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J Dent Res 84(3):245-249, 2005
© 2005 International and American Associations for Dental Research

RESEARCH REPORTS
Biological

Role of Occlusal Vertical Dimension in Spindle Function

T. Yabushita1,2,*, J.L. Zeredo2, 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; 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
 
Several studies have suggested the jaw-muscle spindle as the receptor responsible for regulating and maintaining the occlusal vertical dimension (OVD). However, to challenge this assumption, we hypothesized that long-term changes in OVD could affect the sensory inputs from jaw-muscle spindles. In this study, we investigated changes in masseter muscle spindle function under an increased OVD (iOVD) condition. Responses of primary and secondary endings of masseter muscle spindles to cyclic sinusoidal stretches were investigated. Twenty barbiturate-anesthetized female Wistar rats were divided into control and iOVD groups. Rats in the iOVD group received a 2.0-mm composite resin build-up to the maxillary molars. After iOVD, masseter muscle spindle sensitivity gradually decreased. Primary and secondary spindle endings were affected differently. We conclude that iOVD caused reduction in masseter muscle spindle sensitivity. This result suggests that peripheral sensory plasticity may occur following changes in OVD. Such changes may provide a basis for physiological adaptation to clinical occlusal adjustments.

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


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS & METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Changes in the occlusal vertical dimension (OVD) are often associated with certain syndromes, such as temporomandibular joint disorders (Christensen, 1970) and headache (Hellsing, 1990). The perturbation of a habituated OVD may have such a strong effect on the entire body that even symptoms of tinnitus and vertigo will appear (e.g., Costen, 1936). Nevertheless, bite-raising splints or plates that increase the OVD have been used to treat disorders involving muscular hyperactivity, as in bruxism (Dahlström and Haraldson, 1985). Therefore, the OVD may be critical for the maintenance of a physiological body condition.

Currently, it seems that the OVD is subject to rigorous proprioceptive control (Yagi et al., 2003). The control of jaw movements and jaw position, notoriously lacking visual cues, is performed by inputs from low-threshold mechanoreceptors scattered throughout the orofacial region. These include periodontal and mucosal mechanoreceptors, muscle spindles, Golgi tendon organs, and joint receptors (Lund, 1991; Trulsson and Johansson, 2002). Several reports indicate that jaw-muscle spindles, which are sensitive to muscle length and changes therein, would be responsible for the perception of jaw position and opening magnitude (Brill and Tryde, 1974; Zhang et al., 2003). Therefore, jaw-muscle spindles could be the receptors responsible for the perception and maintenance of the OVD.

The response of muscle spindles after short-term stretch conditioning has been studied from both the primary and secondary endings of soleus muscle spindles in anaesthetized cats (Proske et al., 1992). In contrast, there have been very few studies on the response of muscle spindles after long-term conditioning. Therefore, in this study, we investigated the effects of an increased OVD (iOVD) condition on the function of masseter muscle spindles over a period of 15 days, hypothesizing that long-term changes in OVD could affect the sensory inputs from jaw-muscle spindles.


   MATERIALS & METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS & METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Animal Preparation
Twenty female Wistar albino rats, weighing from 230 to 270 g, were used. Rats were divided into a control group and iOVD groups, which were further divided into 5, 10, and 15 days of iOVD (n = 5 in each group). Rats in the iOVD group were lightly anesthetized with thiamylal sodium (Isozol®, Yoshitomi Pharmaceutical, Osaka, Japan; 60 mg/kg i.p.) and had the distance between the maxillary and mandibular molars increased by 2.0 mm with a resin build-up to the maxillary molars. An increase of 2.0 mm is considered to be within the physiological limits of masticatory muscles in rats (Akagawa et al., 1983). 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 body weight of animals in both control and iOVD groups increased during the experimental period, with no significant differences between the groups.

Stimulation and Recording
In all experiments, the animals were anesthetized with thiamylal sodium (60 mg/kg i.p.). A supplemental injection of 5 mg/kg i.p. was given when necessary. We monitored the level of anesthesia by checking the animals’ pupil size, flexion and corneal reflexes, and heart rate. In iOVD animals, the lack of attritional wear on the resin build-up was confirmed before the electrophysiological recordings were undertaken. The animals were placed in left lateral decubitus with their heads fixed to a stereotaxic frame (models RA-4 and SR-50, Narishige Scientific Instruments, Tokyo, Japan). To stimulate the masseter muscle, we fixed one end of a piece of cotton thread to the animals’ lower incisors and the other end to an automatic pulling machine (modified from an artificial respirator, model SN-480-7, Shinano manufactory, Tokyo, Japan) and applied cyclic sinusoidal stretches (Fig. 1AGo). The maximum jaw-opening distance was set at 7.0 mm, with a cycle duration of 4.0 sec (jaw-opening and -closing time of 2.0 sec, followed by an interval of 2.0 sec). We performed at least 5 trials for stimulation in each unit. The jaw-opening and -closing period was divided into 3 phases (phases 1 to 3) for data analysis (Fig. 1BGo).



