- Email: [email protected]
Influence of jaw gape on EMG of jaw muscles and jaw-stretch reflexes
archives of oral biology 52 (2007) 562–570
available at www.sciencedirect.com
journal homepage: www.intl.elsevierhealth.com/journals/arob
Influence of jaw gape on EMG of jaw muscles and jaw-stretch reflexes Kelun Wang a,*, Frank Lobbezoo b, Peter Svensson a,c, Lars Arendt-Nielsen a a
Center for Sensory-Motor Interaction, Orofacial Pain Laboratory, Aalborg University, Denmark Department of Oral Function, Academic Centre for Dentistry Amsterdam (ACTA), Louwesweg 1, 1066 EA Amsterdam, The Netherlands c Department of Clinical Oral Physiology, School of Dentistry, University of Aarhus, Denmark b
article info
abstract
Article history:
The influence of jaw gapes on jaw-stretch reflexes and jaw muscles activity was studied in
Accepted 5 December 2006
order to test the sensitivity of human muscle spindle afferents in various jaw muscles.
Keywords:
latency excitatory reflex responses were evoked by a custom-made stretch device with the
Human
subjects biting on a jaw-bar with their front teeth. Surface electromyographic (sEMG)
Jaw gape
recordings from right masseter (MAR), and right temporalis (TAR), intramuscular EMG
Stretch reflex
(imEMG) recordings from right lateral pterygoid (LPR) and right anterior digastric (ADR)
Jaw muscle
muscles were made. The reflex at different jaw gapes of 6, 10, 14, 18, 22, 26, 30, 34, and 38 mm
EMG
were examined in random order with standard stretch conditions of 1 mm displacement
Twelve healthy men (mean age S.E.M.: 25.0 1.2 yr) participated in the study. Short-
and 10 ms ramp time. Twenty sweeps of the reflex were recorded at each level with at least 5 s interval between each sweep with online monitoring of the visual feed back at 15% of maximum voluntary contraction (MVC) of each jaw gape from MAR. The results showed that the peak-to-peak amplitude of the jaw-stretch reflex in MAR was significantly higher at 14 mm compared to 30, 34, and 38 mm (P < 0.038), whereas the reflex amplitude in TAR increased with jaw gape until a maximum at 34 mm. There was no significant effect of jaw gape in LPR muscles (P = 0.825) and no obvious stretch reflex was observed in ADR. When the amplitude was normalised to the pre-stimulus EMG at each jaw gape, the highest normalised amplitude was observed at 14 mm jaw gape in MAR, however there was no significant effect of jaw gape on the normalised amplitude in TAR and LPR. In addition, masseter EMG at MVC significantly decreased with the increase of the gapes, i.e. biting at 6, 14, and 18 mm gapes had a significantly higher MVC compared to 26, 30, 34, and 38 mm (ANOVA: P < 0.013). It is concluded that the jaw gapes influence the sensitivity of the human muscle spindle afferents in jaw-closing muscles with a distinct peak, which is within normal jaw gapes during function. # 2006 Elsevier Ltd. All rights reserved.
1.
Introduction
A sudden stretch of the jaw-closing muscles can elicit a shortlatency excitatory response in the muscles, the so-called
stretch reflex. The modulation of the stretch reflex in jawclosing muscle has been studied previously.1–8 The human jaw-closing muscles are richly endowed with muscle spindles, and the spindle afferents make excitatory connections to the
* Corresponding author at: Center for Sensory-Motor Interaction, Orofacial Pain Laboratory, Aalborg University, Fredrik Bajers Vej 7 D-3, DK-9220 Aalborg S, Denmark. Tel.: +45 9635 8745; fax: +45 9815 4008. E-mail address: [email protected] (K. Wang). 0003–9969/$ – see front matter # 2006 Elsevier Ltd. All rights reserved. doi:10.1016/j.archoralbio.2006.12.004
archives of oral biology 52 (2007) 562–570
motoneurons of jaw-closing muscles.9 The stretch reflex plays a significant role in the modulation of activity of jaw-closing muscles.10,11 In a number of orofacial muscles, in particular, the lateral pterygoid muscle and anterior digastric muscles, few muscle spindles have been reported.12 Even though the stretch reflex-like response has also been observed in the lateral pterygoid muscle in cats13 and humans,14 it has, however, been suggested that the stretch reflex plays a minimal role in the regulation of the jaw-opening muscles (see Luschei and Goldberg, 1981 for summary15). A recent study suggested that the stretch reflex-like response, elicited in the human lateral pterygoid muscle, is probably a monosynaptic reflex triggered by muscle spindles.16 The lateral pterygoid muscle has been suggested to play a role in parafunctional excursive jaw movements and also possibly a role in influencing jaw position during jaw movement (for a review see: 17,18). In addition, a study has demonstrated phasic and tonic stretch reflexes in human jaw-opener muscles, which have few muscle spindles.19 The results suggested that spindle afferents in jaw-opening muscles might be sufficient in number to provide the observed patterns of responses, and non-spindle afferents such as free nerve endings in the opening muscles might contribute as well.19 Further studies on stretch reflex activity in the lateral pterygoid muscle and anterior digastric muscles during different jaw gapes may help to increase the insight into the purported role in regulation of the activity in these muscles, especially at wider jaw gapes. Methodological differences in clinical neurophysiology may unfortunately contribute to contradictory views about the behaviour of jaw-stretch reflexes. For example, the amplitude of the jaw-stretch reflex may be influenced by the displacement and velocity of the mandibular movement evoked by the stretcher.7 The level of background EMG activity as well as the specific biting task10,20 has also been shown to influence the stretch reflex amplitude. In our previous study, we found that an increase in jaw gape by 2.5 mm resulted in significantly larger stretch reflex amplitudes compared with the initial jaw gape.7 Lobbezoo et al.2 on the other hand, did not find an effect on the jaw-stretch reflex amplitude of increases in jaw gape by 1 and 2 mm on top of the initial 3 mm. However, only two subjects were tested in that study, which makes it difficult to extrapolate their finding to the other studies. Van der Bilt et al.20 studied the modulation of the jaw-stretch reflex during rhythmic openclose movements. They found larger reflex amplitudes at a jaw gape of about 20 mm than at smaller jaw gapes during the opening phase. However, the reflex amplitudes were not correlated with jaw gape during the jaw closing phase. In a recent study, we found that there is a significant effect of jaw gape for the masseter and anterior temporalis muscles, with the 14-mm gape having the highest amplitude.4 In that study, we investigated the situation at only three different gapes, viz., 4, 14, and 24 mm. The tendency of the sensitivity changes of the stretch reflex during the change of jaw gapes has been not fully shown. Therefore the relationship between jaw gape and stretch reflex amplitude is still not fully clear. Thus, the purpose of this study was to investigate the influence of different jaw gapes on the jaw-stretch reflex in the jaw-closing muscles, as to provide further insight into the properties of the human muscle spindle afferents. The
563
influence on the EMG activity in the lateral pterygoid and anterior digastric muscles was also investigated.
2.
Materials and methods
2.1.
Subjects
The volunteers for this study were all healthy and unmedicated subjects without signs or symptoms of temporomandibular disorders (TMD).21 All subjects had natural dentitions (28 teeth) without significant malocclusion. Twelve men (mean age S.E.M.: 25.0 1.2 yr) participated in the experiment. The study was conducted in accordance with the Helsinki Declaration and informed consent was obtained from all subjects. The study was approved by the local Ethics Committee.
2.2.
Jaw-muscle stretcher
Stretch reflexes were evoked in the jaw muscles with a muscle stretcher based on that described by Miles et al.22 A stainlesssteel jaw-bar was mounted on a frame attached to the floor. A powerful electromagnetic vibrator (Model 406; Ling Dynamic Systems Ltd., Royston, UK) imposed servo-controlled displacements of the lower jaw-bar. A 200 N load cell (Kistler 5039 A312; Winterthur, Switzerland), mounted in series with the moveable probe of the vibrator, measured forces on the lower jaw-bar. The displacement of the vibrator probe was measured with a linear potentiometer (Sakae Type 20 FLP 30A-5K; Kawasaki, Japan), mounted in parallel with the probe. Acceleration in the vertical plane was measured by an accelerometer (Delta Tron Accelerometer Type 4399; Bruel & Kjær, Nærum, Denmark), mounted on the lower jaw-bar. The lower jaw-bar displaces down linearly 1 mm with a ramp time 10 ms when the program is triggered (see Section 2.4). The subjects were instructed to bite on the jaw-bar with their incisors during the recordings. Thus, the initial jaw separation for the subjects was determined by the distance between the upper and lower jaw-bar, which corresponded to 6.0 mm.
