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J Dent Res 82(7): 565-569, 2003
© 2003 International and American Associations for Dental Research

RESEARCH REPORT
Biological

An Involvement of Trigeminal Mesencephalic Neurons in Regulation of Occlusal Vertical Dimension in the Guinea Pig

W. Zhang1,2, M. Kobayashi1,*, M. Moritani3, Y. Masuda1, J. Dong4, T. Yagi5, T. Maeda6, and T. Morimoto1,7

1 Department of Oral Physiology,
2 Department of Fixed Prothodontics,
3 Department of Oral Anatomy,
4 Department of Removal Prothodontics,
5 Department of Orthodontics, and
6 Department of Oral Radiology, Osaka University Graduate School of Dentistry, 1-8, Yamadaoka, Suita, Osaka 565-0871, Japan;
7 Department of Oral Physiology, Comprehensive Dental Research Laboratory, Matsumoto Dental University, Shiojiri, Nagano 399-0781, Japan;

*corresponding author, masayuki{at}dent.osaka-u.ac.jp


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS & METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Although the occlusal vertical dimension (OVD) is strictly controlled, the neuronal mechanism of its regulation is still unclear. We hypothesize that neurons in the trigeminal mesencephalic nucleus (MesV) play an important role in the regulation of the OVD, because the MesV receives the projection from jaw-closing muscle spindles and periodontal mechanoreceptors. We measured the temporal OVD change in the guinea pig to study the effects of MesV lesions on the OVD. OVD-raised animals without MesV lesions showed a rapid OVD decrease to the same level as that in naïve controls, followed by an OVD increase after the OVD-raising appliance was removed. In contrast, OVD-raised animals with MesV lesions showed only a slight decrease in the OVD for 15 days after removal of the appliance, and then the OVD increased. The time-course of OVD development in normal-bite animals with MesV lesions was similar to that of naïve controls. These results suggest that MesV neurons are involved in OVD regulation.

KEY WORDS: muscle spindle • periodontal receptor • vertical dimension • trigeminal mesencephalic nucleus • deafferentation


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS & METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Occlusal vertical dimension (OVD), the distance between the mandible and maxilla, is considered to be the main factor in the determination of an individual’s ability to perform oral functions such as mastication, speaking, and swallowing effectively. Christensen (1970) reported that excessively raised OVD causes headache, bruxism, and pains in the masticatory muscles and temporomandibular joint. Indeed several studies using animals have produced supportive evidence demonstrating that an excessively increased OVD induces morphological and physiological changes, such as deformation in the mandible, changes in muscular attachments (McNamara, 1973; Carlson and Schneiderman, 1983), and changes in masticatory muscle fiber composition (Ohnuki et al., 1999). Recently, we have studied the temporal change of the OVD in bite-raised guinea pigs, and have found that within 5 days after the removal of the appliance, the OVD in these animals has decreased to the same level as that of naïve controls (Yagi et al., 2003). This result indicates that the animals are provided with a certain mechanism for regulating the OVD. However, the physiological mechanism of this regulation is still unclear.

MesV neurons receive projections from muscle spindles in the jaw-closing muscles and periodontal mechanoreceptors (Nozaki et al., 1985; Byers et al., 1986), and play an important role in the control of masticatory force (Hidaka et al., 1997, 1999). Therefore, MesV neurons may be involved in the regulation of the OVD. To elucidate the role of MesV neurons in OVD regulation, we studied the temporal change of the OVD in guinea pigs to determine the effect of the MesV lesion on the OVD.


   MATERIALS & METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS & METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Experimental procedures were approved by the Committee on Animal Research of Osaka University Graduate School of Dentistry.

Animals
We used 47 young male Hartley guinea pigs (4-6 post-natal wks old) that were divided into 4 groups: naïve controls, OVD-raised animals without MesV lesions (bite-raised controls), OVD-raised animals with MesV lesions (bite-raised MesV-lesioned animals), and MesV-lesioned animals without OVD-raising (MesV-lesioned controls).

Measurement of the OVD
The protocols for raising and measuring the OVD were described in our previous study (Yagi et al., 2003). A bite-raising appliance was fixed to the lower incisor with bonding resin under ketamine anesthesia (110 mg/kg, i.m.) after chlorpromazine (12.5 mg/kg, i.p.) application. Continuous eruption of the molars filled the space between the upper and lower molars for 7-10 days after the appliance attachment (Holmstedt et al., 1977). The appliance was removed 10 days after bonding.

