean body weight of rats in iOVD and Control groups increased continuously throughout the experimental period, without statistically significant differences in any of the groups or sub-groups.

Typical examples of masseter muscle spindle-afferent activity recorded from the mesencephalic trigeminal nucleus are shown in Fig. 2Go. One hundred and 32 units responded with a high dynamic peak followed by a pause in discharge during release from stretch, and were thus classified as primary endings. Analyses were performed with masseter muscle spindle-afferent activity by 3 consecutive ramp-and-hold stretches from each unit. In the iOVD group, 270 responses were recorded from 90 units (25 rats), while in the control, 126 responses were recorded from 42 units (10 rats). Electrical stimulation of the masseter nerve evoked unit responses in the mesencephalic trigeminal nucleus with a latency of 0.5 ± 0.05 ms (± SD). With the conduction distance from the site of stimulation to the recording electrode in the mesencephalic trigeminal nucleus estimated at 20 mm, the mean conduction velocity of the recorded afferents was 40.3 ± 3.9 m/s (± SD).


Figure 2
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  		Figure 2. Examples of responses from single masseter muscle spindle units to ramp-and-hold stretch. (A) Typical responses from (a) Control group, (b) two-week iOVD group, and (c) eight-week iOVD group. (B) Ramp-and-hold stretch was applied with maximum opening distance of 7.0 mm; stimulus duration was 8.5 sec, divided into 4.5 sec and 4.0 sec for ramp-stretch and hold phases, respectively.

 
In the Control group, there were no significant differences among the one-day, two-, four-, six-, and eight-week subgroups in dynamic index (Fig. 3AGo). Compared with the respective Control subgroups, the mean dynamic index was significantly lower only in the two-week iOVD, but not in the one-day, four, six-, or eight-week iOVD subgroup. At 2 wks of iOVD, the dynamic index values were also significantly lower than the initial values recorded at 1 day, but not at 4, 6, or 8 wks of iOVD (Fig. 3BGo).


Figure 3
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  		Figure 3. Dynamic index of normal and iOVD groups. (A) Control groups. (B) iOVD groups. A significantly lower dynamic index was observed after 2 wks of iOVD. Datapoints represent averaged data from 3 consecutive ramp-and-hold stretches in each unit. Error bars indicate SD; n means number of single afferent units; *P < 0.05 vs. one-day iOVD, and #P < 0.05 vs. the respective Control subgroup in repeated-measures ANOVA followed by Scheffé’s post hoc test. "n" refers to the number of units at each time period. Imp/s, impulses per sec.

 
Likewise, the static index did not change with time in the Control group. There were no statistically significant differences in the static index among the one-day, two-, four-, six-, and eight-week subgroups (Fig. 4AGo). However, the mean static index was significantly lower between the two- and four-week iOVD and their respective Control subgroups. After 6 wks, there were no statistically significant differences in either dynamic index or static index between Control and iOVD groups. Also at 6 and 8 wks of iOVD, the static index values were found to be similar to those initially recorded at 1 day of iOVD (Fig. 4BGo).


Figure 4
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  		Figure 4. Static index of normal and iOVD groups. (A) Control groups. (B) iOVD groups. A significantly lower static index was observed after 2 and 4 wks of iOVD. Datapoints represent averaged data from 3 consecutive ramp-and-hold stretches in each unit. Error bars indicate SD; n means number of single afferent units; *P < 0.05 vs. one-day iOVD, and #P < 0.05 vs. the respective Control subgroup in repeated-measures ANOVA, followed by Scheffé’s post hoc test. "n" refers to the number of units at each time period. Imp/s, impulses per sec.

 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS & METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
The jaw-closing muscles (masseter, temporalis, and medial pterygoid) are richly supplied with muscle spindles (Yoshimura et al., 1990). Muscle spindles are stimulated by increases in muscle length, which activate primary and secondary endings originating from the spindles. Jaw-muscle spindles are regarded as fundamental in determining mandibular position (McCloskey, 1978; Proske et al., 2000). In this study, we recorded muscle-spindle activities from the masseter muscle, one of the jaw muscles with a greater number of spindles (Lennartsson, 1980). In addition, we attempted to assess the effect of iOVD on speed sensitivity and length sensitivity (dynamic index and static index, respectively).

In the muscles throughout the body, primary endings are more predominant (Edin and Vallbo, 1990; Johansson et al., 1991; Ribot-Ciscar et al., 2000). Likewise, in the masseter muscle, primary endings were found to be nearly twice as frequent as secondary ones (Yabushita et al., 2005). The discharge of a primary ending indicates both muscular length changes (static sensitivity) and velocity of length changes (dynamic sensitivity), whereas the discharge of a secondary ending provides mainly information about length changes (McCloskey, 1978). In the present study, we needed information about the changes in speed- and length-sensitivity after long-term bite-raising; therefore, we chose to analyze further the responses of primary endings only.