2.3.
Experimental protocol
Surface electromyographic (sEMG) recordings from the right masseter (MAR) and right temporalis (TAR) muscles, as well as intramuscular EMG (imEMG) recordings from the right lateral pterygoid (LPR) and right anterior digastric (ADR) muscles were made. The stretch reflexes at nine different jaw gapes of 6, 10, 14, 18, 22, 26, 30, 34, and 38 mm were examined in random order, with standard stretch conditions of 1 mm displacement and 10 ms ramp time. All jaw-stretch reflex recordings were examined with the subject biting with the incisors on the bars of the stretcher in a central position and without mandibular deviation.
2.4.
Recordings of jaw-stretch reflex
The sEMG activity was recorded with use of bipolar disposable surface electrodes (4 mm 7 mm recording area, 720-01-k,
564
archives of oral biology 52 (2007) 562–570
Neuroline; Medicotest, Ølstykke, Denmark) placed 10 mm apart along the central part of the MAR and the TAR muscles. The skin over the recording positions was cleaned with alcohol. The imEMG was recorded with a pair of fine wire electrodes (Ø 80 mm, Medwire, USA), uninsulated 1 mm at the tip and aimed to be inserted into the inferior head of right lateral pterygoid muscle and into the anterior belly of the right digastric muscle via a 23G needle (Microlance, Spain). The intraoral technique for electrode placement in the inferior head was modified from Wood et al.23 The needle was inserted through the oral mucosa above the level of the upper second molar, and advanced to contact the middle third of the lateral surface of the lateral pterygoid plate. The needle was withdrawn, leaving the wires within the inferior head, and the
wires were secured to the buccal surface of the upper first molar and led out through the angle of the mouth, then the wires were fixed by a piece of tape. To record the imEMG of the anterior digastric muscle, the needle was inserted 15 mm through the skin about 1 cm medial and inferior to the lower border of the mandible 4–5 cm from the chin below the region of the first and second mandibular molar.24,25 The location of the intramuscular electrodes was confirmed after withdrawal of the needle by observing the EMG when subjects performed a series of jaw-opening and jaw-protruding movement. The EMG signals were amplified 2000–5000 times (Counterpoint MK2, DK), filtered with bandpass 20 Hz to 1 kHz, sampled at 4 kHz, and stored for off-line analysis. The subjects were initially asked to perform 3 maximal clenches at the intercuspal position each lasting up to 3 s to record the EMG at maximal voluntary contraction (MVC-EMG). Then subjects were asked to bite on the jaw-bar with their incisors. The stretch reflexes were evoked in blocks of 20 sweeps at 9 different jaw gapes in random order varying from 4 mm (i.e. 6, 10, 14, 18, 22, 26, 30, 34, and 38 mm). Before each block of recordings, subjects were asked to make a maximal voluntary biting (MVB) with their incisor teeth on the jaw-bar of the stretch device to obtain the individual MVB-EMG value at each jaw gape in the four muscles. The sEMG activity recorded from the MAR muscle subsequently served for visual feedback (see below). The MVB-EMG recorded from MAR at the start of the each block was used to construct a window of 10% below and above the 15% MVB-EMG level (i.e. 13.5–16.5% MVBEMG). To help subjects achieve this, online calculation of the root-mean-square (RMS) value in 200 ms intervals was performed. The subjects received visual feedback from markers on the computer screen, which changed from green to red upon crossing the upper and lower limits of the window.26 The program automatically triggered the muscle stretcher when the EMG activity remained within the pre-set window for more than 400 ms. A total of 300 ms EMG activity was recorded with 100 ms pre-stimulus and 200 ms poststimulus (Fig. 1). Twenty sweeps of the reflex were recorded at each gape with at least 5 s interval between each sweep (around 0.2 Hz).
2.5.
Fig. 1 – Averaged reflex responses (20 sweeps) in four jaw muscles evoked by jaw-stretches in a single subject. The dotted line shows the onset of the stretch stimulus. (A) Surface EMG recording from right masseter muscle (MAR). Arrows show the onset and offset of reflex. The amplitude was measured as the peak-to-peak value of the positive and negative potential. (B) The reflex response recorded from surface EMG of right temporalis muscles (TAR). (C) The reflex response from intramuscular recording of right lateral pterygoid muscle (LPR). (D) Intramuscular recording from right anterior digastric muscle (ADR). (E) Displacement signal of the stretch with 1 mm displacement and 10 ms ramp.
Analysis
A special-purpose computer program (Aalborg University, Denmark) was used to analyse the jaw-stretch reflex responses. First, the mean EMG activity in the pre-stimulus interval ( 100 to 0 ms) of the averaged and rectified signal was calculated.3,5 The onset latency and peak-to-peak amplitude of the early reflex component, which appeared as a biphasic potential in the average of the non-rectified recordings, was measured (Fig. 1). The peak-to-peak amplitude was then normalised with respect to the mean pre-stimulus EMG activity observed at each stage of jaw gapes.
2.6.
Statistics
One-way and two-way analyses of variance (ANOVA) with repeated measures were performed and followed by pair-wise multiple comparison procedures (Student–Newman–Keuls, SNK). The factors in the ANOVA were experimental conditions
archives of oral biology 52 (2007) 562–570
565
(jaw gape level: 9 levels) and muscles (4 levels). The level of significance was set at P < 0.05. Mean values S.E.M. are presented in the text and figures.
3.
Results
3.1.
Influence of jaw gape on the amplitude of stretch reflex
The stretch reflex was successfully recorded with sEMG from MAR and TAR, and with imEMG from LPR muscles at all different jaw gapes in all subjects. However, the stretch reflex could not be recorded from the ADR in most subjects: although it was clearly seen in two subjects. Therefore, the stretch reflex in ADR was not further analysed in this study. In the MAR muscle, the peak to peak amplitude of the jawstretch reflex was highest at 14 mm when compared to 30, 34, and 38 mm (ANOVA: P < 0.038). The amplitude was lowest at 38 mm, i.e. the biggest gape, when compared to all other jaw gapes (P < 0.044) except 30 and 34 mm (Fig. 2A). In the TAR muscle, the reflex amplitude increased with increase in jaw gape, with a peak at 34 mm, after which it decreased again at 38 mm. The amplitude recorded at 30 and 34 mm was significantly higher than that at 6, 10, and 14 mm (ANOVA: P < 0.010), and higher at 26 mm compared to 6 and Fig. 3 – Influence of jaw gapes on the normalised amplitude of stretch reflex. ‘‘Amplitude (100%)’’ (ordinate) represents the normalised peak-to-peak amplitude to the prestimulus EMG. The normalised reflex amplitude was from surface EMG of MAR and TAR, and from intramuscular EMG of LPR. The feedback was derived from the surface EMG of the MAR. Mean values + S.E.M. (n = 12). *Significant difference between conditions (SNK: P < 0.05).
10 mm (P < 0.007). It was also significantly higher at 22 and 38 mm compared to 6 mm (P < 0.012) (Fig. 2B). There was no significant effect of the jaw gape on the stretch amplitude in the LPR muscle (ANOVA: P = 0.825) (Fig. 2C). When the amplitude was normalised to the pre-stimulus EMG at each jaw gape, the highest normalised amplitude was observed at 14 mm jaw gape in the MAR. It was significantly higher compared to 6 mm (ANOVA: P = 0.03) (Fig. 3A). No significant effect of jaw gape on the normalised amplitude was observed in TAR and LPR muscles (ANOVA: P > 0.381) (Fig. 3B and C).
3.2. Influence of jaw gape on the latency and duration of the stretch reflex Fig. 2 – Influence of jaw gapes on the amplitude of the stretch reflex. The reflex response was from surface EMG of MAR and TAR, and from intramuscular EMG of LPR. The feedback was derived from the surface EMG of the MAR. Mean values + S.E.M. (n = 12). *Significant difference between conditions (SNK: P < 0.05). Note the stretch reflex was only successfully recorded from ADR in 2 out of 12 subjects.
The overall mean values of the latency were: 8.9 0.3 ms in MAR, 8.4 0.3 ms in TAR, and 7.6 0.3 ms in LPR, respectively. There was no significant effect of jaw gape on the latency of the stretch reflex in any jaw muscle (ANOVA: P > 0.213). The duration of the reflex (overall average: 9.2 2.1 ms) was significantly longer at the 38 mm jaw gape compared to 6, 10, 14, 18, 20, 24, and 28 mm jaw gapes (ANOVA: P < 0.030) in the MAR muscle (Fig. 4A). The duration was significantly
566
archives of oral biology 52 (2007) 562–570
Fig. 4 – Influence of jaw gapes on the duration of stretch reflex in surface EMG of MAR and TAR, and in intramuscular EMG of LPR. Mean values + S.E.M. (n = 12). * Significant difference between conditions (SNK: P < 0.05).
longer at 38 mm gape compared to 10 and 14 mm jaw gapes (P < 0.015) in the TAR muscle (Fig. 4B). No effect of jaw gape was seen in the LPR muscle (P > 0.958) (Fig. 4C).
