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Neck Motor Unit Activities Induced by Inputs from Periodontal Mechanoreceptors in Rats

¹ Orthodontic Science, Department of Orofacial Development and Function, Division of Oral Health Science and
² Section of Cognitive Neurobiology, Department of Maxillofacial Biology, Graduate School, Tokyo Medical and Dental University, 1-5-45 Yushima, Bunkyo-ku, Tokyo 113-8549, Japan; and
³ Department of Physiology, Nagasaki University School of Dentistry, Nagasaki 852-8588, Japan;

*corresponding author, jorge.orts{at}tmd.ac.jp

	ABSTRACT

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Clinical evidence suggests that head movements may be coupled with oro-facial functions, which are predominantly controlled by somatosensory inputs from the oro-facial area. However, the effects of specific modalities of sensory inputs on the neck muscles' motor activity are still unclear. In the present study, natural pressure stimulation was applied to the rat's upper first molars, while motor unit electromyographic activity was recorded from the dorsal neck splenius muscle. During the hold phase of pressure stimulation, clear tonic discharges were elicited in the splenius muscles on both sides. Mean threshold values were 622.3 mN (± 19.6 SEM, n = 39) and 496.8 mN (± 26.4 SEM, n = 43) for ipsi- and contralateral sides, respectively (p < 0.001, Mann-Whitney U test). Analysis of our data suggests that periodontal inputs may play an important role in controlling the motor activity of neck muscles, in addition to its well-known coordination of the masticatory function.

KEY WORDS: mechanoreceptors • periodontium • electromyography • neck muscles • rat

	INTRODUCTION

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Recent observations strongly suggest the functional coupling of the stomatognathic system with neck muscle activities. Clinical studies show that jaw and neck muscles can actually work together in a relatively stereotypical fashion during rhythmic movements (Yamabe et al., 1999; Eriksson et al., 2000). Moreover, patients suffering from occlusal or temporomandibular joint disorders frequently report dysfunction and pain in neck muscles (Emshoff and Bertram, 1998; Karppinen et al., 1999). These studies suggest that oro-facial sensory information can modify the neck muscles' activity, especially the periodontal input, which is thought to be an important neural substrate for the coordination of masticatory function (Trulsson and Johansson, 1996).

On the other hand, head postures affect mandibular movements (Goldstein et al., 1984; McKay and Christensen, 1999), mandibular resting position (Darling et al., 1984; Ferrario et al., 1997), and even the bite force (Hellsing and Hagberg, 1990). Assuming that sensory information from the periodontal ligament plays an important role in physiological mastication, we hypothesized that it may also have an influence on head posture.

Most of the studies that dealt with the effects of trigeminal afferents on the neck motor system used electrical trigeminal nerve stimulation in cats, and trigemino-cervical reflexes were reported (Abrahams and Richmond, 1977; Sumino and Nozaki, 1977; Alstermark et al., 1992; Abrahams et al., 1993). However, it is still unknown which receptors or what kinds of somatosensory inputs could possibly be concerned with these reflexes. Therefore, we studied the effects of periodontal sensory inputs on the splenius muscle, one of the deep dorsal neck muscles that regulate head posture.

	MATERIALS & METHODS

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Animal Preparation
Twelve male Wistar albino rats, each weighing from 250 to 420 g, were used. In all experiments, the rats were lightly anesthetized with thiamylal sodium (Isozol^®, Yoshitomi Pharmaceutical, Osaka, Japan; 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 pupil size, flexion and corneal reflexes, and heart rate. Tracheotomy was performed to establish artificial ventilation (60 strokes/min), and the animals were placed in a prone position with their heads fixed to a stereotaxic frame specially designed for the rat (models RA-4 and EB-4, Narishige Scientific Instruments, Tokyo, Japan). The frame was then adjusted in a perfect horizontal plane. Tight fixation of the head was important to avoid postural reflexes elicited by receptors in the neck joints or vestibular system.

After the experiments, the animals were killed with a thiamylal sodium overdose. The experimental procedure was in agreement with the Animal Care Standards of the Tokyo Medical and Dental University, and had the approval of the Animal Welfare Committee.

Stimulation and Recording
We used the following setting specifically to stimulate the periodontal mechanoreceptors. An orthodontic accessory (the "lingual button") was bonded to the occlusal surfaces of both maxillary first molars. The accessory was then connected with a cotton thread to a force transducer and its amplifier (Transbridge, WPI, Sarasota, FL, USA). Ramp-and-hold pressure stimulation was applied by manual pulling of the force transducer. The stimulation used in the present study was always in a postero-anterior direction, with ramp speed of about 300 mN/s, hold time of 3 to 6 sec, and maximum intensities never higher than 882 mN.