Lateral radiographic cephalograms were taken by means of a soft x-ray system under ketamine anesthesia (Fig. 1AGo). The radiographs were digitized and fed into a computer via a scanner, and analyzed with image-processing programs. Landmarks on the trace of the cephalometric radiograph, So, E, A, Po, Pg, Gn, U1, Mu, Ml, V, and T, were determined as follows (Fig. 1BGo): So, the intersection between the posterior border of the basisphenoid and tympanic bulla; E, the intersection between the frontal bone and the most superior-anterior point of the posterior limit of the ethmoid bone; A, the most anterior point on the nasal bone; Po, the most posterior point on the cranial vault; Pg, a point on the most inferior contour of the lower border of the mandible, adjacent to the incisor; Gn, a point on the most inferior contour of the angular process of the mandible; U1, a point on the most anterior edge of the upper first molar; Mu, a point on the intersection between the maxillary bone and the mesial surface of the upper first molar; Ml, a point on the intersection between the mandibular alveolar bone and the mesial surface of the upper first molar; V, the intersection between the E-A line and the perpendicular to the E-A line through U1; and T, the intersection between the Pg-Gn line and the U1-V line. The distance of V-T was taken as the OVD in the present study, while the distances of A-Po and Mu-Ml were measured as the skeletal and crown lengths, respectively.




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  		Figure 1. Cephalometric radiograph (A) and landmarks on the trace of it (B).

 
Lesion in the MesV
Five to seven days after the appliance attachment, the animals were placed in a stereotaxic frame under ketamine anesthesia. An isotonic-transducer (TD-111T, Nihon Kohden, Tokyo, Japan) was fixed to the lower incisor with dental cement to monitor vertical jaw movements. A glass-coated elgiloy electrode with impedance of 1-3 M{omega} at 1 kHz was stereotaxically inserted into the MesV. MesV neurons were identified by single-unit or multi-unit activities responding to passive jaw opening and palpation of the masseter muscle (Fig. 2Go). The neuronal responses and vertical jaw movements were stored at 10 kHz and analyzed (Spike2, Cambridge Electronic Design, Cambridge, UK). The MesV was systematically searched at 250-µm steps in the mediolateral and rostrocaudal directions throughout the nucleus. Then, the MesV was coagulated by 40-µA DC current injection through the electrode for 40 sec. After making lesions in the MesV, we detached the isotonic-transducer, sutured the wound, and let the animals recover.



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  		Figure 2. An example of an extracellular unit recording from a MesV neuron. (A) The neuronal responses to ramp stretch. The uppermost and second traces indicate the single-unit activity and firing rate, respectively. The bottom trace shows the vertical jaw movement. (B) The neuronal responses to palpation to the masseter muscle. The MesV neuron responds to gentle palpations to the masseter muscle (bars on the top trace).

 
Histology
After the experiments, the animals were perfused with 0.1 M phosphate buffer followed by 10% formaldehyde under deep anesthesia with pentobarbital. The brainstem was transversely sectioned (50 µm thickness) and stained with cresyl-violet. Histological quantification was performed with use of a microscope (BX40, Olympus Optical, Tokyo, Japan) equipped with Lucivid and Neurolucida (MicroBrightField, Williston, VT, USA). To reconstruct the MesV, we outlined the brainstem using a 4X objective, and mapped MesV neurons with nuclei using a 40X objective.

Data Analysis
Statistical comparisons were performed with an unpaired t test or a one-way ANOVA with the HSD method of Scheffé’s test. The level of P < 0.05 was taken as significant. All statistical values are presented as means ± SEM.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS & METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Identification of MesV Neurons
MesV neurons were identified by ramp-and-hold stretch of the mandible (Fig. 2AGo). Some MesV neurons were also activated by a gentle palpation of a small region (1.5 mm diameter) of the masseter muscle (Fig. 2BGo), suggesting that the neurons extend into the muscle spindles in the masseter muscle. To check the coagulated regions in the brainstem, we reconstructed the MesV (Figs. 3A, 3BGoGo). Examples of Nissl-stained sections in a naïve control and MesV-lesioned animal are shown in Figs. 3C and 3DGoGo, respectively. The lesioned sites were distributed throughout the brainstem (Fig. 3EGo). The numbers of MesV neurons in a hemisphere in naïve controls and bite-raised MesV-lesioned animals were 1169 ± 63 (N = 6) and 336 ± 73 (N = 7), respectively (Fig. 3FGo).