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  		Figure 1. Schematic drawing of the experimental setting. (A) Barbiturate-anesthetized rats had their heads fixed to a stereotaxic frame in the left lateral decubitus. The masseteric nerve was exposed, hooked to an electrode, and preserved in a pool of liquid paraffin. A thread was attached to the mandible, and the masseter muscle was passively stretched by pulling the jaw open. (B) Sinusoidal stretch stimulation was applied with a maximum opening distance of 7.0 mm and a cycle duration of 4.0 sec (jaw-opening and -closing time of 2.0 seconds, followed by an interval of 2.0 sec). For data analysis, the stimulation (jaw-opening/-closing period) was divided into 3 phases (phases 1 to 3).

 
Stretch responses of spindle endings were recorded from the fine filament of the masseteric nerve on the right side. We accessed the masseteric nerve after removing the temporalis muscle, then tied the nerve with a piece of cotton thread, cut at the central end from the tying point. The nerve bundle was then divided into several filaments. We used a silver hook electrode (diameter, 0.7 mm) to record functional single-unit responses. 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).

Spindle afferents were classified as primary and secondary, based on the responses to stretch stimulation (Edin and Vallbo, 1990b). An initial burst at the start of a stretch and silence during the release phase were considered as primary afferent signs. Secondary afferents were characterized by a continuous discharge during stretch and release.

After the electrophysiological recordings, the animals were killed with an intraperitoneal thiamylal sodium overdose. The experimental procedure was in agreement with the Animal Care Standards of the Tokyo Medical and Dental University and Nagasaki University, and had the approval of the respective Animal Welfare Committees.

Data Analysis
All data were captured by means of a CED 1401 interface (Cambridge Electronic Design, Cambridge, UK) and were 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).

Statistical Analysis
Data from the 4 groups (control, 5, 10, and 15 days of iOVD) were compared with 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
 
Typical examples of spindle responses from the masseteric nerve are shown in Fig. 2Go. Two types of responses were observed. Forty-three units responded with a high dynamic peak followed by a pause in discharge during stretch release; these were classified as primary endings (Fig. 2AGo). Twenty-seven units showing lower dynamic peak value and continuous discharges during stretch and release were classified as secondary endings (Fig. 2BGo). After 15 days of iOVD, both primary and secondary endings responded with clearly lower discharge frequencies (Fig. 2Go, lower tracings). A cycle histogram shows high hysteresis in primary endings (Fig. 2AGo) and low hysteresis in secondary endings. This trend applies to both control and iOVD groups (Fig. 2BGo).



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  		Figure 2. Typical examples of responses from single masseter muscle spindle units to cyclic sinusoidal stretching. Vertical lines indicate the start of a stretch stimulation (continuous) and the first spike of a spindle unit response (dashed). Muscle spindle units were classified as primary or secondary according to their response patterns. Primary endings (A) discharged during stretch and were silent during release, while secondary endings (B) responded with tonic discharges in proportion to the change of muscle length during the entire stimulation period. Lower tracings show typical primary and secondary unit responses after 15 days of iOVD. Cycle histograms show averaged unit responses over 5 consecutive cycles (bins of 100 ms).

 
Under iOVD, the peak instantaneous frequency of spindle discharge decreased in both primary and secondary endings, except for phase 3 in primary endings, where the overall values were very low (Fig. 3Go). Analyses were performed on the first 5 cycles recorded from each unit. In primary endings, 215 responses were recorded from 43 units (Fig. 3AGo), while in secondary endings, 135 responses were recorded from 27 secondary units (Fig. 3BGo). Compared with controls, significantly lower instantaneous frequencies were observed in secondary endings as early as after 5 days under iOVD. Primary endings experienced an abrupt decline in instantaneous frequency between 5 and 10 days of iOVD. There were no significant differences between control and 5 days of iOVD, or between 10 and 15 days of iOVD, in primary endings. Likewise, there were no statistically significant differences between iOVD groups in secondary endings.



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  		Figure 3. Peak instantaneous frequencies during each phase of stimulation. (A) Primary endings (n = 43). (B) Secondary endings (n = 27). Significantly lower instantaneous frequencies were observed after 5 and 10 days of iOVD in secondary and primary endings, respectively, except for phase 3 in primary endings. Data points represent data averaged from 5 consecutive cycles in each unit. Error bars indicate SD. *Statistical significance vs. control; ANOVA followed by Scheffé’s post hoc test (5% significance level).

 
Response thresholds increased gradually under iOVD (Fig. 4Go). Threshold values were determined by the amount of jaw opening observed at the first spike response (Fig. 2Go). For each unit, the value obtained in the first stimulating cycle was used. In both primary and secondary endings, significantly higher threshold values were observed between 5 days iOVD and control. Measurements were taken from the first stimulating cycle of each unit. Overall, the threshold values were higher in primary endings (Fig. 4AGo) than in secondary endings (Fig. 4BGo) for control and iOVD groups. There were no significant differences in threshold values among the 5-, 10-, and 15-day iOVD groups.