3.3.
Influence of jaw gape on MVB-EMG
In the MAR muscle, intercuspal clenching produced significantly higher MVC-EMG value compared to biting on the jawbar with the incisors (MVB-EMG) at all jaw gape positions (ANOVA: P < 0.001) (Fig. 5A). The MVB-EMG significantly decreased with an increase of the gapes, i.e. biting at 6, 14, and 18 mm gapes produced significantly higher MVB-EMG values compared to 26, 30, 34, and 38 mm (P < 0.013). Biting at 38 mm was associated with significantly lower MVB-EMG values compared to all other gapes (P < 0.003) except 34 mm (Fig. 5A). In the TAR muscle, intercuspal clenching evoked significantly higher MVC-EMG values compared to MVB-EMG at all jaw gapes (ANOVA: P < 0.001) (Fig. 5B). There was no significant effect of jaw gape (ANOVA: P = 0.642). In the LPR muscle, intercuspal clenching produced significantly higher MVC-EMG values compared to MVB-EMG at 6, 10, and 14 mm jaw gapes (ANOVA: P < 0.049) (Fig. 5C). No significant effect was noted between MVC-EMG and MVBEMG, nor was there an effect of jaw gape on the MVB-EMG values in the ADR muscle (P = 0.672) (Fig. 5D).
Fig. 5 – Average EMG during maximum voluntary contraction (MVC-EMG) and maximal voluntary biting (MVB-EMG) at the jaw-bar in the four muscles: (A) surface EMG recorded form MAR; (B) surface EMG from TAR; (C) intramuscular EMG from LPR; (D) intramuscular EMG from ADR. Mean values + S.E.M. (n = 12). *Significant difference between conditions (SNK: P < 0.05).
4.
Discussion
The main finding of this study was that the influence of jaw gape on the jaw-stretch reflex was muscle-dependent. In the masseter, the reflex amplitude reached a peak at 14 mm gape, after which it decreased with increasing gape. In the temporalis muscle, the amplitude increased with increases in jaw gape up to 34 mm. There was no significant effect of the different gapes on the latency of the reflex. Furthermore, the EMG activity during maximal biting was highest at the intercuspal position, and decreased with increases in the jaw gape in the masseter muscle.
4.1.
Methodological considerations
Tapping the chin with a tendon hammer has been widely used to evoke a stretch reflex response in previous studies and is
archives of oral biology 52 (2007) 562–570
routinely used in the neurological clinic.27–30 A number of different jaw stretch devices has been developed for research purposes and has improved the accuracy of the stretch stimulus.31,32 The present stretch device was similar to that described by Miles et al.22 and allowed a high degree of control with the stretch stimulus which has allowed us to systematically examine the influence of the pain on the reflex.5,6,8,33– 35
The present results clearly demonstrated that the amplitude of the short-latency jaw-stretch reflex is modulated by differences in jaw gape. The results of our previous studies showed that the amplitude of the jaw-stretch reflex to a given stimulus is proportional to the level of EMG activity.4,5,7 To study the stretch reflex response in individual muscles, the background muscle activity should therefore be carefully controlled. Normalisation of the reflex amplitude to the background EMG activity has the advantage that the excitability of the alpha-motoneuron can be standardised across muscles, individuals, and conditions.3 The increase in stretch reflex amplitude may be related to a larger excitability of the alpha-motoneurons at a higher level of background muscle activity.10 In this study, the pre-stimulus EMG activity had been controlled by the visual feedback and the normalisation of reflex amplitude was performed with respect to prestimulus EMG. It is therefore equivalent to the reflex gain corrected for the influence of the excitability level of the motor neurons.32 Considerations of the maximal EMG could be dependent upon the jaw gape, the individual MVC at each jaw gape was tested prior to the reflex recordings in this study. The pre-stimulus EMG in MAR was set to 15% of MVB-EMG according to each individual gape. In addition, normalisation was performed in the analysis with respect to the pre-stimulus EMG. Although the sEMG activity recorded from the MAR muscle served as feedback, and as a consequence, the muscles whose EMG activity were not controlled by visual feedback did not necessarily have the same activity levels as the controlled muscle.1,3 Nevertheless, it should be emphasised that the variation in jaw gapes in the pre-stimulus EMG may not affect the interpretation of the reflex amplitude findings at different jaw gapes since the normalisation was performed at each stage of jaw gapes. It has been argued that convergence of afferent discharge from a variety of orofacial receptors contributes to the shortlatency masseter excitatory response.36 The mechanical stimuli are likely to cause vibrations which may excite receptors in the inner ear in addition to the jaw-muscle spindles.37,38 Several human studies have demonstrated short-latency excitatory responses from jaw-closing muscle to electrical or mechanical stimulation of the periodontal receptors.39–41 An anaesthetic block of the receptors around the upper and lower incisors had, however, no significant influence on the jaw-stretch reflex when the reflex was evoked by the stretch device of the present study.7 This finding is in accordance with previous study by Poliakov and Miles.42 It seems likely that the periodontal receptors play an important role when the excitatory reflexes are elicited by tapping the chin or tooth, and that mechanoreceptors in the periodontium have little influence on the jaw-stretch reflex when a rigid muscle stretch device is used to displace the mandible in a fixed downward direction, although Lobbezoo et al.43 did find a
567
significant inhibitory influence of periodontal mechanoreceptors on the anterior temporalis stretch reflex amplitude. Another factor to be taken into account is the possible influence of temporomandibular joint receptors on the reflex responses. The amount of loading of the temporomandibular joint may have influenced the jaw-stretch reflex during different biting tasks.44 The neuromuscular adaptation of jaw-closing muscles to fatigue has been widely studied in conditions of voluntary muscle actions.45–47 However, little information is available on the influence of muscle fatigue on the jaw-stretch reflex. In our previous study, in the same experimental condition as the present one, it was found that the averaged peak-to-peak reflex amplitude of the last 20 out of 40 sweeps was similar to that of the first 20 sweeps.7 This suggests that recording of the jaw-stretch reflex, evoked at a 5-s interval at 15% MVC, is not confounded by fatigue or other neuromuscular adaptation. Another issue is that the surface electrodes used in present study, located over MAR and TAR muscles, recorded the EMG activity predominantly from superficial rather than the deep muscle fibres. The wide jaw gape could have different lengthening effects on the jaw-closing muscles. Goto et al.48 demonstrated that during maximum jaw-opening, the largest increases in muscle length occurred in the medial part of the deep masseter (34–83%), whereas the smallest changes occurred in the posterior-most, superficial masseter (2–19%). Given this limitation of the surface EMG recordings, the outcome from this study might represent only the superficial part of the elevator muscles. The function of the LPR muscle in normal function is still controversial.17,18 The superior head is active on closing, retrusion, and ipsilateral jaw movements, while the inferior head is active on opening, protrusion and contralateral jaw movement.17,18 The lateral pterygoid muscle is therefore likely to play an important role in parafunctional excursive jaw movements and possibly a role in influencing the jaw position.18 The stretch reflex has been observed in the lateral pterygoid muscle in cats13 and humans14,16 and it has been indicated that the evoked stretch response in human muscle is probably a monosynaptic reflex triggered by muscle spindles.16 In this present study, bipolar wire electrodes were used to record the EMG activity of the LPR muscle and ADR. Because of its deep location and the small size of the LPR, it may be difficult to place the electrodes into the inferior head. Previous researchers reported that the EMG patterns differ widely, depending upon the position of the electrodes in the LPR muscle. Furthermore, the wire electrodes as used here might have the potential to move after insertion, especially with major motion of the mandibular condyle during wide opening. The implication is that the recording electrodes may also have provided interference signals from multi-fibre activity from the close-approximating elevator muscle fibres.18 A computed tomography (CT) was used to clarify the normal function of the lateral pterygoid muscle during a single motor unit recording of the muscle.49 In living humans, there is no reliable means for confirmable electrode placement other than CT scans which is, however, not easily accessible at most research labs. It was therefore difficult to prove that the recording of the LPR was exactly from the target muscle alone.16 A stretch reflex in
568
archives of oral biology 52 (2007) 562–570
the ADR muscle was not generally supported by the findings in this study. The result was expected since jaw-opening muscles have no clear background EMG activity during biting and, as previously shown, there are few muscle spindles in the jaw-opening muscles.12 The recorded EMG (Fig. 5C), and reflex responses (Figs. 2C and 3C) in the LPR, which was coincident with the strong elevator reflex responses, and in ADR, which was observed in only two subjects, might be the results of cross-talk from adjacent jaw elevator fibres.