In this study, the recording method was different from that used in our previous study (Yabushita et al., 2005). This time, we recorded muscle spindle afferents from the trigeminal mesencephalic nucleus, whereas we had previously recorded, from the masseteric nerve, the activity of muscle spindles that were de-efferented during recording. Therefore, with the recording method used in this study, the gamma motoneurons (Lund et al., 1979) remained intact. The sensitivity to both length and velocity can be altered by the CNS via activity in the fusimotor system, the static gamma system controlling length sensitivity, and the dynamic gamma system controlling velocity sensitivity (Hunt, 1990). Nevertheless, the results of this study were similar to those of our previous study in the change of spindle sensitivity. In both studies, the decrease of masseter muscle spindle-sensitivity up to 2 wks after establishment of an iOVD condition was significant. The changes in spindle function may be attributed to one or more of the following: (1) increased muscle stretch changing the responsiveness of the units per se, (2) stimulation of intra-oral (e.g., periodontal) afferent input by the occlusal resin build-up, or (3) changes in occlusal function producing changes in CNS masticatory controls.

We assessed the dynamic index to examine speed-sensitivity, and the static index to examine length-sensitivity. In the iOVD groups, the dynamic index returned to the original value (the value obtained at 1 day of iOVD) earlier than did the static index, suggesting that the adaptability of length-sensitivity could be higher than that of speed-sensitivity. However, both the dynamic index and the static index of masseter muscle spindles were able to recover to their original values in 4 to 6 wks of iOVD. Since the information from jaw-muscle spindles in general is also used in recognizing movement and position of the mandible, the recovery of jaw-muscle spindle sensitivity under long-term iOVD may indicate that these receptors are able to adapt to changes in occlusal vertical dimension, and, in turn, provide adaptability to the cognitive faculty of mandibular movement.

It has been repeatedly suggested that inputs from jaw muscle spindles would be involved in the physiological mechanism of OVD regulation (e.g., Yagi et al., 2003; Zhang et al., 2003). Thus, sensory feedback from the jaw muscle could be blamed for the instability and relapse of occlusal treatments. Nevertheless, in this study there was no significant difference between the properties of muscle-spindle sensitivity of normal rats and and those of long-term iOVD rats. This result suggests that masseter muscle spindles may ultimately adapt to iOVD, and thus supports the idea that, clinically, the relapse of occlusal treatments would not be dependent on peripheral receptors.


   ACKNOWLEDGMENTS
 
This study was financially supported by Grants-in-Aid for Scientific Research (14370688, 2002–2003) from the Ministry of Education, Culture, Sports, Science and Technology of Japan. Part of this study was presented at the 63rd Annual Meeting of the Japanese Orthodontic Society, Fukuoka City, November 17–19, 2004 [Yabushita T, Fujita K, Toda K, and Soma K (2004). An electrophysiological study on adaptability of jaw-closing muscle spindle after bite-raising].

Received December 8, 2004; Last revision April 6, 2006; Accepted May 24, 2006


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS & METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Brill N, Tryde G (1974). Physiology of mandibular positions. Front Oral Physiol 1:199–237.[Medline]

Broekhuijsen ML, van Willigen JD (1983). Factors influencing jaw position sense in man. Arch Oral Biol 28:387–391.[ISI][Medline]

Crowe A, Matthews PB (1964). The effects of stimulation of static and dynamic fusimotor fibers on the response of stretching of the primary endings of muscle spindles. J Physiol 174:109–131.[Free Full Text]

Dahlström L, Haraldson T (1985). Bite plates and stabilization splints in mandibular dysfunction. A clinical and electromyographic comparison. Acta Odontol Scand 43:109–114.[ISI][Medline]

Edin BB, Vallbo AB (1990). Dynamic response of human muscle spindle afferents to stretch. J Neurophysiol 63:1297–1306.[Abstract/Free Full Text]

Hellsing E (1990). Increased overbite and craniomandibular disorders—a clinical approach. Am J Orthod Dentofacial Orthop 98:516–522.[ISI][Medline]

Hunt CC (1990). Mammalian muscle spindle: peripheral mechanisms. Physiol Rev 70:643–663.[Abstract/Free Full Text]

Johansson H, Sjolander P, Sojka P (1991). Fusimotor reflex profiles of individual triceps surae primary muscle spindle afferents assessed with multi-afferent recording technique. J Physiol (Paris) 85:6–19.[Medline]

Lennartsson B (1980). Number and distribution of muscle spindles in the masticatory muscles of the rat. J Anat 130:279–288.[ISI][Medline]

Lund JP (1991). Mastication and its control by the brain stem. Crit Rev Oral Biol Med 2:33–64.[Abstract/Free Full Text]

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Lund JP, Smith AM, Sessle BJ, Murakami T (1979). Activity of trigeminal alpha- and gamma-motoneurons and muscle afferents during performance of a biting task. J Neurophysiol 42:710–725.[Free Full Text]

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McCloskey DI (1978). Kinesthetic sensibility. Physiol Rev 58:763–820.[Free Full Text]

Paxinos G, Watson C (1998). The rat brain in stereotaxic coordinates. 4th ed. New York: Academic Press.

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This Article
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Right arrow Articles by Yabushita, T.
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