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Modulation of cortically induced rhythmic jaw movements in rats by stimulation of the vestibular nuclear complex
Neuroscience Research 68 (2010) 307–314
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Modulation of cortically induced rhythmic jaw movements in rats by stimulation of the vestibular nuclear complex Yoshihide Satoh ∗ , Ken’Ichi Ishizuka, Toshiki Murakami Department of Physiology, The Nippon Dental University School of Life Dentistry at Niigata, 1-8 Hamaura-cho, Chuo-ku, Niigata 951-8580, Japan
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Article history: Received 25 May 2010 Received in revised form 12 August 2010 Accepted 18 August 2010 Available online 26 August 2010 Keywords: Rhythmic jaw movements Orofacial motor cortex Vestibular nuclear complex Lateral vestibulospinal tracts Medial vestibulospinal tracts Locomotion
a b s t r a c t We study whether stimulation of the vestibular nuclear (VN) complex can modulate rhythmic jaw movements in rats anesthetized by urethane. Rhythmic jaw movements were induced by repetitive electrical stimulation of the orofacial motor cortex. Stimulation of the medial vestibular nucleus (MVN) during the jaw-closing phase increased the amplitude of the jaw-closing movement. (This is not a movement that continues to closure.) Stimulation of the MVN during the jaw-opening phase disturbed the rhythm of jaw movements and induced a small jaw-closing movement. Stimulation of the superior VN (SVN) and the lateral VN (LVN) during the jaw-closing phase did not affect the amplitude of the jaw-closing movement. Stimulation of the SVN and the LVN during the jaw-opening phase increased the amplitude of the jawopening movement, however. Stimulation of the inferior VN during the jaw-closing and the jaw-opening phase, respectively decreased the amplitude of the jaw-closing and the jaw-opening movements. Stimulation applied outside the VN did not modulate the amplitude of the jaw movements. These results imply that the VN is involved in the modulation of rhythmic jaw movements induced by stimulation of the orofacial motor cortex. © 2010 Elsevier Ireland Ltd and the Japan Neuroscience Society. All rights reserved.
1. Introduction The vestibular nuclear (VN) complex lies in the floor of the fourth ventricle. It extends from levels that are rostral to the hypoglossal nucleus to slightly beyond the level of the abducens nucleus. The VN consists of the four major nuclei, namely the medial (MVN), lateral (LVN), superior (SVN) and inferior (IVN) vestibular nuclei. Cytoarchitecturally, the MVN is divided into three parts: the parvicellular part, which consists mainly of small cells (MVNPC); the magnocellular part, which contains medium-sized and relatively large cells (MVNMC); and the caudal part (Rubertone et al., 1995). The lateral vestibulospinal tract originates from the LVN and is a major descending pathway of the extrapyramidal motor system. The lateral vestibulospinal neurons are phasically active when extensor muscles are active at the beginning of the stance phase of locomotion (Orlovsky, 1972b; Marlinsky, 1992). Also, stimulation of the LVN during the standing phase of locomotion enhances activity in the ipsilateral extensor muscles, whereas stimulation during the swing phase, when most flexor muscles are active, has little effect (Orlovsky, 1972a; Russel and Zajac, 1979). Like locomotion, mastication is largely programmed in the neural structure within the central nervous system known as the central pattern generator (Dellow and Lund, 1971).
∗ Corresponding author. Tel.: +81 25 267 1500; fax: +81 25 267 1134. E-mail address: [email protected] (Y. Satoh).
Morphological studies have found reciprocal connections between the VN and the spinal trigeminal nucleus (SpV) in rats (Buisseret-Delmas et al., 1999; Diagne et al., 2006; Valla et al., 2003). The SpV is known to contain premotor neurons projecting to the trigeminal motor nucleus (Donga et al., 1990; Li et al., 1995; Olsson and Westberg, 1991; Westberg et al., 1995). Moreover, the trigeminal primary afferent fibers project to the VN (Marfurt and Rajchert, 1991; Matesz, 1983; Pinganaud et al., 1999). Recent studies have found that the MVN and the IVN projects to motoneurons that innervate the masseter muscle (Cuccurazzu et al., 2007; Giaconi et al., 2006). Physiological studies showed that the vestibular input elicited an excitatory tonic control of masseter muscle activity (Tolu and Pugliatti, 1993), and that activation of the vestibular afferents elicited excitatory responses in the jaw-opening and the jaw-closing motoneurons in guinea pigs (Tolu et al., 1996). Our previous paper showed that stimulation of the MVN, the LVN and the SVN facilitates the jaw-opening reflex (JOR), and that stimulation of the IVN inhibits the JOR (Satoh et al., 2009a). Further, stimulation of the MVN facilitates the masseteric monosynaptic reflex (MMR), and stimulation of the IVN inhibits the MMR (Satoh et al., 2009b). It is therefore likely that the VN is involved in the control of jaw movements, as well as locomotion. No description has yet been published of the effect of stimulating the VN during jaw movement. Rhythmic jaw movements can be induced by repetitive electrical stimulation of the orofacial motor cortex (OfM: A-area) (Sasamoto et al., 1990). This study examines whether VN stimulation modulates cortically
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induced rhythmic jaw movements and the activity of the jaw muscles.
2. Methods The experiments were carried out on 23 male Sprague–Dawley rats, weighing 306–401 g. All animal care protocols and surgical procedures were approved by the Laboratory Animal Committee of The Nippon Dental University School of Life Dentistry at Niigata. The animals were initially anesthetized with urethane (1 g/kg i.p.). Supplementary doses (0.2 g/kg) were given via a cannula placed in the femoral vein, to maintain anesthesia at a level that suppressed the withdrawal reflex evoked by noxious stimulation of the paw. The skin and muscles were infiltrated with 2% lidocaine. The trachea and the femoral artery were cannulated. Arterial blood pressure was monitored as a measure of the condition of the animal during the experiment. The rectal temperature was maintained at 37 ◦ C using a regulated heating pad. The anterior belly of the digastric and masseter muscles was exposed on the left or right side, and pairs of Teflon-coated silver wires (diameter 0.1 mm, exposed tip size 2 mm, inter-electrode distance 1.5 mm) were inserted in order to record the electromyograms (dEMG and mEMG, respectively). EMGs were recorded ipsilateral to the OfM stimulation. Activities in the dEMG and the mEMG were amplified (filter bandwidth: 10 Hz to 1 kHz). Jaw movements were recorded in the vertical and horizontal directions by a photodiode transducer that tracked the displacement of a light attached to the mandibular. The recording system was calibrated by attaching the light to an object for which the motion was known. The head was fixed in a stereotaxic apparatus, with ear bars and an incisal bar. Part of the frontal, parietal and interparietal bones was removed, using a dental drill to expose the cortical surface. A bipolar concentric electrode (inner electrode diameter 0.06 mm, outer electrode diameter 0.3 mm, interpolar distance 1 mm) was inserted vertically into the left or right OfM. Electrical stimulation (0.5 ms duration, 30 Hz, 50–250 A, 10 s) was applied to the OfM. The intensity of stimulation was set at the threshold for inducing rhythmic jaw movements. An indifferent electrode was placed on the exposed neck muscle. The cerebellum was removed by suction to expose the brainstem. A bipolar concentric electrode was inserted stereotaxically, vertically into the left or right VN. Stimulation (0.2 ms duration, 1 Hz, 100–130 A, 4 s) was applied to the VN ipsilateral to the OfM stimulation 6 s after the beginning of stimulation of the OfM, once the amplitude of jaw movements was stable. The stimulation site of the OfM was sites 1–4 in one rat. Three trials were performed at each stimulation site. A small screw was implanted into the nasal bone, and a metal rod was attached to the stereotaxic apparatus. The metal rod and screw were connected using acrylic resin. The incisal bar was taken out of the mouth so that the jaw could move freely. The rhythmic jaw movements and dEMG and mEMG were stored on a computer disk. A jaw movement cycle was defined to begin at the moment of maximum jaw opening (the start of the jaw-closing phase) and to end at the next maximum jaw opening. The distance between the maximum jaw-opening position and minimum jaw-opening position was measured for a single cycle. A horizontal movement cycle was defined to begin at the moment of maximum left jaw position (the start of the right movement phase) and to end at the next maximum left jaw position. The distance between the maximum right and left jaw position was also measured. The duration of a jaw movement cycle, the duration of a horizontal movement cycle, the distance between the maximum jaw-opening position and minimum jaw-opening position, and the distance between the
maximum right and left jaw position before the VN stimulation were taken as control values (100%), because the amplitude and frequency of jaw movements changed according to the stimulation sites in a single animal and between animals. We determined the percentage change in the duration of a cycle, the distance between the maximum jaw-opening position and minimum jaw-opening position, and the distance between the maximum right and left jaw position after VN stimulation. The EMG was full-wave rectified and averaged. As a control, the mean EMG activity and standard deviation (S.D.) were calculated for 5 s before the OfM stimulation. The onset of mEMG burst was defined as the instant when mEMG activity exceeded 2 S.D. from the control. Likewise, the offset was defined as the instant when mEMG activity fell below 2 S.D. from the control. The base line of the dEMG activity during the jaw-closing phase exceeded 2 S.D. from the control, however, so that the onset of dEMG burst was defined as the instants at which the dEMG activity exceeded 2 S.D. from the baseline. The duration of the EMG burst for which the perturbation occurred by stimulation of the VN is referred to as the perturbed duration. The duration of the EMG burst after the perturbed duration is termed the post-stimulus duration. The duration of the EMG burst immediately prior to the perturbed duration is referred to as the pre-stimulus duration. The durations of the mean perturbed duration and the post-stimulus duration are expressed as a percentage of the mean pre-stimulus duration (control). All data were analyzed for statistical significance by the Wilcoxon t-test (P < 0.05). At the end of each experiment, electric lesions were made by passing negative current (20 A, 30 s) through the stimulating electrode. The animals were then given a lethal dose of anesthetic, and the brain was perfused through the left cardiac ventricle with 0.9% saline followed by 10% buffered formalin solution (pH 7.4). Serial coronal sections of the brain were cut (50 m thick) and counterstained with cresyl violet. The stimulation sites were verified using the atlas of Paxinos and Watson (2007). 3. Results The threshold of the rhythmic jaw movements varied from 50 to 250 A. The characteristics of the jaw movement pattern and the EMG match those found in previous studies (Sasamoto et al., 1990; Satoh et al., 2006, 2007). The movements always began with opening of the jaw, and were followed by rhythmic movements which consisted of simple opening–closing movements. The frequency of rhythmic jaw movements was 5–7 Hz. Vertical movements were small and horizontal movement was very small. The uppermost position of the jaw movements was below the resting position of the jaw; as a result, the lower teeth did not come into contact with the upper teeth. There was no activity in the mEMG in the early stage of the jaw movements. Activity in the dEMG and mEMG showed bursts during the jaw-opening and the jaw-closing phase, respectively. The rhythmic jaw movements that were induced from the OfM exhibited a similar pattern in different animals, but the amplitude of these jaw movements varied with stimulation site in a single animal and between animals. The sites for electrical stimulation are similar to those in our previous study (Satoh et al., 2007). 3.1. MVNPC Stimuli applied in the jaw-closing phase increased the amplitude of the jaw-closing movement (which is incomplete and does not proceed to complete closure) in all cases (5 rats). The amplitude of the horizontal movements increased ipsilaterally with the OfM stimulation (Fig. 1A). Of 96 cases, 81 increased the amplitude of
Y. Satoh et al. / Neuroscience Research 68 (2010) 307–314
Fig. 1. Effect of stimulation of the right MVNPC (0.2 ms duration, 1 Hz, 130 A, 4 s) on the rhythmic jaw movements induced by stimulation of the right OfM (0.5 ms duration, 30 Hz, 60 A, 10 s). The arrow indicates the moment of stimulation to the MVNPC. HORZ: horizontal jaw movements (left down); VERT: vertical jaw movements (opening down); dEMG and mEMG: electromyographic activities of the anterior belly of the digastric muscle and masseter muscle on the right side. (A) Example of the recording. (B) EMGs were rectified and averaged in eight stimuli in the jaw-closing phase. (C) EMGs were rectified and averaged in four stimuli in the jaw-opening phase.