Motor unit activities were recorded from the splenius muscles on both sides. The splenius muscle was chosen from the group of dorsal neck muscles because it is reported to be involved in various head movements, including extension, lateral tilting, and rotation, and is responsible for anti-gravitational support of head posture (Pfister and Zenker, 1984). In addition, it is also easily accessible for surgery and electrode placement.

Bipolar stainless steel wires (type E-2, Narishige Scientific Instruments, Tokyo, Japan) of 1 mm interpolar distance, enamel-coated except for the tips, and 100 µm in diameter were used as recording electrodes. Spike signals were amplified by a differential amplifier (DAM-80, WPI, Sarasota, FL; x1000 gain, 300 Hz and 3 KHz for low and high filters, respectively).

Pressure stimulation was applied in a ramp-and-hold fashion. Stimulus intensity was increased rapidly until the first spikes fired, and was then kept slightly above this level for a few seconds. The stimulus intensity that evoked the first spike was measured, and threshold values were obtained. During the hold-phase of stimulation, peak instantaneous spike frequencies were measured for the assessment of response properties.

All data were captured and analyzed in a computer with a CED 1401 interface and the Spike2 software for Windows, version 2.19 (Cambridge Electronic Design, Cambridge, UK).

Statistical Analysis
The Mann-Whitney U test was used for statistical comparison of data from the ipsi- and contralateral sides; statistical significance was considered as p < 0.05. Reflex activities of the three groups of stimulations in both sides were compared by the ANOVA post hoc test (Fisher's PLSD, 5% significance level). The software Statview for Windows, version 5.0 (SAS Institute, Cary, NC, USA), aided in statistical analysis.

	RESULTS

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Unilateral pressure stimulation elicited tonic discharges in the splenius muscles on both sides. A typical example is shown in Fig. 1. In this instance, the threshold intensity (indicated by horizontal arrows) was 435.7 mN for the ipsi- (Fig. 1A) and 410.4 mN for the contralateral side (Fig. 1B). Peak instantaneous spike frequencies were 28 Hz and 36 Hz for the ipsi- and contralateral sides, respectively.

View larger version (21K): [in this window] [in a new window]   Figure 1. A typical reflex response from the splenius muscle. Tonic discharges are observed under steady, moderate-intensity, unilateral pressure stimulation of the periodontal mechanoreceptors. Motor unit activity under (A) ipsi- and (B) contralateral periodontal stimulation. The threshold was 435.7 mN for the ipsi- and 410.4 mN for the contralateral side (indicated by horizontal arrows). Peak instant spike frequencies were 28 Hz and 36 Hz for the ipsi- and contralateral sides, respectively.

View larger version (12K): [in this window] [in a new window]   Figure 2. Differences between threshold values for ipsi- and contralateral sides (± SEM). Data from 16 motor units combined, ipsilateral n = 39 trials, contralateral n = 43 trials. Threshold value was determined during the ramp-phase of stimulation when the first spike was obtained. **p < 0.001 in the Mann-Whitney U test.

View larger version (17K): [in this window] [in a new window]   Figure 3. Mean spike frequencies for 3 different levels of stimulation, ipsi- and contralateral sides (± SEM). One hundred thirty-two responses were recorded from 16 motor units. Ipsilateral side — weak n = 15, moderate n = 27, strong n = 20; contralateral side — weak n = 27, moderate n = 23, strong n = 20. *Statistical significance, ANOVA post hoc test (Fisher PLSD, 5% significance level).

To guarantee that these responses were evoked by periodontal stimulation, we administered local anesthesia with 2% lidocaine (Xylocaine^®, Astra Pharmaceuticals, Osaka, Japan, 50 µL, supraperiosteal injection) to the upper molar region in 2 rats. Reflex responses completely disappeared 3 min after the infusion of local anesthetics.