4.2.
Influence of jaw gape on the stretch reflex
Firstly, the relationship between the amplitude of stretch reflex and the jaw gape is muscle-dependent. In the MAR muscle, the amplitude of the stretch reflex increased from 6 to 10 mm, and reached its highest value at 14 mm, after which it decreased with further increases in jaw gape (Fig. 2A). In the TAR muscle, the amplitude of the stretch reflex increased with increases the jaw gape up to 34 mm (Fig. 2B). There was, however, no significant change in the amplitude of stretch reflex with changes of the jaw gapes in the LPR muscle. The different changes in the three muscles likely depend on the direction of the muscle fibres and different functions at each biting task.29 Secondly, the jaw gape did affect the amplitude of the jawstretch reflex in jaw-closing muscles. In previous studies, we have found that the amplitude of the reflex was increased with an increased vertical dimension.7 The increased amplitude reached its highest value at 14 mm, and then decreased again at 24 mm.4 In this present study, the reflex was recorded at jaw gapes varying from 6 to 38 mm, at a 4-mm intervals. It seems likely that an increase in muscle spindle excitability at larger jaw gapes (and thus at larger muscle lengths) is responsible for the larger reflex amplitudes. It was marginally, but significantly (P = 0.038) larger at 14 mm than other jaw gapes in MAR, whereas the reflex amplitude is highest at 34 mm in the TAR. Our previous study7 showed that an increase in jaw gape by 2.5 mm resulted in significantly larger reflex amplitudes compared with the initial jaw gape, which corroborates the results of the present study. The position with an increased vertical dimension leads to an increase in the length of the masseter muscle fibres. Generally, muscle spindles are highly sensitive to small changes in muscle length.50 Thus, an increase in the muscle spindle excitability at longer muscle length may have been responsible for the larger reflex amplitude.29 Van der Bilt et al.20 studied the modulation of the jaw-stretch reflex during rhythmic open-close movements. They found larger reflex amplitudes at a jaw gape of about 20 mm, the maximum gape in their study, than at smaller jaw gapes during the opening phase. The reflex amplitudes, however, were not correlated with jaw gape during the jaw closing phase. Functionally, the larger amplitudes at a larger jaw gape may reflect a preparation of the masticatory system for possible unexpected events during food handling in the subsequent closing phase. A comparable explanation has been formulated for the reflex modulation that was observed during human locomotion in terms of a preparation for unexpected ground conditions.36 Another factor to be taken into account is the possible influence of temporomandibular joint (TMJ) receptors on the
stretch reflex responses even though we did not find any influence on the stretch amplitude by blocking the afferent sensory input from the TMJ in our previous study.4 The amount of loading of the TMJ may have influenced the jawstretch reflex during different biting tasks.51 Moreover, the influence of the higher central nervous system should also be considered. Biting at different jaw gapes, descending signals from higher centres, may have influenced motoneurons, primary afferents, or the fusimotor system in the reflex pathways, and could have contributed to the observed results.29 The onset latency of the stretch reflex was not influenced by the jaw gape in this study. The observed reflex duration, with a range of 8–10 ms, was as in accordance with our previous studies using the same experimental equipment.5–8 The duration of the jaw-stretch reflex was not significantly changed at different jaw gapes, except at the biggest opening in MAR and TAR (Fig. 4). The onset latency of the stretch reflex was also not influenced by the jaw gape.
4.3.
Influence of jaw gape on MVB-EMG
Measurement of the MVC-EMG is an attempt to quantify the total force of the jaw-closing muscles. The present study showed that the EMG activity is much higher when biting at the intercuspal position (MVC-EMG) than biting on the jaw-bar with incisors (MVB-EMG) in all muscles (Fig. 5). The specific direction of the bite force determines the pattern of EMG activity in the jaw-closing muscles.50 It was reported that the EMG activity declined to 47% in the deep masseter and to 86% in the superficial masseter during incisor clenching.52 When biting on the bar with the incisors, the EMG activity during MVB was significantly higher at the smaller gapes of 6, 10, and 14 mm compared to bigger gapes of 26, 30, 34, and 38 mm (Fig. 5). Many physiological factors, i.e. size, composition and mechanical advantage of jaw-closing muscles, sensitivity of the teeth, muscle and TMJ may have influenced the generation of MVB-EMG.53 The maximum bite force appears to be different when measured at different jaw gapes.54–56 As shown by Manns et al.,54 bite force increases up to jaw gapes of 15–20 mm and thereafter decreases as long as the EMG activity level is constant. On the other hand, when the bite force maintained is at a constant value, the EMG activity of the jaw-closing muscle decreases with increase in the vertical dimension.57 This change could be related to a change in the bite direction. Paphangkorakit and Osborn58 reported that the average biting force increased as the jaw was opened, reached a plateau between 14 and 28 mm of incisal separation, and then decreased at wider jaw openings. The initial forward bite direction with respect to the mandibular occlusal plane shifted backwards during jaw opening, while the EMG activity of the masseter muscles declined and that of the temporalis muscles was largely unchanged, resulting in an increase of the ratio between the EMG activity in temporalis and masseter muscles.
4.4.
Clinical significance
Clinically, changes in the occlusal vertical dimension (OVD) have often been associated with certain problems, such as
archives of oral biology 52 (2007) 562–570
temporomandibular disorders,59 and headache.60 Although more recent reviews have questioned the relationships, the control of jaw movements and jaw position is performed by inputs from periodontal and mucosal mechanoreceptors, muscle spindles, Golgi tendon organs, and joint receptors.61,62 The jaw-muscle spindles are sensitive to muscle length and would be responsible for the perception of jaw position and jaw gapes.63 Neurons in the trigeminal mesencephalic nucleus (MesV) play an important role in the regulation of the OVD, because the MesV receives the projection from jaw-closing muscle spindles and periodontal mechanoreceptors.64 The muscle activity could be significantly changed when clinical changes are made to the OVD.65 Changes of OVD may be related in many situations, such as in the orthodontic treatment of mild Class III and deep anterior overbite cases, or in the prosthetic rehabilitation of advanced attrition. Increasing the OVD has also been used to treat disorders involving muscular hyperactivity, such as certain types of TMD.65,66 Recently it was shown in an animal study that when the OVD increase in rats represented 30% of the maximum jaw opening, the sensitivity of masseter muscle spindles was reduced.64 This was supposed to be about the same percentage as the physiological rest position reported for humans.54 In conclusion, the jaw gapes influence the sensitivity of the human muscle spindle afferents in jaw-closing muscles with a distinct peak, which is within normal jaw gapes during function. This new knowledge may add additional pieces of physiological information to the clinical situation with changes in occlusal vertical dimension.
Acknowledgements The Danish National Research Foundation supported the present study. The participation of volunteers is greatly appreciated.
references
1. Lobbezoo F, Van der Glas HW, Buchner R, Van der Bilt A, Bosman F. Gain and threshold of the jaw-jerk reflex in man during isometric contraction. Exp Brain Res 1993;93:129–38. 2. Lobbezoo F, Van der Glas HW, Buchner R, Van der Bilt A, Bosman F. Jaw-jerk reflex activity in relation to various clenching tasks in man. Exp Brain Res 1993;93:139–47. 3. Lobbezoo F, van der Glas HW, van der Bilt A, Buchner R, Bosman F. Sensitivity of the jaw-jerk reflex in patients with myogenous temporomandibular disorder. Arch Oral Biol 1996;41:553–63. 4. Lobbezoo F, Wang K, Aartman IHA, Svensson P. Effects of TMJ anesthesia and jaw gape on jaw-stretch reflexes in humans. Clin Neurophysiol 2003;114:1656–61. 5. Wang K, Svensson P, Arendt-Nielsen L. Effect of tonic muscle pain on short-latency jaw-stretch reflexes in humans. Pain 2000;88:189–97. 6. Wang K, Arendt-Nielsen L, Svensson P. Excitatory actions of experimental muscle pain on early and late components of human jaw stretch reflexes. Arch Oral Biol 2001;46:433–42. 7. Wang K, Svensson P. Influence of methodological parameters on human jaw-stretch reflexes. Eur J Oral Sci 2001;109:86–94.