the horizontal movements and 15 did not modulate it. There was a significant difference (P < 0.05) before and after stimulation of the MVNPC in the distance from the maximum to the minimum jawopening position, and in the distance from the maximum left to maximum right positions (Table 1). The rhythm of the jaw movements was altered slightly. The duration of a jaw movement cycle after stimulation of the MVNPC was increased to 108.7 ± 11.2% (mean ± S.D., n = 96) of the value in controls. The duration of the horizontal movement was lengthened to 105.1 ± 8.9% (mean ± S.D.,
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n = 96) of the value in controls. There was a significant difference (P < 0.05) in the duration of the jaw movement cycle and the horizontal movement before and after stimulation of the MVNPC. These effects were induced transiently in one cycle of vertical and horizontal jaw movements. The duration of activity in the mEMG was increased (Fig. 1B). The perturbed duration in the mEMG rose to 118.4 ± 15.1% (mean ± S.D., n = 96). There was significant difference between the pre-stimulus duration and the perturbed duration (P < 0.05). On the other hand, the post-stimulus duration in the mEMG was 100.1 ± 7.9% (mean ± S.D., n = 96). There was no significant difference between the pre-stimulus duration and the post-stimulus duration (P > 0.05). Stimuli applied in the jaw-opening phase disturbed the rhythm of jaw movements in all cases (5 rats). A small jaw-closing movement was induced at 4.0–11.0 ms (6.4 ± 1.8 ms, mean ± S.D., n = 41) after the stimulation of the MVNPC. The distance from the maximum to the minimum jaw-opening position after stimulation of the MVNPC fell (Fig. 1A). There was a significant difference (P < 0.05) in the distance before and after stimulation of the MVNPC (Table 1). The duration of a jaw movement cycle after stimulation of the MVNPC rose to 120.0 ± 30.0% (mean ± S.D., n = 41) of the value in controls. The amplitude of the horizontal movements was unaffected, but the duration of the horizontal movement was lengthened to 109.3 ± 12.9% (mean ± S.D., n = 41) of the value in controls. There was a significant difference (P < 0.05) in the duration of a jaw movement cycle and the horizontal movement before and after stimulation of the MVNPC. These effects were induced transiently in one cycle of vertical and horizontal jaw movements. A transient burst and inhibitory period was induced in the mEMG and in the dEMG (Fig. 1C). The perturbed duration in the dEMG was significantly reduced to 70.6 ± 17.2% (mean ± S.D., n = 41) (P < 0.05). On the other hand, the post-stimulus duration in the dEMG was 101.6 ± 7.0% (mean ± S.D., n = 41). There was no significant difference between the pre-stimulus duration and the post-stimulus duration (P > 0.05). These results were consistent across the animals tested.
3.2. MVNMC Stimuli applied in the jaw-closing phase increased the amplitude of the jaw-closing movement in all cases (5 rats). The amplitude of the horizontal movements increased ipsilaterally with the OfM stimulation (Fig. 2A). Only 2 cases did not modulate the amplitude of the horizontal movements. There was a significant difference (P < 0.05) before and after stimulation of the MVNMC in the distance from the maximum to the minimum jaw-opening position, and from the maximum left to maximum right positions (Table 1). Also, the rhythm of the jaw movements was slightly altered. The duration of a jaw movement cycle after stimulation of the MVNMC was lengthened to 108.8 ± 12.9% (mean ± S.D., n = 70) of the value in controls. The duration of the horizontal movement was lengthened to 110.2 ± 10.7% (mean ± S.D., n = 70) of the value in
Table 1 Effect on the rhythmic jaw movements of stimulating the MVNPC, MVNPC, LVN, SVN and IVN. Stimulation sites
Vertical jaw movements Closing phase
MVNPC MVNMC LVN SVN IVN
130.9 141.1 101.0 102.0 97.7
± ± ± ± ±
24.9% (96)* 23.1% (70)* 5.6% (71) 7.9% (73) 9.2% (84)*
Horizontal jaw movements Opening phase 44.7 60.9 112.9 115.1 85.3
± ± ± ± ±
21.7% (41)* 24.2% (52)* 17.1% (51)* 17.1% (63)* 11.1% (80)*
Closing phase 126.8 181.7 102.7 99.2 96.5
± ± ± ± ±
27.3% (96)* 46.5% (70)* 12.9% (71) 12.0% (73) 17.4% (84)*
Opening phase 101.9 140.2 103.3 103.8 85.9
± ± ± ± ±
13.2% (41) 30.4% (52)* 13.5% (51) 14.3% (63) 20.8% (80)*
Values are mean ± S.D. Values in the parenthesis indicate numbers. * Significant difference before and after stimulation of the VN (P < 0.05, Wilcoxon’s t-test) in the distance from the maximum jaw-opening position to the minimum jaw-opening position, or in the distance from the maximum right to the maximum left jaw position.
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Fig. 2. (A) Effect of stimulation of the right MVNMC (0.2 ms duration, 1 Hz, 130 A, 4 s) on the rhythmic jaw movements induced by stimulation of the right OfM (0.5 ms duration, 30 Hz, 120 A, 10 s). (B) EMGs were rectified and averaged in seven stimuli in the jaw-closing phase. (C) EMGs were rectified and averaged in five stimuli in the jaw-opening phase. Other details are as in Fig. 1.
Fig. 3. (A) Effect of stimulation of the left LVN (0.2 ms duration, 1 Hz, 130 A, 4 s) on the rhythmic jaw movements induced by stimulation of the left OfM (0.5 ms duration, 30 Hz, 100 A, 10 s). (B) EMGs were rectified and averaged in six stimuli in the jaw-closing phase. (C) EMGs were rectified and averaged in six stimuli in the jaw-opening phase. Other details are as in Fig. 1.