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  		Figure 3. Distribution and numbers of MesV neurons. (A,B) Examples of localization of MesV neurons in naïve control (A) and MesV-lesioned animals (B). Each dot indicates location of a MesV neuron. (C,D) Nissl-stained sections obtained from naïve control (C) and MesV-lesioned animals (D). (E) Distribution of cell bodies of MesV neurons in 6 naïve controls (open columns) and 7 MesV-lesioned animals (filled columns). Bars on the symbols indicate SEM. Note that about 70% of neurons are coagulated throughout the MesV. (F) The numbers of MesV neurons in naïve controls (N = 6) and MesV-lesioned animals (N = 7). The horizontal bars show the mean of each group.

 
Post-operative Change in the OVD
We fixed the bite appliance to the lower incisor to raise the OVD, and removed it 10 days after fixation. The increase in the OVD was 3.3 ± 0.1 mm (11.4 ± 0.6%, N = 12) in bite-raised controls and 3.6 ± 0.3 mm (12.5 ± 1.1%, N = 11) in bite-raised MesV-lesioned animals on the day of appliance removal.

As previously reported (Yagi et al., 2003), the OVD continuously decreased for 6 days after the appliance was removed in bite-raised controls until it reached the OVD in naïve controls (Fig. 4AGo). The OVD then increased at rate similar to that in the naïve controls. The change in the antero-posterior length of the cranium in bite-raised controls was almost similar to that of naïve controls (Fig. 4BGo). The time-course of change in the crown length in bite-raised controls was almost similar to that of the OVD (Fig. 4CGo).



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  		Figure 4. Temporal changes in the OVD, skeletal, and crown length in naïve controls, bite-raised controls, and bite-raised MesV-lesioned animals. (A) Temporal changes in the OVD measured as the length between V and T. (B) Developmental changes of the anteroposterior length of the cranium measured as the length between A and Po. (C) Temporal changes in the crown length measured as the length between Mu and Ml. The arrows indicate the day of removal of the appliance. *P < 0.05 compared with naïve controls. **P < 0.01 compared with naïve controls. +P < 0.05 compared with bite-raised controls. ++P < 0.01 compared with bite-raised controls. Bars on the symbols indicate SEM, and values on symbols in (A) indicate the number of animals.

 
In contrast, bite-raised MesV-lesioned animals revealed only a slight decrease of the OVD after removal of the appliance. In these animals, the minimum value of the OVD, which was taken 15 days after the appliance was removed, was significantly larger than that of naïve controls and bite-raised controls (P < 0.05). The OVD in bite-raised MesV-lesioned animals then increased at a rate similar to that of naïve controls. The crown length in bite-raised MesV-lesioned animals decreased to the same level as the OVD in naïve controls, and then increased at a rate similar to that of naïve controls. The antero-posterior length in bite-raised MesV-lesioned animals was slightly larger than that of naïve and bite-raised controls at > 20 days after the appliance was removed (Fig. 4BGo). The rate of change in the OVD in normal-bite MesV-lesioned animals was almost the same as that of naïve controls (N = 5, Appendix Fig., www.dentalresearch.org).


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS & METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
Effects of MesV Lesions on the OVD
The main finding of the study is that bite-raised MesV-lesioned animals show only a slight decrease in OVD in contrast to a rapid recovery of the OVD in bite-raised controls. This finding suggests that MesV neurons contribute to the regulation of the OVD. Although MesV neurons mainly transmit sensory information either from muscle spindles or periodontal mechanoreceptors, the present results may be ascribed to loss of muscle spindle sensation. This is because the edentulous subjects that have lost periodontal sensation can detect the comfortable OVD level (Abekura et al., 1996; Nakai et al., 1998). However, two questions arise: (1) Why does the OVD in bite-raised MesV-lesioned animals temporarily decrease? and (2) Why does the OVD in MesV-lesioned controls increase at a rate similar to that of naïve controls? There are at least two possible explanations. First, sensory neurons in the trigeminal ganglion, such as mechanoreceptor neurons innervating the temporomandibular joint or periodontal ligament (Romfh et al., 1979), could partially compensate MesV neurons for sensing the OVD. Second, the surviving MesV neurons of muscle spindle afferents could partly transmit sensation to the OVD. These compensatory mechanisms may not work well under a bite-raised condition, since the continuous stimulus to these receptors by bite-raising may cause their adaptation.