569
8. Svensson P, Macaluso GM, De Laat A, Wang K. Effects of local and remote muscle pain on human jaw reflexes evoked by fast stretches at different clenching levels. Exp Brain Res 2001;139:495–502. 9. Hannam AG. Effect of voluntary contraction of the masseter and other muscles upon the masseteric reflex in man. J Neurol Neurosurg Psychiatry 1972;35:66–71. 10. Lund JP, Lamarry Y, Lavigne G, Duquet G. Human jaw reflexes. Adv Neurol 1983;39:739–55. 11. Hannam AG, McMillan AS. Internal organization in the human jaw muscles. Crit Rev Oral Biol Med 1994;5:55–89. 12. Rowlerson AM. Specialization of mammalian jaw muscle: fiber type compositions and the distribution of muscle spindles. In: Taylor A, editor. Neurophysiology of the jaws and teeth. London: Macmillan; 1990. p. 1–15. 13. Kawamura Y, Kato I, Miyoshi K. Functional anatomy of the lateral pterygoid muscle in the cat. J Dent Res 1968;47:1142–8. 14. Widmalm SE, Lillie JH, Ash Jr MM. Anatomical and electromyographic studies of the lateral pterygoid muscle. J Oral Rehabil 1987;14:429–46. 15. Luschei ES, Goldberg LJ, Neural mechanisms of mandibular control: mastication and voluntary biting. In: Brooks VB, editor. Motor control. Handbook of physiology sect 1 The nervous system, vol. II, part2. Bethesda: MD: American Physiological Society; 1981. p. 1237–74. 16. Hiraba K, Hibino K, Hiranuma K, Negoro T. EMG activities of two heads of the human lateral pterygoid muscle in relation to mandibular condyle movement and biting force. J Neurophysiol 2000;83:2120–37. 17. Murray GM, Phanachet I, Uchida S, Whittle T. The role of the human lateral pterygoid muscle in the control of horizontal jaw movements. J Orofac Pain 2001;15. p. 279–92; 292–305, Review. 18. Murray GM, Phanachet I, Uchida S, White T. The human lateral pterygoid muscle: a review of some experimental aspects and possible clinical relevance. Aust Dent J 2004;49:2–8. Review. 19. Ostry DJ, Gribble PL, Levin MF, Feldman AG. Phasic and tonic stretch reflexes in muscles with few muscle spindles: human jaw-opener muscles. Exp Brain Res 1997;116: 299–308. 20. van der Bilt A, Ottenhoff FAM, van der Glas HW, Bosman F, Abbink JH. Modulation of the mandibular stretch reflex sensitivity during various phases of rhythmic open-close movements in humans. J Dent Res 1997;76:839–47. 21. Dworkin SF, LeResche L. Research diagnostic criteria for temporomandibular disorders. Review, criteria, examinations and specifications, critique. J Craniomandibular Disord Facial Oral Pain 1992;6:301–55. 22. Miles TS, Poliakov AV, Flavel SC. An apparatus for controlled stretch of human jaw-closing muscles. J Neurosci Methods 1993;46:197–202. 23. Wood WW, Takada K, Hannam AG. The electromyographic activity of the inferior part of the human lateral pterygoid muscle during clenching and chewing. Arch Oral Biol 1986;31:245–53. 24. Widmalm SE, Lillie JH, Ash Jr MM. Anatomical and electromyographic studies of the digastric muscle. J Oral Rehabil 1988;15:3–21. 25. Svensson P, Bak J, Troest T. Spread and referral of experimental pain in different jaw muscles. J Orofac Pain 2003;17:214–23. 26. Svensson P, De Laat A, Graven-Nielsen T, Arendt-Nielsen L. Experimental jaw-muscle pain does not change heteronymous H-reflexes in the human temporalis muscle. Exp Brain Res 1998;121:311–8. 27. Murray GM, Klineberg IJ. Electromyographic recordings of human jaw-jerk reflex characteristics evoked under standardized conditions. Arch Oral Biol 1984;29:537–49.
570
archives of oral biology 52 (2007) 562–570
28. Cruccu G, Frisardi G, van Steenberghe D. Side asymmetry of the jaw jerk in human craniomandibular dysfunction. Arch Oral Biol 1992;37:257–62. 29. Goldberg LJ. The effect of jaw position on the excitability of two reflexes involving the masseter muscle in man. Arch Oral Biol 1972;17:565–76. 30. Kimura J, Daube J, Burke D, Hallett M, Cruccu G, Ongerboer de Visser BW, et al. Human reflexes and late responses. Report of an IFCN committee. Electroencephalogr Clin Neurophysiol 1994;90:393–403. 31. Cooker HS, Larson CR, Luschei ES. Evidence that the human jaw stretch reflex increases the resistance of the mandible to small displacements. J Physiol (Lond) 1980;308:61–78. 32. Buchner R, Brouwers JE, van der Glas HW, Bosman F. The bilateral amplitude imbalance in the jaw-jerk reflex after a transient mandibular load in patients with myogenous craniomandibular disorders as compared with normal subjects. In: van Steenberghe D, De Laat A, editors. Electromyography of jaw reflexes in man. Leuven, Belgium: Leuven University Press; 1989. p. 377–88. 33. Wang K, Arendt-Nielsen L, Svensson P. Capsaicin-induced muscle pain alters the excitability of the human jaw-stretch reflex. J Dent Res 2002;81:650–4. 34. Wang K, Arendt-Nielsen L, Jensen T, Svensson P. Reduction of clinical temporomandibular joint pain is associated with a reduction of the jaw-stretch reflex. J Orofac Pain 2004;18:33–40. 35. Cairns BE, Wang K, Hu JW, Sessle BJ, Arendt-Nielsen L, Svensson P. The effect of glutamate-evoked masseter muscle pain on the human jaw-stretch reflex differs in men and women. J Orofac Pain 2003;17:317–25. 36. Hellsing G. Human jaw muscle motor behaviour. II. Reflex and receptor mechanisms. Swed Dent J 1988;12:47–56. 37. Hannam AG, Matthews B, Yemm R. Receptors involved in the response of the masseter muscle to tooth contact in man. Arch Oral Biol 1970;15:17–24. 38. van der Glas HW, De Laat A, Carels C, van Steenberghe D. Interactive periodontal and acoustic influences on the masseteric post-stimulus electromyographic complex in man. Brain Res 1988;22:284–94. 39. Sessle BJ, Schmitt A. Effects of controlled tooth stimulation of jaw muscle activity in man. Arch Oral Biol 1972;17: 1597–607. 40. Goldberg LJ. Masseter muscle excitation induced by stimulation of periodontal and gingival receptors in man. Brain Res 1971;32:369–81. 41. Clark GT, Goldberg LJ. Factors influencing the excitatorymasseteric reflex evoked by gingival electrical stimulation in man. Arch Oral Biol 1983;28:1055–8. 42. Poliakov AV, Miles TS. Stretch reflexes in human masseter. J Physiol (Lond) 1994;476:323–31. 43. Lobbezoo F, Verheij JG, Naeije M. Influence of periodontal receptors on the jaw-jerk reflex amplitude in man. Eur J Oral Sci 2001;109:40–3. 44. Erkelens CJ, Bosman F. Influences of periodontal and mandibular-joint receptors on reflex sensitivity of human jaw-closing muscles. Arch Oral Biol 1985;30:450–545. 45. Clark GT, Carter MC. Electromyographic study of human jaw-closing muscle endurance, fatigue and recovery at various isometric force levels. Arch Oral Biol 1985;30: 563–9. 46. Junge D, Clark GT. Electromyographic turns analysis of sustained contraction in human masseter muscles at various isometric force levels. Arch Oral Biol 1993;38:583–8.