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  		Figure 4. Response thresholds in control and iOVD groups. (A) Primary endings (n = 43). (B) Secondary endings (n = 27). Response thresholds were analyzed by the amount of jaw opening required for the first spike to fire. Significantly higher threshold values were obtained after 5 days of iOVD in both primary and secondary endings. Error bars indicate SD. *Statistical significance vs. control; ANOVA followed by Scheffé’s post hoc test (5% significance level).

 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS & METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
The control of mandibular position and movement is complex and requires several proprioceptive inputs. In the literature, among the orofacial receptors, 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 discriminate between primary and secondary endings and to assess their responses to iOVD separately.

Our findings indicate that masseteric spindle sensitivity was reduced under iOVD. This finding is in agreement with those of others who used stretch conditioning. For instance, in humans, subjects conditioned for 10 min to a wide-open jaw position have more difficulty in determining the sizes of objects put into their mouths (Broekhuijsen and van Willigen, 1983). Reduced spindle sensitivity might have been the cause of increased mismatch of the standard. Likewise, in animal experiments, short-term (a few sec) stretch conditioning has been reported to decrease muscle spindle sensitivity (Proske et al., 1992).

Anatomical studies indicate that muscle spindles may be capable of remodeling and adaptation. In a recent report, the effects of changing the OVD on the structural and functional status of jaw-muscle spindles were investigated by means of immunohistochemistry (Santiwong et al., 2002). Remodeling of nerve terminals in muscle spindles was shown to take place soon after the loss of occlusion. It is possible that some degree of remodeling occurs under iOVD as well, which may have caused reduction in muscle spindle sensitivity. Other factors, such as temperature (Fischer and Schäfer, 1999) and external Ca2+ concentration (Fischer and Schäfer, 2000), have also been reported to affect muscle spindle sensitivity.

Muscle spindles possess 2 types of sensory endings: primary and secondary. In the muscles throughout the body, primary endings are more predominant (Edin and Vallbo, 1990a; Johansson et al., 1991; Ribot-Ciscar et al., 2000). Likewise, we also found a larger population of primary (n = 43) than secondary endings (n = 27) in the masseter muscle. Primary and secondary endings exhibit different responses to imposed ramp-and-hold stretch (Matthews, 1963; Cheney and Preston, 1976). The discharge of primary endings indicates both muscular length (static sensitivity) and velocity (dynamic sensitivity), whereas the discharge of secondary endings provides mainly information about muscular length (McCloskey, 1978). In this study, we observed reduction in stretch sensitivity earlier in secondary endings than in primary endings, suggesting that the former type may be more susceptible to changes in an iOVD condition.

The responses of the primary and secondary endings to stretch differ. Secondary afferents are characterized by a continuous discharge in proportion to the change of muscle length during stretch and release, while primary afferents discharge during stretch and are silent during release (Edin and Vallbo, 1990b). Therefore, responses of primary endings to sinusoidal stretch showed high hysteresis, whereas secondary endings showed low hysteresis.

Clinically, many situations can be foreseen where patients would benefit from an increase in the OVD, such as in the orthodontic treatment of mild Class III and deep anterior overbite cases, or in the prosthetic rehabilitation of worn dentitions. In this study, the OVD increase represented 30% of the maximum jaw opening in rats, which is supposed to be about the same ratio as the physiological rest position reported for humans (Manns et al., 1981). A similar treatment in humans was found to adapt satisfactorily and remained constant over a two-year observation period (Ormianer and Gross, 1998). Therefore, our results support the view that the adaptational changes in the musculoskeletal complex may allow for alterations in the OVD (Carlsson et al., 1979; Carlson and Schneiderman, 1983; Dahl and Krogstad, 1985; Ahn and Schneider, 2000).

We conclude that iOVD gradually affected the sensitivity of masseteric muscle spindles over time, suggesting that some degree of peripheral sensory plasticity may occur following changes in OVD. Since inputs from muscle spindles in general are also used in learning processes, the reduced sensitivity from jaw-muscle spindles may provide substrate for the CNS to adapt to long-term changes in OVD.


   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 26th Annual Meeting of the Japan Neuroscience Society, Nagoya, Japan, July 23–25, 2003 [ Yabushita T et al.(2003). Altered occlusal vertical dimension changes the sensitivity of jaw-muscle spindle afferents. Neurosci Res (in press)].

Received November 26, 2003; Last revision October 14, 2004; Accepted November 3, 2004


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 MATERIALS & METHODS
 RESULTS
 DISCUSSION
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T. Yabushita, J.L. Zeredo, K. Fujita, K. Toda, and K. Soma
Functional Adaptability of Jaw-muscle Spindles after Bite-raising
J. Dent. Res., September 1, 2006; 85(9): 849 - 853.
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