controls. There was a significant difference (P < 0.05) in the duration of the jaw movement cycle, and the horizontal movement, before and after stimulation of the MVNMC. These effects were induced transiently in one cycle of vertical and horizontal jaw movements. The amplitude of activity was increased in the mEMG (Fig. 2B). The perturbed duration in the mEMG was significantly increased to 115.3 ± 13.4% (mean ± S.D., n = 70) (P < 0.05). The post-stimulus duration in the mEMG was 99.8 ± 7.4% (mean ± S.D., n = 70), however. There was no significant difference between the pre-stimulus duration and the post-stimulus duration (P > 0.05). Stimuli applied in the jaw-opening phase disturbed the rhythm of jaw movements in all cases (5 rats). A small jaw-closing movement was induced at 5.0–15.0 ms (8.4 ± 1.7 ms, mean ± S.D., n = 52) after the MVNMC stimulation. The small horizontal movement induced was ipsilateral to the OfM stimulation (Fig. 2A). There was a significant difference (P < 0.05) before and after stimulation of the MVNMC in the distance from the maximum to the minimum jaw-opening position, and from the maximum left to maximum right positions (Table 1). The duration of a jaw movement cycle after stimulation of the MVNMC increased to 108.0 ± 10.1% of the value in controls (mean ± S.D., n = 52). The duration of the horizontal movement increased to 113.4 ± 13.5% (mean ± S.D., n = 52) of the value in controls. There was a significant difference (P < 0.05) in the duration of the jaw movement cycle and in the horizontal movement before and after stimulation of the MVNMC. These effects were induced transiently in one cycle of vertical and horizontal jaw
movements. A transient burst was induced in the mEMG (Fig. 2C). The perturbed duration in the dEMG was reduced significantly, to 68.8 ± 22.1% (mean ± S.D., n = 52) (P < 0.05). The post-stimulus duration in the dEMG was 100.8 ± 11.6% (mean ± S.D., n = 52). There was no significant difference between the pre-stimulus duration and the post-stimulus duration (P > 0.05). These results were consistent across the animals tested. 3.3. LVN Stimuli applied in the jaw-closing phase did not modulate the amplitude of the jaw-closing and the jaw-opening movement (Fig. 3A). There was no significant difference (P > 0.05) in the distance from the maximum to the minimum jaw-opening position before and after stimulation of the LVN (Table 1). Also, the rhythm of the jaw movements was unchanged. The duration of a jaw movement cycle after stimulation of the LVN was 102.4 ± 10.6% (mean ± S.D., n = 71) of the value in controls. There was no significant difference (P > 0.05) in the duration of the jaw movement cycle before and after stimulation of the LVN. The amplitude and duration of the horizontal movements and of the activity in the EMG were unaffected (Fig. 3A and B). Stimuli applied in the jaw-opening phase increased the amplitude of the jaw-opening movement in 41 cases (6 rats) (Fig. 3A). 10 cases did not modulate the amplitude of the jaw-opening movement. There was a significant difference (P < 0.05) in the distance
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Fig. 4. (A) Effect of stimulation of the left SVN (0.2 ms duration, 1 Hz, 130 A, 4 s) on the rhythmic jaw movements induced by stimulation of the left OfM (0.5 ms duration, 30 Hz, 130 A, 10 s). (B) EMGs were rectified and averaged in six stimuli in the jaw-closing phase. (C) EMGs were rectified and averaged in six stimuli in the jaw-opening phase. Other details are as in Fig. 1.
from the maximum to the minimum jaw-opening position before and after stimulation of the LVN (Table 1). This effect was induced transiently in one cycle of vertical and horizontal jaw movements. The rhythm of the jaw movements was unchanged, however. The duration of the jaw movement cycle after stimulation of the LVN was 102.0 ± 9.4% (mean ± S.D., n = 51) of the value in controls. There was no significant difference (P > 0.05) in the duration of the jaw movement cycle before and after stimulation of the LVN. The amplitude and duration of the horizontal movement and of the activity in the EMG were unaffected (Fig. 3A and C). These results were consistent across the animals tested. 3.4. SVN Stimuli applied in the jaw-closing phase did not modulate the amplitude of the jaw-closing movement and the jaw-opening movement (Fig. 4A). There was no significant difference (P > 0.05) in the distance from the maximum to the minimum jaw-opening position before and after stimulation of the SVN (Table 1). Also, the rhythm of the jaw movements was unchanged. The duration of the jaw movement cycle after stimulation of the SVN was 102.0 ± 7.9% (mean ± S.D., n = 73) of the value in controls. There was no significant difference (P > 0.05) in the duration of the jaw movement cycle before and after stimulation of the SVN. The amplitude and duration of the horizontal movements and of the activity in the EMG were unaffected (Fig. 4A and B).
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Fig. 5. (A) Effect of stimulation of the right IVN (0.2 ms duration, 1 Hz, 130 A, 4 s) on the rhythmic jaw movements induced by stimulation of the right OfM (0.5 ms duration, 30 Hz, 85 A, 10 s). (B) EMGs were rectified and averaged in five stimuli in the jaw-closing phase. (C) EMGs were rectified and averaged in seven stimuli in the jaw-opening phase. Other details are as in Fig. 1.
Stimuli applied in the jaw-opening phase increased the amplitude of the jaw-opening movement in 51 cases (6 rats) (Fig. 4A). 12 cases did not modulate the amplitude of the jaw-opening movement. There was a significant difference (P < 0.05) in the distance from the maximum to the minimum jaw-opening position before and after stimulation of the SVN (Table 1). Also, the rhythm of the jaw movements was altered slightly. The duration of the jaw movement cycle after stimulation of the SVN was lengthened to 105.2 ± 10.9% (mean ± S.D., n = 63) of the value in controls. There was a significant difference (P < 0.05) in the duration of the jaw movement cycle before and after stimulation of the SVN. These effects were induced transiently in one cycle of vertical and horizontal jaw movements. The amplitude and duration of the horizontal movements and of the activity in the EMG were unaffected (Fig. 4A and C). These results were consistent across the animals tested. 3.5. IVN Stimuli applied in the jaw-closing phase reduced the amplitude of the jaw-closing movement in 51 cases (3 rats). 33 cases did not modulate the amplitude of the jaw-closing movement. The amplitude of the horizontal movements decreased slightly in 53 cases (Fig. 5A). 31 cases did not modulate the amplitude of the horizontal movements. There was a significant difference before and after stimulation of the IVN (P < 0.05) in the distance from the maximum
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Fig. 6. Diagrammatic representation of the stimulating sites. Filled circles indicate that stimuli during the jaw-closing phase increase the amplitude of the jaw-closing movement and stimuli during the jaw-opening phase induced a small jaw-closing movement. Open circles indicate that stimuli in the jaw-opening phase increase the amplitude of the jaw-opening movement. Triangles indicate that stimuli in the jaw-closing and the jaw-opening phase reduced the amplitudes of the jaw-closing and jawopening movements, respectively. Squares indicate ineffective sites. The number associated with each diagram represents the level of the coronal section from the bregma in mm; – signs denote caudal to the bregma. Abbreviations: MVNPC, medial vestibular nucleus, parvicellular part; MVNMC, medial vestibular nucleus, magnocellular part; SVN, superior vestibular nucleus; LVN, lateral vestibular nucleus; IVN, inferior vestibular nucleus; scp, superior cerebellar peduncle; icp, inferior cerebellar peduncle; veme, vestibulomesencephalic tract; vesp, vestibulospinal tract; Pr, prepositus nucleus; Sol, solitary tract; 7n, facial nerve; g7, genu of the facial nerve, asc 7, ascending fibers of the facial nerve; 8vn, vestibular root of the vestibulocochlear nerve.
to the minimum jaw-opening position, and from the maximum left to maximum right position (Table 1). These effects were induced transiently in one cycle of vertical and horizontal jaw movements. The rhythm of the jaw movements was unchanged, however. The duration of the jaw movement cycle after stimulation of the IVN was 98.2 ± 10.1% (mean ± S.D., n = 84) of the value in controls. There was no significant difference (P > 0.05) in the duration of the jaw movement cycle before and after stimulation of the IVN. The duration of horizontal movement and the activity in the EMG were unaffected (Fig. 5A and B). Stimuli applied in the jaw-opening phase reduced the amplitude of the jaw-opening movement in 73 cases (3 rats). 7 cases did not modulate the amplitude of the jaw-opening movement. The amplitude of the horizontal movements decreased in 64 cases (Fig. 5A). 16 cases did not modulate the amplitude of the horizontal movements. There was a significant difference (P < 0.05) before and after stimulation of the IVN in the distance from the maximum to the minimum jaw-opening position, and from the maximum left to maximum right position (Table 1). Also, the rhythm of the jaw movements was altered slightly. The duration of the jaw movement cycle after stimulation of the IVN increase to 104.2 ± 10.7% (mean ± S.D., n = 80) of controls. There was a significant difference (P < 0.05) in the duration of the jaw movement cycle before and after stimulation of the IVN. These effects were induced transiently in one cycle of vertical and horizontal jaw movements. The duration of horizontal movement and the activity in the EMG were unaffected (Fig. 5A and C). These results were consistent across the animals tested.