47. Gay T, Maton B, Rendell J, Majourau A. Characteristics of muscle fatigue in patients with myofacial pain-dysfunction syndrome. Arch Oral Biol 1994;39:847–52. 48. Goto TK, Langenbach GE, Hannam AG. Length changes in the human masseter muscle after jaw movement. Anat Rec 2001;262:293–300. 49. Murray GM, Phanachet I, Hupalo M, Wanigaratne K. Simultaneous recording of mandibular condylar movement and single motor-unit activity at verified sites in the human lateral pterygoid muscle. Arch Oral Biol 1999;44:671–82. 50. Matthews PB, Stein RB. The sensitivity of muscle spindle afferents to small sinusoidal changes of length. J Physiol (Lond) 1969;200:723–43. 51. Mao J, Osborn JW. Direction of a bite force determines the pattern of activity in jaw-closing muscles. J Dent Res 1994;73:1112–20. 52. Blanksma NG, van Eijden TM. Electromyographic heterogeneity in the human temporalis and masseter muscles during static biting, open/close excursions, and chewing. J Dent Res 1995;74:1318–27. 53. Dean JS, Throckmorton GS, Ellis III E, Sinn DP. A preliminary study of maximum voluntary bite force and jaw muscle efficiency in pre-orthognathic surgery patients. J Oral Maxillofac Surg 1992;50:1284–8. 54. Manns A, Miralles R, Guerrero F. The changes in electrical activity of the postural muscles of the mandible upon varying the vertical dimension. J Prosthet Dent 1981;45: 438–45. 55. Mackenna BR, Turker KS. Jaw separation and maximum incising force. J Prosthet Dent 1983;49:726–30. 56. Lindauer SJ, Gay T, Rendell J. Effect of jaw opening on masticatory muscle EMG-force characteristics. J Dent Res 1993;72:51–5. 57. Morimoto T, Abekura H, Tokuyama H, Hamada T. Alteration in the bite force and EMG activity with changes in the vertical dimension of edentulous subjects. J Oral Rehabil 1996;23:336–41. 58. Paphangkorakit J, Osborn JW. Effect of jaw opening on the direction and magnitude of human incisal bite forces. J Dent Res 1997;76:561–7. 59. Christensen J. Effect of occlusion-raising procedures on the chewing system. Dent Pract Dent Rec 1970;20:233–8. 60. Hellsing E. Increased overbite and craniomandibular disorders—a clinical approach. Am J Orthod Dentofacial Orthop 1990;98:516–22. 61. Lund JP. Mastication and its control by the brain stem. Crit Rev Oral Biol Med 1991;2:33–64. 62. Trulsson M, Johansson RS. Orofacial mechanoreceptors in humans: encoding characteristics and responses during natural orofacial behaviors. Behav Brain Res 2002;135:27–33. 63. Zhang W, Kobayashi M, Moritani M, Masuda Y, Dong J, Yagi T, et al. An involvement of trigeminal mesencephalic neurons in regulation of occlusal vertical dimension in the guinea pig. J Dent Res 2003;82:565–9. 64. Yabushita T, Zeredo JL, Toda K, Soma K. Role of occlusal vertical dimension in spindle function. J Dent Res 2005;84:245–9. 65. Abduljabbar T, Mehta NR, Forgione AG, Clark RE, Kronman JH, Munsat TL, et al. Effect of increased maxillo-mandibular relationship on isometric strength in TMD patients with loss of vertical dimension of occlusion. Cranio 1997;15:57–67. 66. Hagag G, Yoshida K, Miura H. Occlusion, prosthodontic treatment, and temporomandibular disorders: a review. J Med Dent Sci 2000;47:61–6.
available at www.sciencedirect.com
journal homepage: www.intl.elsevierhealth.com/journals/arob
Influence of jaw gape on EMG of jaw muscles and jaw-stretch reflexes Kelun Wang a,*, Frank Lobbezoo b, Peter Svensson a,c, Lars Arendt-Nielsen a a
Center for Sensory-Motor Interaction, Orofacial Pain Laboratory, Aalborg University, Denmark Department of Oral Function, Academic Centre for Dentistry Amsterdam (ACTA), Louwesweg 1, 1066 EA Amsterdam, The Netherlands c Department of Clinical Oral Physiology, School of Dentistry, University of Aarhus, Denmark b
article info
abstract
Article history:
The influence of jaw gapes on jaw-stretch reflexes and jaw muscles activity was studied in
Accepted 5 December 2006
order to test the sensitivity of human muscle spindle afferents in various jaw muscles.
Keywords:
latency excitatory reflex responses were evoked by a custom-made stretch device with the
Human
subjects biting on a jaw-bar with their front teeth. Surface electromyographic (sEMG)
Jaw gape
recordings from right masseter (MAR), and right temporalis (TAR), intramuscular EMG
Stretch reflex
(imEMG) recordings from right lateral pterygoid (LPR) and right anterior digastric (ADR)
Jaw muscle
muscles were made. The reflex at different jaw gapes of 6, 10, 14, 18, 22, 26, 30, 34, and 38 mm
EMG
were examined in random order with standard stretch conditions of 1 mm displacement
Twelve healthy men (mean age S.E.M.: 25.0 1.2 yr) participated in the study. Short-
and 10 ms ramp time. Twenty sweeps of the reflex were recorded at each level with at least 5 s interval between each sweep with online monitoring of the visual feed back at 15% of maximum voluntary contraction (MVC) of each jaw gape from MAR. The results showed that the peak-to-peak amplitude of the jaw-stretch reflex in MAR was significantly higher at 14 mm compared to 30, 34, and 38 mm (P < 0.038), whereas the reflex amplitude in TAR increased with jaw gape until a maximum at 34 mm. There was no significant effect of jaw gape in LPR muscles (P = 0.825) and no obvious stretch reflex was observed in ADR. When the amplitude was normalised to the pre-stimulus EMG at each jaw gape, the highest normalised amplitude was observed at 14 mm jaw gape in MAR, however there was no significant effect of jaw gape on the normalised amplitude in TAR and LPR. In addition, masseter EMG at MVC significantly decreased with the increase of the gapes, i.e. biting at 6, 14, and 18 mm gapes had a significantly higher MVC compared to 26, 30, 34, and 38 mm (ANOVA: P < 0.013). It is concluded that the jaw gapes influence the sensitivity of the human muscle spindle afferents in jaw-closing muscles with a distinct peak, which is within normal jaw gapes during function. # 2006 Elsevier Ltd. All rights reserved.
1.
Introduction
A sudden stretch of the jaw-closing muscles can elicit a shortlatency excitatory response in the muscles, the so-called
stretch reflex. The modulation of the stretch reflex in jawclosing muscle has been studied previously.1–8 The human jaw-closing muscles are richly endowed with muscle spindles, and the spindle afferents make excitatory connections to the
* Corresponding author at: Center for Sensory-Motor Interaction, Orofacial Pain Laboratory, Aalborg University, Fredrik Bajers Vej 7 D-3, DK-9220 Aalborg S, Denmark. Tel.: +45 9635 8745; fax: +45 9815 4008. E-mail address: [email protected] (K. Wang). 0003–9969/$ – see front matter # 2006 Elsevier Ltd. All rights reserved. doi:10.1016/j.archoralbio.2006.12.004
archives of oral biology 52 (2007) 562–570
motoneurons of jaw-closing muscles.9 The stretch reflex plays a significant role in the modulation of activity of jaw-closing muscles.10,11 In a number of orofacial muscles, in particular, the lateral pterygoid muscle and anterior digastric muscles, few muscle spindles have been reported.12 Even though the stretch reflex-like response has also been observed in the lateral pterygoid muscle in cats13 and humans,14 it has, however, been suggested that the stretch reflex plays a minimal role in the regulation of the jaw-opening muscles (see Luschei and Goldberg, 1981 for summary15). A recent study suggested that the stretch reflex-like response, elicited in the human lateral pterygoid muscle, is probably a monosynaptic reflex triggered by muscle spindles.16 The lateral pterygoid muscle has been suggested to play a role in parafunctional excursive jaw movements and also possibly a role in influencing jaw position during jaw movement (for a review see: 17,18). In addition, a study has demonstrated phasic and tonic stretch reflexes in human jaw-opener muscles, which have few muscle spindles.19 The results suggested that spindle afferents in jaw-opening muscles might be sufficient in number to provide the observed patterns of responses, and non-spindle afferents such as free nerve endings in the opening muscles might contribute as well.19 Further studies on stretch reflex activity in the lateral pterygoid muscle and anterior digastric muscles during different jaw gapes may help to increase the insight into the purported role in regulation of the activity in these muscles, especially at wider jaw gapes. Methodological differences in clinical neurophysiology may unfortunately contribute to contradictory views about the behaviour of jaw-stretch reflexes. For example, the amplitude of the jaw-stretch reflex may be influenced by the displacement and velocity of the mandibular movement evoked by the stretcher.7 The level of background EMG activity as well as the specific biting task10,20 has also been shown to influence the stretch reflex amplitude. In our previous study, we found that an increase in jaw gape by 2.5 mm resulted in significantly larger stretch reflex amplitudes compared with the initial jaw gape.7 Lobbezoo et al.2 on the other hand, did not find an effect on the jaw-stretch reflex amplitude of increases in jaw gape by 1 and 2 mm on top of the initial 3 mm. However, only two subjects were tested in that study, which makes it difficult to extrapolate their finding to the other studies. Van der Bilt et al.20 studied the modulation of the jaw-stretch reflex during rhythmic openclose movements. They found larger reflex amplitudes at a jaw gape of about 20 mm than at smaller jaw gapes during the opening phase. However, the reflex amplitudes were not correlated with jaw gape during the jaw closing phase. In a recent study, we found that there is a significant effect of jaw gape for the masseter and anterior temporalis muscles, with the 14-mm gape having the highest amplitude.4 In that study, we investigated the situation at only three different gapes, viz., 4, 14, and 24 mm. The tendency of the sensitivity changes of the stretch reflex during the change of jaw gapes has been not fully shown. Therefore the relationship between jaw gape and stretch reflex amplitude is still not fully clear. Thus, the purpose of this study was to investigate the influence of different jaw gapes on the jaw-stretch reflex in the jaw-closing muscles, as to provide further insight into the properties of the human muscle spindle afferents. The
563
influence on the EMG activity in the lateral pterygoid and anterior digastric muscles was also investigated.