Functional Implication
MesV neurons are included in the loop of the jaw-jerk reflex, which effectively regulates jaw-closing muscle activity during mastication (Morimoto et al., 1989). MesV neurons may also contribute to the feed-forward regulation of the masticatory muscle activity during fictive mastication in the rabbit (Komuro et al., 2001). In addition to these short-term physiological roles for the oral functions, the present study suggests a long-term role of MesV neurons: adjustment of the OVD. Bite-raised MesV-lesioned animals showed larger OVD and antero-posterior length with normal crown length ≥ 20 days after the appliance was removed. This finding suggests that the larger OVD may be caused by a skeletal change. In other words, the excessive large OVD with MesV-lesions could affect skeletal growth during development. This hypothesis is supported by the finding that bite-raising causes vertical displacement of the pre-maxilla and maxilla in the superior direction in the miniature pig (Ferrari and Herring, 1995).


   ACKNOWLEDGMENTS
 
We thank Dr. Youngnam Kang for critical reading of the manuscript, and Drs. Atsushi Yoshida and Takashi Nokubi for encouraging the study. This study was supported by grants from the Japan Society for the Promotion of Science (Grants-in-Aid for Science Research Nos. 11357017 and 13307056).


   FOOTNOTES
 
A supplemental appendix to this article is published electronically only at http://www.dentalresearch.org.

Received January 3, 2003; Last revision March 31, 2003; Accepted April 4, 2003


   REFERENCES
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 ABSTRACT
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 MATERIALS & METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Abekura H, Tokuyama H, Hamada T, Morimoto T (1996). Comfortable zone of the mandible evaluated by the constant stimuli method. J Oral Rehabil 23:330–335.[ISI][Medline]

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Carlson DS, Schneiderman ED (1983). Cephalometric analysis of adaptations after lengthening of the masseter muscle in adult rhesus monkeys, Macaca mulatta. Arch Oral Biol 28:627–637.[ISI][Medline]

Christensen J (1970). Effect of occlusion-raising procedures on the chewing system. Dent Pract Dent Rec 20:233–238.[Medline]

Ferrari CS, Herring SW (1995). Use of a bite-opening appliance in the miniature pig: modification of craniofacial growth. Acta Anat 154:205–215.[ISI][Medline]

Hidaka O, Morimoto T, Masuda Y, Kato T, Matsuo R, Inoue T, et al. (1997). Regulation of masticatory force during cortically induced rhythmic jaw movements in the anesthetized rabbit. J Neurophysiol 77:3168–3179.[Abstract/Free Full Text]

Hidaka O, Morimoto T, Kato T, Masuda Y, Inoue T, Takada K (1999). Behavior of jaw muscle spindle afferents during cortically induced rhythmic jaw movements in the anesthetized rabbit. J Neurophysiol 82:2633–2640.[Abstract/Free Full Text]

Holmstedt JO, McClugage SG Jr, Clark JS, Guevara MJ (1977). Osteodentin formation in continuously erupting teeth of guinea pigs. J Dent Res 56:1569–1576.[Abstract/Free Full Text]

Komuro A, Morimoto T, Iwata K, Inoue T, Kato T, Masuda Y, et al. (2001). Putative feed-forward control of jaw-closing muscle activity during rhythmic jaw movements in the anesthetized rabbit. J Neurophysiol 86:2834–2844.[Abstract/Free Full Text]

McNamara JA Jr (1973). Neuromuscular and skeletal adaptations to altered function in the orofacial region. Am J Orthod 64:578–606.[ISI][Medline]

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Nakai N, Abekura H, Hamada T, Morimoto T (1998). Comparison of the most comfortable mandibular position with the intercuspal position using cephalometric analysis. J Oral Rehabil 25:370–375.[ISI][Medline]

Nozaki S, Iriki A, Nakamura Y (1985). Trigeminal mesencephalic neurons innervating functionally identified muscle spindles and involved in the monosynaptic stretch reflex of the lateral pterygoid muscle of the guinea pig. J Comp Neurol 236:106–120.[ISI][Medline]

Ohnuki Y, Saeki Y, Yamane A, Kawasaki K, Yanagisawa K (1999). Adaptation of guinea-pig superficial masseter muscle to an increase in occlusal vertical dimension. Arch Oral Biol 44:329–335.[ISI][Medline]

Romfh JH, Capra NF, Gatipon GB (1979). Trigeminal nerve and temporomandibular joint of the cat: a horseradish peroxidase study. Exp Neurol 65:99–106.[ISI][Medline]

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