3.6. Outside the VN Stimuli applied in the jaw-closing phase did not modulate the amplitude of the jaw-closing movement or the jaw-opening movement. The distance from the maximum to the minimum jawopening position after stimulation outside the VN was 100.7 ± 6.3% (mean ± S.D., n = 53) of the value in controls. The duration of the jaw movement cycle after stimulation outside the VN was 103.7 ± 8.5% (mean ± S.D., n = 53) of the value in controls. Stimuli applied in the jaw-opening phase did not modulate the amplitude of the jaw-closing movement or the jaw-opening movement. The distance from the maximum to the minimum jawopening position after stimulation outside the VN was 99.6 ± 10.6% (mean ± S.D., n = 41) of the value in controls. The duration of the jaw movement cycle after stimulation outside the VN was 102.6 ± 10.7% (mean ± S.D., n = 41) of the value in controls. There was no significant difference (P > 0.05) in these values before and after stimulation outside the VN. The amplitude and duration of the horizontal movements and of the activity in the EMG were unaffected. These results were consistent across the animals tested. The electrical stimulation sites of the VN are shown in Fig. 6 on diagrams of the transverse section. 4. Discussion Stimuli applied to the MVN in the jaw-closing phase increased the amplitude of the jaw-closing movement, whereas stimuli applied to the MVN in the jaw-opening phase disturbed the rhythm
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of jaw movements and induced a small jaw-closing movement. This result was unexpected. Our previous study found that the JOR and the MMR was facilitated by stimulation of the MVN (Satoh et al., 2009a,b). We therefore suppose that stimuli applied in the jaw-opening phase increase the amplitude of the jaw-opening movement. Rhythmic jaw movements always begin with sustained jaw-opening and consist of simple opening–closing movements of the jaw. In all cases the jaw remained at a level below the resting position during the rhythmic jaw movements. Consequently, the excitability of the jaw-opening motoneurons may not be enhanced during the jaw-opening phase upon stimulation of the MVN, and the jaw-closing movement occurred preferentially during jaw movements. Stimuli applied to the LVN and the SVN in the jaw-closing phase and in the jaw-opening phase did not modulate the amplitude of the jaw-closing movement, and increased the amplitude of the jawopening movement. The jaw-closing and the jaw-opening muscles are regarded as the equivalents of the extensor and the flexor muscles of the limbs, respectively, since noxious stimulation of the orofacial region evokes the JOR via one or more interneurons, and the MMR is evoked by muscle spindle afferents in the jaw-closing muscles (Dessem et al., 1988; Nakamura et al., 1973; Sumino, 1971). Stimulation of the LVN during the standing phase of locomotion, when the extensor muscles are active, enhances activity in the ipsilateral extensor muscles. Stimulation of the LVN during the swing phase, when the flexor muscles are active, has little effect (Orlovsky, 1972a; Russel and Zajac, 1979). We therefore suggest that the functional role of the LVN is not analogous in jaw movements and in locomotion. Stimuli applied to the IVN in the jaw-closing and the jawopening phase reduced the amplitude of the jaw-closing and the jaw-opening movement, respectively. These results could be related to physiological findings in our previous studies that the JOR and the MMR are inhibited by stimulation of the IVN (Satoh et al., 2009a,b). Stimulation of the MVN and the IVN, especially the MVNMC, affected horizontal movements of the jaw (Table 1). This suggests that the effects of the MVN and the IVN manifest at the unilateral jaw muscles. No such phenomena were observed, however, when stimulation was applied to the LVN and the SVN, suggesting that the effects of the LVN and the SVN manifest at the bilateral jaw muscles. When horizontal movements are made in humans, the lateral pterygoid muscle (jaw-opening muscle), the medial pterygoid muscle (jaw-closing muscle) on the contralateral side, and the posterior portion of the temporal muscle (jaw-closing muscle) on the ipsilateral side to rotation direction are all active (Mahan et al., 1983; Miller, 1991; Murray et al., 1999). Lateral pterygoid muscle activity in the rat appears to show the same basic pattern as in humans (Byrd and Chai, 1988). As a result, stimulation of the MVN and the IVN affected these muscles. This suggestion is supported by the morphological studies. The LVN and the SVN project bilaterally to the SpV oralis (SpVO) and the interporalis (SpVI). However, the MVN and the IVN project bilaterally to the dorsal part of the SpVO and the entire of the SpVI with ipsilateral dominance. The MVN projects bilaterally to the intermediate part of the SpVO with contralateral or ipsilateral dominance (Buisseret-Delmas et al., 1999). The dorsal part of the SpVO and the SpVI project bilaterally to the jaw-closing motoneurons with ipsilateral dominance, whereas the intermediate part of the SpVO and the SpVI project bilaterally to the jaw-opening motoneurons with ipsilateral dominance (Li et al., 1995). Stimulation of the VN induced transient effects, and had no effect on the onset and cessation of cycle of jaw movements. This suggests that effects of the VN stimulation act on only output side from the central pattern generator of the rhythmic jaw movements or from the premotor neurons projecting to the trigeminal motor
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nucleus, and do not directly influence the central pattern generator of the rhythmic jaw movements. The cycle duration of the jaw movements was altered by stimulation of the MVN. It was also slightly altered by stimulation of the SVN and the IVN in the jaw-opening phase. In guinea pigs, the output from the cortical masticatory area descends to the nucleus reticularis paragigantocellularis via the corticobulbar fibers. The output from the nucleus reticularis paragigantocellularis runs in turn to the nucleus reticularis gigantocellularis (Nozaki et al., 1986a,b). It has been reported that the central pattern generator of the rhythmic jaw movements is located in the medial bulbar reticular formation, including the nucleus reticularis gigantocellularis (Nozaki et al., 1986a). In the rat, the VN, especially the MVN, projects to the nucleus reticularis paragigantocellularis (Andrezik et al., 1981). The VN projects to the SpV in rats (Buisseret-Delmas et al., 1999; Diagne et al., 2006; Valla et al., 2003). The SpV is known to contain premotor neurons projecting to the trigeminal motor nucleus (Donga et al., 1990; Li et al., 1995; Olsson and Westberg, 1991; Westberg et al., 1995). Stimulation of the contralateral trigeminal motor nucleus antidromically activates neurons in the SpVO (Donga et al., 1990). These neurons were almost all activated by stimulating the cortical masticatory area after a short latency, and most showed rhythmic activity during cortically induced fictive mastication (Donga and Lund, 1991). The VN stimulation may therefore influence these premotor neurons in the SpV and the nucleus reticularis paragigantocellularis, and alter the rhythm of jaw movements. The pathways from the OfM to the VN have been revealed by morphological studies. The OfM neurons project to the dorsal part of the trigeminal sensory complex (Zhang and Sasamoto, 1990). The VN receives fibers from the SpV (Buisseret-Delmas et al., 1999; Diagne et al., 2006; Valla et al., 2003). It may therefore be assumed that the VN receives inputs from the OfM via these pathways. In conclusion, the present study has shown that stimuli applied to the VN influence the rhythmic jaw movements induced by stimulation of the OfM. We suggest that the VN is involved in modulating the rhythmic jaw movements induced by stimulation of the OfM, and is related to the control of jaw movements. The physiological role of the VN in regulating the rhythmic jaw movements appears to be the coordination between the jaw-opening movement, the jaw-closing movement and the lateral movement of jaw. Acknowledgments This study was partly supported by Research Promotion Grant (NDUF-09-01) from The Nippon Dental University and by Grantsin-Aid for Scientific Research from the Ministry of Education, Culture, Sports, Science and Technology of Japan (#22592079). References Andrezik, J.A., Chan-Palay, V., Palay, S.L., 1981. The nucleus paragigantocellularis lateralis in the rat. Anat. Embryol. 161, 373–390. Buisseret-Delmas, C., Compoint, C., Delfini, C., Buisseret, P., 1999. Organisation of reciprocal connections between trigeminal and vestibular nuclei in the rat. J. Comp. Neurol. 409, 153–168. Byrd, K.E., Chai, Y., 1988. Three-dimensional movement analysis of lateral pterygoid electromyographic activity during mastication in the rat. Arch. Oral Biol. 33, 635–640. Cuccurazzu, B., Deriu, F., Tolu, E., Yates, B.J., Billing, I., 2007. A monosynaptic pathway links the vestibular nuclei and masseter muscle motoneurons in rats. Exp. Brain Res. 176, 665–671. Dellow, P.G., Lund, J.P., 1971. Evidence for central timing of rhythmical mastication. J. Physiol. 215, 1–13. Dessem, D., Iyadurai, O.D., Taylor, A., 1988. The role of periodontal receptors in the jaw-opening reflex in the cat. J. Physiol. 406, 315–330. Diagne, M., Valla, J., Delfini, C., Buisseret-Delmas, C., Buisseret, P., 2006. Trigeminovestibular and trigeminospinal pathways in rats: retrograde tracing
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compared with glutamic acid decarboxylase and glutamate immunohistochemistry. J. Comp. Neurol. 496, 759–772. Donga, R., Lund, J.P., Veilleux, D., 1990. An electrophysiological study of trigeminal commissural interneurons in the anaesthetized rabbit. Brain Res. 515, 351–354. Donga, R., Lund, J.P., 1991. Discharge patterns of trigeminal commissural lastorder interneurons during fictive mastication in the rabbit. J. Neurophysiol. 66, 1564–1578. Giaconi, E., Deriu, F., Tolu, E., Cuccurazzu, B., Yates, B.J., Billing, I., 2006. Transneuronal tracing of vestibulo-trigeminal pathways innervating the masseter muscle in the rat. Exp. Brain Res. 171, 330–339. Li, Y.Q., Takada, M., Kaneko, T., Mizuno, N., 1995. Premotor neurons for trigeminal motor nucleus neurons innervating the jaw-closing and jaw-opening muscles: differential distribution in the lower brainstem in the rat. J. Comp. Neurol. 356, 563–579. Mahan, P.E., Wilkinson, T.M., Gibbs, C.H., Mauderli, A., Brannon, L.S., 1983. Superior and inferior bellies of the lateral pterygoid muscle EMG activity at basic jaw positions. J. Prosthet. Dent. 50, 710–718. Marfurt, C.F., Rajchert, D.M., 1991. Trigeminal primary afferent projections to “nontrigeminal” areas of the rat central nervous system. J. Comp. Neurol. 303, 489–511. Marlinsky, V.V., 1992. Activity of lateral vestibular nucleus neurons during locomotion in the decerebrate guinea pig. Exp. Brain Res. 90, 583–588. Matesz, C., 1983. Termination of primary afferent fibers of the trigeminal nerve in the rat. Acta Biol. Hung. 34, 31–44. Miller, A.J., 1991. Craniomandibular Muscles: Their Role in Function and Form. CRC Press, Florida. Murray, G.M., Orfanos, T., Chan, J.Y., Wanigaratne, K., Klineberg, I.J., 1999. Electromyographic activity of the human lateral pterygoid muscle during contralateral and protrusive jaw movements. Arch. Oral Biol. 44, 269–285. Nakamura, Y., Nagashima, H., Mori, S., 1973. Bilateral effects of the afferent impulses from the masseteric muscle on the trigeminal motoneuron of the cat. Brain Res. 57, 15–27. Nozaki, S., Iriki, A., Nakamura, Y., 1986a. Localization of central rhythm generator involved in cortically induced rhythmical masticatory jaw-opening movement in the guinea pig. J. Neurophysiol. 55, 806–825. Nozaki, S., Iriki, A., Nakamura, Y., 1986b. Role of corticobulbar projection neurons in cortically induced rhythmical masticatory jaw-opening movement in the guinea pig. J. Neurophysiol. 55, 826–845. Olsson, K.Å., Westberg, K.-G., 1991. Integration in trigeminal premotor interneurons in the cat. 2. Functional characteristics of neurones in the subnucleus-␥ of the oral nucleus of the spinal trigeminal tract with a projection to the digastric motoneurone subnucleus. Exp. Brain Res. 84, 115–124. Orlovsky, G.N., 1972a. The effect of different descending systems on flexor and extensor activity during locomotion. Brain Res. 40, 359–371.