2.
Materials and methods
2.1.
Subjects
The volunteers for this study were all healthy and unmedicated subjects without signs or symptoms of temporomandibular disorders (TMD).21 All subjects had natural dentitions (28 teeth) without significant malocclusion. Twelve men (mean age S.E.M.: 25.0 1.2 yr) participated in the experiment. The study was conducted in accordance with the Helsinki Declaration and informed consent was obtained from all subjects. The study was approved by the local Ethics Committee.
2.2.
Jaw-muscle stretcher
Stretch reflexes were evoked in the jaw muscles with a muscle stretcher based on that described by Miles et al.22 A stainlesssteel jaw-bar was mounted on a frame attached to the floor. A powerful electromagnetic vibrator (Model 406; Ling Dynamic Systems Ltd., Royston, UK) imposed servo-controlled displacements of the lower jaw-bar. A 200 N load cell (Kistler 5039 A312; Winterthur, Switzerland), mounted in series with the moveable probe of the vibrator, measured forces on the lower jaw-bar. The displacement of the vibrator probe was measured with a linear potentiometer (Sakae Type 20 FLP 30A-5K; Kawasaki, Japan), mounted in parallel with the probe. Acceleration in the vertical plane was measured by an accelerometer (Delta Tron Accelerometer Type 4399; Bruel & Kjær, Nærum, Denmark), mounted on the lower jaw-bar. The lower jaw-bar displaces down linearly 1 mm with a ramp time 10 ms when the program is triggered (see Section 2.4). The subjects were instructed to bite on the jaw-bar with their incisors during the recordings. Thus, the initial jaw separation for the subjects was determined by the distance between the upper and lower jaw-bar, which corresponded to 6.0 mm.
2.3.
Experimental protocol
Surface electromyographic (sEMG) recordings from the right masseter (MAR) and right temporalis (TAR) muscles, as well as intramuscular EMG (imEMG) recordings from the right lateral pterygoid (LPR) and right anterior digastric (ADR) muscles were made. The stretch reflexes at nine different jaw gapes of 6, 10, 14, 18, 22, 26, 30, 34, and 38 mm were examined in random order, with standard stretch conditions of 1 mm displacement and 10 ms ramp time. All jaw-stretch reflex recordings were examined with the subject biting with the incisors on the bars of the stretcher in a central position and without mandibular deviation.
2.4.
Recordings of jaw-stretch reflex
The sEMG activity was recorded with use of bipolar disposable surface electrodes (4 mm 7 mm recording area, 720-01-k,
564
archives of oral biology 52 (2007) 562–570
Neuroline; Medicotest, Ølstykke, Denmark) placed 10 mm apart along the central part of the MAR and the TAR muscles. The skin over the recording positions was cleaned with alcohol. The imEMG was recorded with a pair of fine wire electrodes (Ø 80 mm, Medwire, USA), uninsulated 1 mm at the tip and aimed to be inserted into the inferior head of right lateral pterygoid muscle and into the anterior belly of the right digastric muscle via a 23G needle (Microlance, Spain). The intraoral technique for electrode placement in the inferior head was modified from Wood et al.23 The needle was inserted through the oral mucosa above the level of the upper second molar, and advanced to contact the middle third of the lateral surface of the lateral pterygoid plate. The needle was withdrawn, leaving the wires within the inferior head, and the
wires were secured to the buccal surface of the upper first molar and led out through the angle of the mouth, then the wires were fixed by a piece of tape. To record the imEMG of the anterior digastric muscle, the needle was inserted 15 mm through the skin about 1 cm medial and inferior to the lower border of the mandible 4–5 cm from the chin below the region of the first and second mandibular molar.24,25 The location of the intramuscular electrodes was confirmed after withdrawal of the needle by observing the EMG when subjects performed a series of jaw-opening and jaw-protruding movement. The EMG signals were amplified 2000–5000 times (Counterpoint MK2, DK), filtered with bandpass 20 Hz to 1 kHz, sampled at 4 kHz, and stored for off-line analysis. The subjects were initially asked to perform 3 maximal clenches at the intercuspal position each lasting up to 3 s to record the EMG at maximal voluntary contraction (MVC-EMG). Then subjects were asked to bite on the jaw-bar with their incisors. The stretch reflexes were evoked in blocks of 20 sweeps at 9 different jaw gapes in random order varying from 4 mm (i.e. 6, 10, 14, 18, 22, 26, 30, 34, and 38 mm). Before each block of recordings, subjects were asked to make a maximal voluntary biting (MVB) with their incisor teeth on the jaw-bar of the stretch device to obtain the individual MVB-EMG value at each jaw gape in the four muscles. The sEMG activity recorded from the MAR muscle subsequently served for visual feedback (see below). The MVB-EMG recorded from MAR at the start of the each block was used to construct a window of 10% below and above the 15% MVB-EMG level (i.e. 13.5–16.5% MVBEMG). To help subjects achieve this, online calculation of the root-mean-square (RMS) value in 200 ms intervals was performed. The subjects received visual feedback from markers on the computer screen, which changed from green to red upon crossing the upper and lower limits of the window.26 The program automatically triggered the muscle stretcher when the EMG activity remained within the pre-set window for more than 400 ms. A total of 300 ms EMG activity was recorded with 100 ms pre-stimulus and 200 ms poststimulus (Fig. 1). Twenty sweeps of the reflex were recorded at each gape with at least 5 s interval between each sweep (around 0.2 Hz).
2.5.
Fig. 1 – Averaged reflex responses (20 sweeps) in four jaw muscles evoked by jaw-stretches in a single subject. The dotted line shows the onset of the stretch stimulus. (A) Surface EMG recording from right masseter muscle (MAR). Arrows show the onset and offset of reflex. The amplitude was measured as the peak-to-peak value of the positive and negative potential. (B) The reflex response recorded from surface EMG of right temporalis muscles (TAR). (C) The reflex response from intramuscular recording of right lateral pterygoid muscle (LPR). (D) Intramuscular recording from right anterior digastric muscle (ADR). (E) Displacement signal of the stretch with 1 mm displacement and 10 ms ramp.
Analysis
A special-purpose computer program (Aalborg University, Denmark) was used to analyse the jaw-stretch reflex responses. First, the mean EMG activity in the pre-stimulus interval ( 100 to 0 ms) of the averaged and rectified signal was calculated.3,5 The onset latency and peak-to-peak amplitude of the early reflex component, which appeared as a biphasic potential in the average of the non-rectified recordings, was measured (Fig. 1). The peak-to-peak amplitude was then normalised with respect to the mean pre-stimulus EMG activity observed at each stage of jaw gapes.
2.6.
Statistics
One-way and two-way analyses of variance (ANOVA) with repeated measures were performed and followed by pair-wise multiple comparison procedures (Student–Newman–Keuls, SNK). The factors in the ANOVA were experimental conditions
archives of oral biology 52 (2007) 562–570
565
(jaw gape level: 9 levels) and muscles (4 levels). The level of significance was set at P < 0.05. Mean values S.E.M. are presented in the text and figures.
3.
Results
3.1.