	DISCUSSION

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The coordination between jaw and head movements has been reported extensively. There are several situations in which this coordination could be assessed, such as in speech, respiration, or gaze. A major difficulty in assessing the problem is that oral function is very diversified. For each oral task, a vast amount of somatosensory information is brought up from receptors in facial and oral structures. In our study, we chose to stimulate the periodontal mechanoreceptor selectively, not only because it is one of the most important receptors in the intra-oral region, but also due to its crucial role in the feedback/feedforward control of masticatory muscles (for a review, see Jacobs and van Steenberghe, 1994; Trulsson and Johansson, 1996). It also seems that the loss of periodontal mechanoreceptors cannot be sufficiently compensated for by other oral receptors (Trulsson and Gunne, 1998; Veyrune and Mioche, 2000).

Anatomic evidence indicates putative connections between trigeminal afferents and cervical motoneurons. Retrograde labeling studies have shown that the oral and interpolar subdivisions of the spinal trigeminal nucleus project to the spinal cord (Kerr, 1972; Matsushita et al., 1981; Phelan and Falls, 1991a,b). Trigeminal descending fibers were found throughout the spinal cord, bilaterally in its ventral and dorsal horns (Ruggiero et al., 1981; Chang et al., 1988).

From a physiologic point of view, a trigemino-neck reflex has been described, when neck motoneurons received strong, long latency phasic excitation from trigeminal afferent nerves (Abrahams and Richmond, 1977; Sumino and Nozaki, 1977). A later study used direct electrical stimulation of the trigeminal ganglion. The authors reported a short latency, presumably disynaptic transmission through trigeminal neurons from the ipsilateral and contralateral oral subnucleus into the splenius motoneurons (Alstermark et al., 1992). These findings suggest that the pathway for neck motor unit activation by trigeminal inputs is through the trigeminal ganglion and spinal trigeminal nucleus. The tonic splenius discharges evoked by periodontal inputs observed in the present study are thought to be mediated through the same pathway, although much more complex pathways—such as cortico- and tecto-reticulospinal pathways—might be involved as well (Alstermark et al., 1992).

In our experiments, periodontal mechanoreceptors were specifically stimulated through the tooth, unlike the usual electrical nerve stimulation applied in previous studies. Moreover, the recordings were made from motor units of the splenius muscle, which responded to the stimulation with tonic discharges.

The overall stimulation used in this study is supposed to be of low intensity. We believe that even higher forces can be expected during normal masticatory function in rats, since natural bite loads above 45 N were measured at the rat's incisors (Robins, 1977). However, it might be considered that for rodents, as opposed to humans, the bite force at the incisors could be greater than that at the molar area. Moreover, we observed, in a side experiment, that 20 times the force used in our study evoked only pressure sensation when applied to the human tooth. Since it has been estimated that the periodontal ligament area of a human molar is about 20 times that of a rat molar (Sato et al., 1984), we may conclude that the reflex responses observed in this study were elicited at non-nociceptive stimulus strengths. Nevertheless, we cannot completely rule out any minor activation of mechanoreceptors in the surrounding alveolar bone or gingiva.

The question that arises is, What kind of head movement is actually produced by activation of periodontal mechanoreceptors? Human experiments have found a prevailing head extension during rhythmic jaw exercises and chewing (Eriksson et al., 2000). In animal experiments, a tendency to extend the head after tooth-loading was observed (Igarashi et al., 2000). The bilateral activation of the splenius muscle shown in this study is consistent with a tendency to head extension. However, since the dorsal neck muscles are also responsible for anti-gravitational support of the head (Pfister and Zenker, 1984), the splenius activation would serve the purpose of stabilizing head posture during mastication. This may explain the difference between the ipsi- and contralateral sides found in our trials. Further experiments with simultaneous recordings from several key neck muscles are required to clarify which specific head movements could be elicited by periodontal mechanoreceptor stimulation alone.

From the present experiment, we conclude that periodontal mechanoreceptors can bilaterally evoke tonic splenius discharges, suggesting that neck muscles may play a supplemental role in normal masticatory movements. Proper inputs from periodontal mechanoreceptors might be important for a possible coupling between neck and jaw muscles.

	ACKNOWLEDGMENTS

 
The authors thank Prof. A. Iriki for valuable discussions. This study was supported in part by Grants-in-Aid for Scientific Research (nos. 12671800 and 12307050, 2000—2001) from the Ministry of Education, Culture, Sports, Science and Technology of Japan. Part of this study was presented at the 23rd Annual Meeting of the Japan Neuroscience Society, Yokohama, Japan, September 4-6, 2000 [Zeredo J, Soma K, Toda K (2001). Motor unit activities in rat splenius muscles following periodontal stimulation. Neurosci Res 24:S22].

Received March 16, 2001; Last revision September 17, 2001; Accepted November 14, 2001

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