Orlovsky, G.N., 1972b. Activity of vestibulospinal neurons during locomotion. Brain Res. 46, 85–98. Paxinos, G., Watson, C., 2007. The Rat Brain in Stereotaxic Coordinates. Academic Press, San Diego. Pinganaud, G., Bourcier, F., Buisseret-Delmas, C., Buisseret, P., 1999. Primary trigeminal afferents to the vestibular nuclei in the rat: existence of a collateral projection to the vestibulo-cerebellum. Neurosci. Lett. 264, 133–136. Rubertone, J.A., Mehler, W.R., Voogd, J., 1995. The vestibular nuclear complex. In: Paxinos, G. (Ed.), The Rat Nervous System, 2nd ed. Academic Press, San Diego, pp. 773–796. Russel, D.F., Zajac, F.E., 1979. Effects of stimulating Deiters’ nucleus and medial longitudinal fasciculus on the timing of the fictive locomotor rhythm induced in cats by DOPA. Brain Res. 177, 588–592. Sasamoto, K., Zhang, G., Iwasaki, M., 1990. Two types of rhythmical jaw movements evoked by stimulation of the rat. Jpn. J. Oral Biol. 32, 57–68. Satoh, Y., Ishizuka, K., Murakami, T., 2006. Modulation of cortically induced rhythmical jaw movements by stimulation of the red nucleus in the rat. Brain Res. 1087, 114–122. Satoh, Y., Ishizuka, K., Murakami, T., 2007. Changes in cortically induced rhythmic jaw movements after lesioning of the red nucleus in rats. Brain Res. 1165, 60–70. Satoh, Y., Ishizuka, K., Murakami, T., 2009a. Modulation of the jaw-opening reflex by stimulation of the vestibular nuclear complex in rats. Neurosci. Lett. 457, 21–26. Satoh, Y., Ishizuka, K., Murakami, T., 2009b. Modulation of the masseteric monosynaptic reflex by stimulation of the vestibular nuclear complex in rats. Neurosci. Lett. 466, 16–20. Sumino, R., 1971. Central neural pathways involved in the jaw-opening reflex in the cat. In: Dubner, R., Kawamura, Y. (Eds.), Oral-Facial Sensory and Motor Mechanisms. Appleton-Century-Croft, New York, pp. 315–331. Tolu, E., Pugliatti, M., 1993. The vestibular system modulates masseter muscle activity. J. Vestib. Res. 3, 163–171. Tolu, E., Caria, M.A., Chessa, G., Meils, F., Simula, M.E., Podda, M.V., Solinas, A., Deriu, F., 1996. Trigeminal motoneuron responses to vestibular stimulation in the guinea pig. Arch. Ital. Biol. 134, 141–151. Valla, J., Delfini, C., Diagne, M., Pinganaud, G., Buisseret, P., Buisseret-Delmas, C., 2003. Vestibulotrigeminal and vestibulospinal projections in rats: retrograde tracing coupled to glutamic acid decarboxylase immunoreactivity. Neurosci. Lett. 340, 225–228. Westberg, K.-G., Sandström, G., Olsson, K.Å., 1995. Integration in trigeminal premotor interneurons in the cat. 3. Input characteristics and synaptic actions of neurones in the subnucleus-␥ of the oral nucleus of the spinal trigeminal tract with a projection to the masseteric motoneurone subnucleus. Exp. Brain Res. 104, 449–461. Zhang, G., Sasamoto, K., 1990. Projections of two separate cortical areas for rhythmical jaw movements in the rat. Brain Res. Bull. 24, 221–230.
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Modulation of cortically induced rhythmic jaw movements in rats by stimulation of the vestibular nuclear complex Yoshihide Satoh ∗ , Ken’Ichi Ishizuka, Toshiki Murakami Department of Physiology, The Nippon Dental University School of Life Dentistry at Niigata, 1-8 Hamaura-cho, Chuo-ku, Niigata 951-8580, Japan
a r t i c l e
i n f o
Article history: Received 25 May 2010 Received in revised form 12 August 2010 Accepted 18 August 2010 Available online 26 August 2010 Keywords: Rhythmic jaw movements Orofacial motor cortex Vestibular nuclear complex Lateral vestibulospinal tracts Medial vestibulospinal tracts Locomotion
a b s t r a c t We study whether stimulation of the vestibular nuclear (VN) complex can modulate rhythmic jaw movements in rats anesthetized by urethane. Rhythmic jaw movements were induced by repetitive electrical stimulation of the orofacial motor cortex. Stimulation of the medial vestibular nucleus (MVN) during the jaw-closing phase increased the amplitude of the jaw-closing movement. (This is not a movement that continues to closure.) Stimulation of the MVN during the jaw-opening phase disturbed the rhythm of jaw movements and induced a small jaw-closing movement. Stimulation of the superior VN (SVN) and the lateral VN (LVN) during the jaw-closing phase did not affect the amplitude of the jaw-closing movement. Stimulation of the SVN and the LVN during the jaw-opening phase increased the amplitude of the jawopening movement, however. Stimulation of the inferior VN during the jaw-closing and the jaw-opening phase, respectively decreased the amplitude of the jaw-closing and the jaw-opening movements. Stimulation applied outside the VN did not modulate the amplitude of the jaw movements. These results imply that the VN is involved in the modulation of rhythmic jaw movements induced by stimulation of the orofacial motor cortex. © 2010 Elsevier Ireland Ltd and the Japan Neuroscience Society. All rights reserved.
1. Introduction The vestibular nuclear (VN) complex lies in the floor of the fourth ventricle. It extends from levels that are rostral to the hypoglossal nucleus to slightly beyond the level of the abducens nucleus. The VN consists of the four major nuclei, namely the medial (MVN), lateral (LVN), superior (SVN) and inferior (IVN) vestibular nuclei. Cytoarchitecturally, the MVN is divided into three parts: the parvicellular part, which consists mainly of small cells (MVNPC); the magnocellular part, which contains medium-sized and relatively large cells (MVNMC); and the caudal part (Rubertone et al., 1995). The lateral vestibulospinal tract originates from the LVN and is a major descending pathway of the extrapyramidal motor system. The lateral vestibulospinal neurons are phasically active when extensor muscles are active at the beginning of the stance phase of locomotion (Orlovsky, 1972b; Marlinsky, 1992). Also, stimulation of the LVN during the standing phase of locomotion enhances activity in the ipsilateral extensor muscles, whereas stimulation during the swing phase, when most flexor muscles are active, has little effect (Orlovsky, 1972a; Russel and Zajac, 1979). Like locomotion, mastication is largely programmed in the neural structure within the central nervous system known as the central pattern generator (Dellow and Lund, 1971).
∗ Corresponding author. Tel.: +81 25 267 1500; fax: +81 25 267 1134. E-mail address: [email protected] (Y. Satoh).
Morphological studies have found reciprocal connections between the VN and the spinal trigeminal nucleus (SpV) in rats (Buisseret-Delmas et al., 1999; Diagne et al., 2006; Valla et al., 2003). The SpV is known to contain premotor neurons projecting to the trigeminal motor nucleus (Donga et al., 1990; Li et al., 1995; Olsson and Westberg, 1991; Westberg et al., 1995). Moreover, the trigeminal primary afferent fibers project to the VN (Marfurt and Rajchert, 1991; Matesz, 1983; Pinganaud et al., 1999). Recent studies have found that the MVN and the IVN projects to motoneurons that innervate the masseter muscle (Cuccurazzu et al., 2007; Giaconi et al., 2006). Physiological studies showed that the vestibular input elicited an excitatory tonic control of masseter muscle activity (Tolu and Pugliatti, 1993), and that activation of the vestibular afferents elicited excitatory responses in the jaw-opening and the jaw-closing motoneurons in guinea pigs (Tolu et al., 1996). Our previous paper showed that stimulation of the MVN, the LVN and the SVN facilitates the jaw-opening reflex (JOR), and that stimulation of the IVN inhibits the JOR (Satoh et al., 2009a). Further, stimulation of the MVN facilitates the masseteric monosynaptic reflex (MMR), and stimulation of the IVN inhibits the MMR (Satoh et al., 2009b). It is therefore likely that the VN is involved in the control of jaw movements, as well as locomotion. No description has yet been published of the effect of stimulating the VN during jaw movement. Rhythmic jaw movements can be induced by repetitive electrical stimulation of the orofacial motor cortex (OfM: A-area) (Sasamoto et al., 1990). This study examines whether VN stimulation modulates cortically
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induced rhythmic jaw movements and the activity of the jaw muscles.
2. Methods The experiments were carried out on 23 male Sprague–Dawley rats, weighing 306–401 g. All animal care protocols and surgical procedures were approved by the Laboratory Animal Committee of The Nippon Dental University School of Life Dentistry at Niigata. The animals were initially anesthetized with urethane (1 g/kg i.p.). Supplementary doses (0.2 g/kg) were given via a cannula placed in the femoral vein, to maintain anesthesia at a level that suppressed the withdrawal reflex evoked by noxious stimulation of the paw. The skin and muscles were infiltrated with 2% lidocaine. The trachea and the femoral artery were cannulated. Arterial blood pressure was monitored as a measure of the condition of the animal during the experiment. The rectal temperature was maintained at 37 ◦ C using a regulated heating pad. The anterior belly of the digastric and masseter muscles was exposed on the left or right side, and pairs of Teflon-coated silver wires (diameter 0.1 mm, exposed tip size 2 mm, inter-electrode distance 1.5 mm) were inserted in order to record the electromyograms (dEMG and mEMG, respectively). EMGs were recorded ipsilateral to the OfM stimulation. Activities in the dEMG and the mEMG were amplified (filter bandwidth: 10 Hz to 1 kHz). Jaw movements were recorded in the vertical and horizontal directions by a photodiode transducer that tracked the displacement of a light attached to the mandibular. The recording system was calibrated by attaching the light to an object for which the motion was known. The head was fixed in a stereotaxic apparatus, with ear bars and an incisal bar. Part of the frontal, parietal and interparietal bones was removed, using a dental drill to expose the cortical surface. A bipolar concentric electrode (inner electrode diameter 0.06 mm, outer electrode diameter 0.3 mm, interpolar distance 1 mm) was inserted vertically into the left or right OfM. Electrical stimulation (0.5 ms duration, 30 Hz, 50–250 A, 10 s) was applied to the OfM. The intensity of stimulation was set at the threshold for inducing rhythmic jaw movements. An indifferent electrode was placed on the exposed neck muscle. The cerebellum was removed by suction to expose the brainstem. A bipolar concentric electrode was inserted stereotaxically, vertically into the left or right VN. Stimulation (0.2 ms duration, 1 Hz, 100–130 A, 4 s) was applied to the VN ipsilateral to the OfM stimulation 6 s after the beginning of stimulation of the OfM, once the amplitude of jaw movements was stable. The stimulation site of the OfM was sites 1–4 in one rat. Three trials were performed at each stimulation site. A small screw was implanted into the nasal bone, and a metal rod was attached to the stereotaxic apparatus. The metal rod and screw were connected using acrylic resin. The incisal bar was taken out of the mouth so that the jaw could move freely. The rhythmic jaw movements and dEMG and mEMG were stored on a computer disk. A jaw movement cycle was defined to begin at the moment of maximum jaw opening (the start of the jaw-closing phase) and to end at the next maximum jaw opening. The distance between the maximum jaw-opening position and minimum jaw-opening position was measured for a single cycle. A horizontal movement cycle was defined to begin at the moment of maximum left jaw position (the start of the right movement phase) and to end at the next maximum left jaw position. The distance between the maximum right and left jaw position was also measured. The duration of a jaw movement cycle, the duration of a horizontal movement cycle, the distance between the maximum jaw-opening position and minimum jaw-opening position, and the distance between the
maximum right and left jaw position before the VN stimulation were taken as control values (100%), because the amplitude and frequency of jaw movements changed according to the stimulation sites in a single animal and between animals. We determined the percentage change in the duration of a cycle, the distance between the maximum jaw-opening position and minimum jaw-opening position, and the distance between the maximum right and left jaw position after VN stimulation. The EMG was full-wave rectified and averaged. As a control, the mean EMG activity and standard deviation (S.D.) were calculated for 5 s before the OfM stimulation. The onset of mEMG burst was defined as the instant when mEMG activity exceeded 2 S.D. from the control. Likewise, the offset was defined as the instant when mEMG activity fell below 2 S.D. from the control. The base line of the dEMG activity during the jaw-closing phase exceeded 2 S.D. from the control, however, so that the onset of dEMG burst was defined as the instants at which the dEMG activity exceeded 2 S.D. from the baseline. The duration of the EMG burst for which the perturbation occurred by stimulation of the VN is referred to as the perturbed duration. The duration of the EMG burst after the perturbed duration is termed the post-stimulus duration. The duration of the EMG burst immediately prior to the perturbed duration is referred to as the pre-stimulus duration. The durations of the mean perturbed duration and the post-stimulus duration are expressed as a percentage of the mean pre-stimulus duration (control). All data were analyzed for statistical significance by the Wilcoxon t-test (P < 0.05). At the end of each experiment, electric lesions were made by passing negative current (20 A, 30 s) through the stimulating electrode. The animals were then given a lethal dose of anesthetic, and the brain was perfused through the left cardiac ventricle with 0.9% saline followed by 10% buffered formalin solution (pH 7.4). Serial coronal sections of the brain were cut (50 m thick) and counterstained with cresyl violet. The stimulation sites were verified using the atlas of Paxinos and Watson (2007). 3. Results The threshold of the rhythmic jaw movements varied from 50 to 250 A. The characteristics of the jaw movement pattern and the EMG match those found in previous studies (Sasamoto et al., 1990; Satoh et al., 2006, 2007). The movements always began with opening of the jaw, and were followed by rhythmic movements which consisted of simple opening–closing movements. The frequency of rhythmic jaw movements was 5–7 Hz. Vertical movements were small and horizontal movement was very small. The uppermost position of the jaw movements was below the resting position of the jaw; as a result, the lower teeth did not come into contact with the upper teeth. There was no activity in the mEMG in the early stage of the jaw movements. Activity in the dEMG and mEMG showed bursts during the jaw-opening and the jaw-closing phase, respectively. The rhythmic jaw movements that were induced from the OfM exhibited a similar pattern in different animals, but the amplitude of these jaw movements varied with stimulation site in a single animal and between animals. The sites for electrical stimulation are similar to those in our previous study (Satoh et al., 2007). 3.1. MVNPC Stimuli applied in the jaw-closing phase increased the amplitude of the jaw-closing movement (which is incomplete and does not proceed to complete closure) in all cases (5 rats). The amplitude of the horizontal movements increased ipsilaterally with the OfM stimulation (Fig. 1A). Of 96 cases, 81 increased the amplitude of
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Fig. 1. Effect of stimulation of the right MVNPC (0.2 ms duration, 1 Hz, 130 A, 4 s) on the rhythmic jaw movements induced by stimulation of the right OfM (0.5 ms duration, 30 Hz, 60 A, 10 s). The arrow indicates the moment of stimulation to the MVNPC. HORZ: horizontal jaw movements (left down); VERT: vertical jaw movements (opening down); dEMG and mEMG: electromyographic activities of the anterior belly of the digastric muscle and masseter muscle on the right side. (A) Example of the recording. (B) EMGs were rectified and averaged in eight stimuli in the jaw-closing phase. (C) EMGs were rectified and averaged in four stimuli in the jaw-opening phase.
the horizontal movements and 15 did not modulate it. There was a significant difference (P < 0.05) before and after stimulation of the MVNPC in the distance from the maximum to the minimum jawopening position, and in the distance from the maximum left to maximum right positions (Table 1). The rhythm of the jaw movements was altered slightly. The duration of a jaw movement cycle after stimulation of the MVNPC was increased to 108.7 ± 11.2% (mean ± S.D., n = 96) of the value in controls. The duration of the horizontal movement was lengthened to 105.1 ± 8.9% (mean ± S.D.,
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n = 96) of the value in controls. There was a significant difference (P < 0.05) in the duration of the jaw movement cycle and the horizontal movement before and after stimulation of the MVNPC. These effects were induced transiently in one cycle of vertical and horizontal jaw movements. The duration of activity in the mEMG was increased (Fig. 1B). The perturbed duration in the mEMG rose to 118.4 ± 15.1% (mean ± S.D., n = 96). There was significant difference between the pre-stimulus duration and the perturbed duration (P < 0.05). On the other hand, the post-stimulus duration in the mEMG was 100.1 ± 7.9% (mean ± S.D., n = 96). There was no significant difference between the pre-stimulus duration and the post-stimulus duration (P > 0.05). Stimuli applied in the jaw-opening phase disturbed the rhythm of jaw movements in all cases (5 rats). A small jaw-closing movement was induced at 4.0–11.0 ms (6.4 ± 1.8 ms, mean ± S.D., n = 41) after the stimulation of the MVNPC. The distance from the maximum to the minimum jaw-opening position after stimulation of the MVNPC fell (Fig. 1A). There was a significant difference (P < 0.05) in the distance before and after stimulation of the MVNPC (Table 1). The duration of a jaw movement cycle after stimulation of the MVNPC rose to 120.0 ± 30.0% (mean ± S.D., n = 41) of the value in controls. The amplitude of the horizontal movements was unaffected, but the duration of the horizontal movement was lengthened to 109.3 ± 12.9% (mean ± S.D., n = 41) of the value in controls. There was a significant difference (P < 0.05) in the duration of a jaw movement cycle and the horizontal movement before and after stimulation of the MVNPC. These effects were induced transiently in one cycle of vertical and horizontal jaw movements. A transient burst and inhibitory period was induced in the mEMG and in the dEMG (Fig. 1C). The perturbed duration in the dEMG was significantly reduced to 70.6 ± 17.2% (mean ± S.D., n = 41) (P < 0.05). On the other hand, the post-stimulus duration in the dEMG was 101.6 ± 7.0% (mean ± S.D., n = 41). There was no significant difference between the pre-stimulus duration and the post-stimulus duration (P > 0.05). These results were consistent across the animals tested.
3.2. MVNMC Stimuli applied in the jaw-closing phase increased the amplitude of the jaw-closing movement in all cases (5 rats). The amplitude of the horizontal movements increased ipsilaterally with the OfM stimulation (Fig. 2A). Only 2 cases did not modulate the amplitude of the horizontal movements. There was a significant difference (P < 0.05) before and after stimulation of the MVNMC in the distance from the maximum to the minimum jaw-opening position, and from the maximum left to maximum right positions (Table 1). Also, the rhythm of the jaw movements was slightly altered. The duration of a jaw movement cycle after stimulation of the MVNMC was lengthened to 108.8 ± 12.9% (mean ± S.D., n = 70) of the value in controls. The duration of the horizontal movement was lengthened to 110.2 ± 10.7% (mean ± S.D., n = 70) of the value in
Table 1 Effect on the rhythmic jaw movements of stimulating the MVNPC, MVNPC, LVN, SVN and IVN. Stimulation sites
Vertical jaw movements Closing phase
MVNPC MVNMC LVN SVN IVN
130.9 141.1 101.0 102.0 97.7
± ± ± ± ±
24.9% (96)* 23.1% (70)* 5.6% (71) 7.9% (73) 9.2% (84)*
Horizontal jaw movements Opening phase 44.7 60.9 112.9 115.1 85.3
± ± ± ± ±
21.7% (41)* 24.2% (52)* 17.1% (51)* 17.1% (63)* 11.1% (80)*
Closing phase 126.8 181.7 102.7 99.2 96.5
± ± ± ± ±
27.3% (96)* 46.5% (70)* 12.9% (71) 12.0% (73) 17.4% (84)*
Opening phase 101.9 140.2 103.3 103.8 85.9
± ± ± ± ±
13.2% (41) 30.4% (52)* 13.5% (51) 14.3% (63) 20.8% (80)*
Values are mean ± S.D. Values in the parenthesis indicate numbers. * Significant difference before and after stimulation of the VN (P < 0.05, Wilcoxon’s t-test) in the distance from the maximum jaw-opening position to the minimum jaw-opening position, or in the distance from the maximum right to the maximum left jaw position.
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Fig. 2. (A) Effect of stimulation of the right MVNMC (0.2 ms duration, 1 Hz, 130 A, 4 s) on the rhythmic jaw movements induced by stimulation of the right OfM (0.5 ms duration, 30 Hz, 120 A, 10 s). (B) EMGs were rectified and averaged in seven stimuli in the jaw-closing phase. (C) EMGs were rectified and averaged in five stimuli in the jaw-opening phase. Other details are as in Fig. 1.
Fig. 3. (A) Effect of stimulation of the left LVN (0.2 ms duration, 1 Hz, 130 A, 4 s) on the rhythmic jaw movements induced by stimulation of the left OfM (0.5 ms duration, 30 Hz, 100 A, 10 s). (B) EMGs were rectified and averaged in six stimuli in the jaw-closing phase. (C) EMGs were rectified and averaged in six stimuli in the jaw-opening phase. Other details are as in Fig. 1.
controls. There was a significant difference (P < 0.05) in the duration of the jaw movement cycle, and the horizontal movement, before and after stimulation of the MVNMC. These effects were induced transiently in one cycle of vertical and horizontal jaw movements. The amplitude of activity was increased in the mEMG (Fig. 2B). The perturbed duration in the mEMG was significantly increased to 115.3 ± 13.4% (mean ± S.D., n = 70) (P < 0.05). The post-stimulus duration in the mEMG was 99.8 ± 7.4% (mean ± S.D., n = 70), however. There was no significant difference between the pre-stimulus duration and the post-stimulus duration (P > 0.05). Stimuli applied in the jaw-opening phase disturbed the rhythm of jaw movements in all cases (5 rats). A small jaw-closing movement was induced at 5.0–15.0 ms (8.4 ± 1.7 ms, mean ± S.D., n = 52) after the MVNMC stimulation. The small horizontal movement induced was ipsilateral to the OfM stimulation (Fig. 2A). There was a significant difference (P < 0.05) before and after stimulation of the MVNMC in the distance from the maximum to the minimum jaw-opening position, and from the maximum left to maximum right positions (Table 1). The duration of a jaw movement cycle after stimulation of the MVNMC increased to 108.0 ± 10.1% of the value in controls (mean ± S.D., n = 52). The duration of the horizontal movement increased to 113.4 ± 13.5% (mean ± S.D., n = 52) of the value in controls. There was a significant difference (P < 0.05) in the duration of the jaw movement cycle and in the horizontal movement before and after stimulation of the MVNMC. These effects were induced transiently in one cycle of vertical and horizontal jaw
movements. A transient burst was induced in the mEMG (Fig. 2C). The perturbed duration in the dEMG was reduced significantly, to 68.8 ± 22.1% (mean ± S.D., n = 52) (P < 0.05). The post-stimulus duration in the dEMG was 100.8 ± 11.6% (mean ± S.D., n = 52). There was no significant difference between the pre-stimulus duration and the post-stimulus duration (P > 0.05). These results were consistent across the animals tested. 3.3. LVN Stimuli applied in the jaw-closing phase did not modulate the amplitude of the jaw-closing and the jaw-opening movement (Fig. 3A). There was no significant difference (P > 0.05) in the distance from the maximum to the minimum jaw-opening position before and after stimulation of the LVN (Table 1). Also, the rhythm of the jaw movements was unchanged. The duration of a jaw movement cycle after stimulation of the LVN was 102.4 ± 10.6% (mean ± S.D., n = 71) of the value in controls. There was no significant difference (P > 0.05) in the duration of the jaw movement cycle before and after stimulation of the LVN. The amplitude and duration of the horizontal movements and of the activity in the EMG were unaffected (Fig. 3A and B). Stimuli applied in the jaw-opening phase increased the amplitude of the jaw-opening movement in 41 cases (6 rats) (Fig. 3A). 10 cases did not modulate the amplitude of the jaw-opening movement. There was a significant difference (P < 0.05) in the distance
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Fig. 4. (A) Effect of stimulation of the left SVN (0.2 ms duration, 1 Hz, 130 A, 4 s) on the rhythmic jaw movements induced by stimulation of the left OfM (0.5 ms duration, 30 Hz, 130 A, 10 s). (B) EMGs were rectified and averaged in six stimuli in the jaw-closing phase. (C) EMGs were rectified and averaged in six stimuli in the jaw-opening phase. Other details are as in Fig. 1.
from the maximum to the minimum jaw-opening position before and after stimulation of the LVN (Table 1). This effect was induced transiently in one cycle of vertical and horizontal jaw movements. The rhythm of the jaw movements was unchanged, however. The duration of the jaw movement cycle after stimulation of the LVN was 102.0 ± 9.4% (mean ± S.D., n = 51) of the value in controls. There was no significant difference (P > 0.05) in the duration of the jaw movement cycle before and after stimulation of the LVN. The amplitude and duration of the horizontal movement and of the activity in the EMG were unaffected (Fig. 3A and C). These results were consistent across the animals tested. 3.4. SVN Stimuli applied in the jaw-closing phase did not modulate the amplitude of the jaw-closing movement and the jaw-opening movement (Fig. 4A). There was no significant difference (P > 0.05) in the distance from the maximum to the minimum jaw-opening position before and after stimulation of the SVN (Table 1). Also, the rhythm of the jaw movements was unchanged. The duration of the jaw movement cycle after stimulation of the SVN was 102.0 ± 7.9% (mean ± S.D., n = 73) of the value in controls. There was no significant difference (P > 0.05) in the duration of the jaw movement cycle before and after stimulation of the SVN. The amplitude and duration of the horizontal movements and of the activity in the EMG were unaffected (Fig. 4A and B).
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Fig. 5. (A) Effect of stimulation of the right IVN (0.2 ms duration, 1 Hz, 130 A, 4 s) on the rhythmic jaw movements induced by stimulation of the right OfM (0.5 ms duration, 30 Hz, 85 A, 10 s). (B) EMGs were rectified and averaged in five stimuli in the jaw-closing phase. (C) EMGs were rectified and averaged in seven stimuli in the jaw-opening phase. Other details are as in Fig. 1.
Stimuli applied in the jaw-opening phase increased the amplitude of the jaw-opening movement in 51 cases (6 rats) (Fig. 4A). 12 cases did not modulate the amplitude of the jaw-opening movement. There was a significant difference (P < 0.05) in the distance from the maximum to the minimum jaw-opening position before and after stimulation of the SVN (Table 1). Also, the rhythm of the jaw movements was altered slightly. The duration of the jaw movement cycle after stimulation of the SVN was lengthened to 105.2 ± 10.9% (mean ± S.D., n = 63) of the value in controls. There was a significant difference (P < 0.05) in the duration of the jaw movement cycle before and after stimulation of the SVN. These effects were induced transiently in one cycle of vertical and horizontal jaw movements. The amplitude and duration of the horizontal movements and of the activity in the EMG were unaffected (Fig. 4A and C). These results were consistent across the animals tested. 3.5. IVN Stimuli applied in the jaw-closing phase reduced the amplitude of the jaw-closing movement in 51 cases (3 rats). 33 cases did not modulate the amplitude of the jaw-closing movement. The amplitude of the horizontal movements decreased slightly in 53 cases (Fig. 5A). 31 cases did not modulate the amplitude of the horizontal movements. There was a significant difference before and after stimulation of the IVN (P < 0.05) in the distance from the maximum
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Fig. 6. Diagrammatic representation of the stimulating sites. Filled circles indicate that stimuli during the jaw-closing phase increase the amplitude of the jaw-closing movement and stimuli during the jaw-opening phase induced a small jaw-closing movement. Open circles indicate that stimuli in the jaw-opening phase increase the amplitude of the jaw-opening movement. Triangles indicate that stimuli in the jaw-closing and the jaw-opening phase reduced the amplitudes of the jaw-closing and jawopening movements, respectively. Squares indicate ineffective sites. The number associated with each diagram represents the level of the coronal section from the bregma in mm; – signs denote caudal to the bregma. Abbreviations: MVNPC, medial vestibular nucleus, parvicellular part; MVNMC, medial vestibular nucleus, magnocellular part; SVN, superior vestibular nucleus; LVN, lateral vestibular nucleus; IVN, inferior vestibular nucleus; scp, superior cerebellar peduncle; icp, inferior cerebellar peduncle; veme, vestibulomesencephalic tract; vesp, vestibulospinal tract; Pr, prepositus nucleus; Sol, solitary tract; 7n, facial nerve; g7, genu of the facial nerve, asc 7, ascending fibers of the facial nerve; 8vn, vestibular root of the vestibulocochlear nerve.
to the minimum jaw-opening position, and from the maximum left to maximum right position (Table 1). These effects were induced transiently in one cycle of vertical and horizontal jaw movements. The rhythm of the jaw movements was unchanged, however. The duration of the jaw movement cycle after stimulation of the IVN was 98.2 ± 10.1% (mean ± S.D., n = 84) of the value in controls. There was no significant difference (P > 0.05) in the duration of the jaw movement cycle before and after stimulation of the IVN. The duration of horizontal movement and the activity in the EMG were unaffected (Fig. 5A and B). Stimuli applied in the jaw-opening phase reduced the amplitude of the jaw-opening movement in 73 cases (3 rats). 7 cases did not modulate the amplitude of the jaw-opening movement. The amplitude of the horizontal movements decreased in 64 cases (Fig. 5A). 16 cases did not modulate the amplitude of the horizontal movements. There was a significant difference (P < 0.05) before and after stimulation of the IVN in the distance from the maximum to the minimum jaw-opening position, and from the maximum left to maximum right position (Table 1). Also, the rhythm of the jaw movements was altered slightly. The duration of the jaw movement cycle after stimulation of the IVN increase to 104.2 ± 10.7% (mean ± S.D., n = 80) of controls. There was a significant difference (P < 0.05) in the duration of the jaw movement cycle before and after stimulation of the IVN. These effects were induced transiently in one cycle of vertical and horizontal jaw movements. The duration of horizontal movement and the activity in the EMG were unaffected (Fig. 5A and C). These results were consistent across the animals tested.
3.6. Outside the VN Stimuli applied in the jaw-closing phase did not modulate the amplitude of the jaw-closing movement or the jaw-opening movement. The distance from the maximum to the minimum jawopening position after stimulation outside the VN was 100.7 ± 6.3% (mean ± S.D., n = 53) of the value in controls. The duration of the jaw movement cycle after stimulation outside the VN was 103.7 ± 8.5% (mean ± S.D., n = 53) of the value in controls. Stimuli applied in the jaw-opening phase did not modulate the amplitude of the jaw-closing movement or the jaw-opening movement. The distance from the maximum to the minimum jawopening position after stimulation outside the VN was 99.6 ± 10.6% (mean ± S.D., n = 41) of the value in controls. The duration of the jaw movement cycle after stimulation outside the VN was 102.6 ± 10.7% (mean ± S.D., n = 41) of the value in controls. There was no significant difference (P > 0.05) in these values before and after stimulation outside the VN. The amplitude and duration of the horizontal movements and of the activity in the EMG were unaffected. These results were consistent across the animals tested. The electrical stimulation sites of the VN are shown in Fig. 6 on diagrams of the transverse section. 4. Discussion Stimuli applied to the MVN in the jaw-closing phase increased the amplitude of the jaw-closing movement, whereas stimuli applied to the MVN in the jaw-opening phase disturbed the rhythm
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of jaw movements and induced a small jaw-closing movement. This result was unexpected. Our previous study found that the JOR and the MMR was facilitated by stimulation of the MVN (Satoh et al., 2009a,b). We therefore suppose that stimuli applied in the jaw-opening phase increase the amplitude of the jaw-opening movement. Rhythmic jaw movements always begin with sustained jaw-opening and consist of simple opening–closing movements of the jaw. In all cases the jaw remained at a level below the resting position during the rhythmic jaw movements. Consequently, the excitability of the jaw-opening motoneurons may not be enhanced during the jaw-opening phase upon stimulation of the MVN, and the jaw-closing movement occurred preferentially during jaw movements. Stimuli applied to the LVN and the SVN in the jaw-closing phase and in the jaw-opening phase did not modulate the amplitude of the jaw-closing movement, and increased the amplitude of the jawopening movement. The jaw-closing and the jaw-opening muscles are regarded as the equivalents of the extensor and the flexor muscles of the limbs, respectively, since noxious stimulation of the orofacial region evokes the JOR via one or more interneurons, and the MMR is evoked by muscle spindle afferents in the jaw-closing muscles (Dessem et al., 1988; Nakamura et al., 1973; Sumino, 1971). Stimulation of the LVN during the standing phase of locomotion, when the extensor muscles are active, enhances activity in the ipsilateral extensor muscles. Stimulation of the LVN during the swing phase, when the flexor muscles are active, has little effect (Orlovsky, 1972a; Russel and Zajac, 1979). We therefore suggest that the functional role of the LVN is not analogous in jaw movements and in locomotion. Stimuli applied to the IVN in the jaw-closing and the jawopening phase reduced the amplitude of the jaw-closing and the jaw-opening movement, respectively. These results could be related to physiological findings in our previous studies that the JOR and the MMR are inhibited by stimulation of the IVN (Satoh et al., 2009a,b). Stimulation of the MVN and the IVN, especially the MVNMC, affected horizontal movements of the jaw (Table 1). This suggests that the effects of the MVN and the IVN manifest at the unilateral jaw muscles. No such phenomena were observed, however, when stimulation was applied to the LVN and the SVN, suggesting that the effects of the LVN and the SVN manifest at the bilateral jaw muscles. When horizontal movements are made in humans, the lateral pterygoid muscle (jaw-opening muscle), the medial pterygoid muscle (jaw-closing muscle) on the contralateral side, and the posterior portion of the temporal muscle (jaw-closing muscle) on the ipsilateral side to rotation direction are all active (Mahan et al., 1983; Miller, 1991; Murray et al., 1999). Lateral pterygoid muscle activity in the rat appears to show the same basic pattern as in humans (Byrd and Chai, 1988). As a result, stimulation of the MVN and the IVN affected these muscles. This suggestion is supported by the morphological studies. The LVN and the SVN project bilaterally to the SpV oralis (SpVO) and the interporalis (SpVI). However, the MVN and the IVN project bilaterally to the dorsal part of the SpVO and the entire of the SpVI with ipsilateral dominance. The MVN projects bilaterally to the intermediate part of the SpVO with contralateral or ipsilateral dominance (Buisseret-Delmas et al., 1999). The dorsal part of the SpVO and the SpVI project bilaterally to the jaw-closing motoneurons with ipsilateral dominance, whereas the intermediate part of the SpVO and the SpVI project bilaterally to the jaw-opening motoneurons with ipsilateral dominance (Li et al., 1995). Stimulation of the VN induced transient effects, and had no effect on the onset and cessation of cycle of jaw movements. This suggests that effects of the VN stimulation act on only output side from the central pattern generator of the rhythmic jaw movements or from the premotor neurons projecting to the trigeminal motor
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nucleus, and do not directly influence the central pattern generator of the rhythmic jaw movements. The cycle duration of the jaw movements was altered by stimulation of the MVN. It was also slightly altered by stimulation of the SVN and the IVN in the jaw-opening phase. In guinea pigs, the output from the cortical masticatory area descends to the nucleus reticularis paragigantocellularis via the corticobulbar fibers. The output from the nucleus reticularis paragigantocellularis runs in turn to the nucleus reticularis gigantocellularis (Nozaki et al., 1986a,b). It has been reported that the central pattern generator of the rhythmic jaw movements is located in the medial bulbar reticular formation, including the nucleus reticularis gigantocellularis (Nozaki et al., 1986a). In the rat, the VN, especially the MVN, projects to the nucleus reticularis paragigantocellularis (Andrezik et al., 1981). The VN projects to the SpV in rats (Buisseret-Delmas et al., 1999; Diagne et al., 2006; Valla et al., 2003). The SpV is known to contain premotor neurons projecting to the trigeminal motor nucleus (Donga et al., 1990; Li et al., 1995; Olsson and Westberg, 1991; Westberg et al., 1995). Stimulation of the contralateral trigeminal motor nucleus antidromically activates neurons in the SpVO (Donga et al., 1990). These neurons were almost all activated by stimulating the cortical masticatory area after a short latency, and most showed rhythmic activity during cortically induced fictive mastication (Donga and Lund, 1991). The VN stimulation may therefore influence these premotor neurons in the SpV and the nucleus reticularis paragigantocellularis, and alter the rhythm of jaw movements. The pathways from the OfM to the VN have been revealed by morphological studies. The OfM neurons project to the dorsal part of the trigeminal sensory complex (Zhang and Sasamoto, 1990). The VN receives fibers from the SpV (Buisseret-Delmas et al., 1999; Diagne et al., 2006; Valla et al., 2003). It may therefore be assumed that the VN receives inputs from the OfM via these pathways. In conclusion, the present study has shown that stimuli applied to the VN influence the rhythmic jaw movements induced by stimulation of the OfM. We suggest that the VN is involved in modulating the rhythmic jaw movements induced by stimulation of the OfM, and is related to the control of jaw movements. The physiological role of the VN in regulating the rhythmic jaw movements appears to be the coordination between the jaw-opening movement, the jaw-closing movement and the lateral movement of jaw. Acknowledgments This study was partly supported by Research Promotion Grant (NDUF-09-01) from The Nippon Dental University and by Grantsin-Aid for Scientific Research from the Ministry of Education, Culture, Sports, Science and Technology of Japan (#22592079). References Andrezik, J.A., Chan-Palay, V., Palay, S.L., 1981. The nucleus paragigantocellularis lateralis in the rat. Anat. Embryol. 161, 373–390. Buisseret-Delmas, C., Compoint, C., Delfini, C., Buisseret, P., 1999. Organisation of reciprocal connections between trigeminal and vestibular nuclei in the rat. J. Comp. Neurol. 409, 153–168. Byrd, K.E., Chai, Y., 1988. Three-dimensional movement analysis of lateral pterygoid electromyographic activity during mastication in the rat. Arch. Oral Biol. 33, 635–640. Cuccurazzu, B., Deriu, F., Tolu, E., Yates, B.J., Billing, I., 2007. A monosynaptic pathway links the vestibular nuclei and masseter muscle motoneurons in rats. Exp. Brain Res. 176, 665–671. Dellow, P.G., Lund, J.P., 1971. Evidence for central timing of rhythmical mastication. J. Physiol. 215, 1–13. Dessem, D., Iyadurai, O.D., Taylor, A., 1988. The role of periodontal receptors in the jaw-opening reflex in the cat. J. Physiol. 406, 315–330. Diagne, M., Valla, J., Delfini, C., Buisseret-Delmas, C., Buisseret, P., 2006. Trigeminovestibular and trigeminospinal pathways in rats: retrograde tracing
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