Influence of jaw gape on the amplitude of stretch reflex
The stretch reflex was successfully recorded with sEMG from MAR and TAR, and with imEMG from LPR muscles at all different jaw gapes in all subjects. However, the stretch reflex could not be recorded from the ADR in most subjects: although it was clearly seen in two subjects. Therefore, the stretch reflex in ADR was not further analysed in this study. In the MAR muscle, the peak to peak amplitude of the jawstretch reflex was highest at 14 mm when compared to 30, 34, and 38 mm (ANOVA: P < 0.038). The amplitude was lowest at 38 mm, i.e. the biggest gape, when compared to all other jaw gapes (P < 0.044) except 30 and 34 mm (Fig. 2A). In the TAR muscle, the reflex amplitude increased with increase in jaw gape, with a peak at 34 mm, after which it decreased again at 38 mm. The amplitude recorded at 30 and 34 mm was significantly higher than that at 6, 10, and 14 mm (ANOVA: P < 0.010), and higher at 26 mm compared to 6 and Fig. 3 – Influence of jaw gapes on the normalised amplitude of stretch reflex. ‘‘Amplitude (100%)’’ (ordinate) represents the normalised peak-to-peak amplitude to the prestimulus EMG. The normalised reflex amplitude was from surface EMG of MAR and TAR, and from intramuscular EMG of LPR. The feedback was derived from the surface EMG of the MAR. Mean values + S.E.M. (n = 12). *Significant difference between conditions (SNK: P < 0.05).
10 mm (P < 0.007). It was also significantly higher at 22 and 38 mm compared to 6 mm (P < 0.012) (Fig. 2B). There was no significant effect of the jaw gape on the stretch amplitude in the LPR muscle (ANOVA: P = 0.825) (Fig. 2C). When the amplitude was normalised to the pre-stimulus EMG at each jaw gape, the highest normalised amplitude was observed at 14 mm jaw gape in the MAR. It was significantly higher compared to 6 mm (ANOVA: P = 0.03) (Fig. 3A). No significant effect of jaw gape on the normalised amplitude was observed in TAR and LPR muscles (ANOVA: P > 0.381) (Fig. 3B and C).
3.2. Influence of jaw gape on the latency and duration of the stretch reflex Fig. 2 – Influence of jaw gapes on the amplitude of the stretch reflex. The reflex response was from surface EMG of MAR and TAR, and from intramuscular EMG of LPR. The feedback was derived from the surface EMG of the MAR. Mean values + S.E.M. (n = 12). *Significant difference between conditions (SNK: P < 0.05). Note the stretch reflex was only successfully recorded from ADR in 2 out of 12 subjects.
The overall mean values of the latency were: 8.9 0.3 ms in MAR, 8.4 0.3 ms in TAR, and 7.6 0.3 ms in LPR, respectively. There was no significant effect of jaw gape on the latency of the stretch reflex in any jaw muscle (ANOVA: P > 0.213). The duration of the reflex (overall average: 9.2 2.1 ms) was significantly longer at the 38 mm jaw gape compared to 6, 10, 14, 18, 20, 24, and 28 mm jaw gapes (ANOVA: P < 0.030) in the MAR muscle (Fig. 4A). The duration was significantly
566
archives of oral biology 52 (2007) 562–570
Fig. 4 – Influence of jaw gapes on the duration of stretch reflex in surface EMG of MAR and TAR, and in intramuscular EMG of LPR. Mean values + S.E.M. (n = 12). * Significant difference between conditions (SNK: P < 0.05).
longer at 38 mm gape compared to 10 and 14 mm jaw gapes (P < 0.015) in the TAR muscle (Fig. 4B). No effect of jaw gape was seen in the LPR muscle (P > 0.958) (Fig. 4C).
3.3.
Influence of jaw gape on MVB-EMG
In the MAR muscle, intercuspal clenching produced significantly higher MVC-EMG value compared to biting on the jawbar with the incisors (MVB-EMG) at all jaw gape positions (ANOVA: P < 0.001) (Fig. 5A). The MVB-EMG significantly decreased with an increase of the gapes, i.e. biting at 6, 14, and 18 mm gapes produced significantly higher MVB-EMG values compared to 26, 30, 34, and 38 mm (P < 0.013). Biting at 38 mm was associated with significantly lower MVB-EMG values compared to all other gapes (P < 0.003) except 34 mm (Fig. 5A). In the TAR muscle, intercuspal clenching evoked significantly higher MVC-EMG values compared to MVB-EMG at all jaw gapes (ANOVA: P < 0.001) (Fig. 5B). There was no significant effect of jaw gape (ANOVA: P = 0.642). In the LPR muscle, intercuspal clenching produced significantly higher MVC-EMG values compared to MVB-EMG at 6, 10, and 14 mm jaw gapes (ANOVA: P < 0.049) (Fig. 5C). No significant effect was noted between MVC-EMG and MVBEMG, nor was there an effect of jaw gape on the MVB-EMG values in the ADR muscle (P = 0.672) (Fig. 5D).
Fig. 5 – Average EMG during maximum voluntary contraction (MVC-EMG) and maximal voluntary biting (MVB-EMG) at the jaw-bar in the four muscles: (A) surface EMG recorded form MAR; (B) surface EMG from TAR; (C) intramuscular EMG from LPR; (D) intramuscular EMG from ADR. Mean values + S.E.M. (n = 12). *Significant difference between conditions (SNK: P < 0.05).
4.
Discussion
The main finding of this study was that the influence of jaw gape on the jaw-stretch reflex was muscle-dependent. In the masseter, the reflex amplitude reached a peak at 14 mm gape, after which it decreased with increasing gape. In the temporalis muscle, the amplitude increased with increases in jaw gape up to 34 mm. There was no significant effect of the different gapes on the latency of the reflex. Furthermore, the EMG activity during maximal biting was highest at the intercuspal position, and decreased with increases in the jaw gape in the masseter muscle.
4.1.
Methodological considerations
Tapping the chin with a tendon hammer has been widely used to evoke a stretch reflex response in previous studies and is
archives of oral biology 52 (2007) 562–570
routinely used in the neurological clinic.27–30 A number of different jaw stretch devices has been developed for research purposes and has improved the accuracy of the stretch stimulus.31,32 The present stretch device was similar to that described by Miles et al.22 and allowed a high degree of control with the stretch stimulus which has allowed us to systematically examine the influence of the pain on the reflex.5,6,8,33– 35
The present results clearly demonstrated that the amplitude of the short-latency jaw-stretch reflex is modulated by differences in jaw gape. The results of our previous studies showed that the amplitude of the jaw-stretch reflex to a given stimulus is proportional to the level of EMG activity.4,5,7 To study the stretch reflex response in individual muscles, the background muscle activity should therefore be carefully controlled. Normalisation of the reflex amplitude to the background EMG activity has the advantage that the excitability of the alpha-motoneuron can be standardised across muscles, individuals, and conditions.3 The increase in stretch reflex amplitude may be related to a larger excitability of the alpha-motoneurons at a higher level of background muscle activity.10 In this study, the pre-stimulus EMG activity had been controlled by the visual feedback and the normalisation of reflex amplitude was performed with respect to prestimulus EMG. It is therefore equivalent to the reflex gain corrected for the influence of the excitability level of the motor neurons.32 Considerations of the maximal EMG could be dependent upon the jaw gape, the individual MVC at each jaw gape was tested prior to the reflex recordings in this study. The pre-stimulus EMG in MAR was set to 15% of MVB-EMG according to each individual gape. In addition, normalisation was performed in the analysis with respect to the pre-stimulus EMG. Although the sEMG activity recorded from the MAR muscle served as feedback, and as a consequence, the muscles whose EMG activity were not controlled by visual feedback did not necessarily have the same activity levels as the controlled muscle.1,3 Nevertheless, it should be emphasised that the variation in jaw gapes in the pre-stimulus EMG may not affect the interpretation of the reflex amplitude findings at different jaw gapes since the normalisation was performed at each stage of jaw gapes. It has been argued that convergence of afferent discharge from a variety of orofacial receptors contributes to the shortlatency masseter excitatory response.36 The mechanical stimuli are likely to cause vibrations which may excite receptors in the inner ear in addition to the jaw-muscle spindles.37,38 Several human studies have demonstrated short-latency excitatory responses from jaw-closing muscle to electrical or mechanical stimulation of the periodontal receptors.39–41 An anaesthetic block of the receptors around the upper and lower incisors had, however, no significant influence on the jaw-stretch reflex when the reflex was evoked by the stretch device of the present study.7 This finding is in accordance with previous study by Poliakov and Miles.42 It seems likely that the periodontal receptors play an important role when the excitatory reflexes are elicited by tapping the chin or tooth, and that mechanoreceptors in the periodontium have little influence on the jaw-stretch reflex when a rigid muscle stretch device is used to displace the mandible in a fixed downward direction, although Lobbezoo et al.43 did find a
567
significant inhibitory influence of periodontal mechanoreceptors on the anterior temporalis stretch reflex amplitude. Another factor to be taken into account is the possible influence of temporomandibular joint receptors on the reflex responses. The amount of loading of the temporomandibular joint may have influenced the jaw-stretch reflex during different biting tasks.44 The neuromuscular adaptation of jaw-closing muscles to fatigue has been widely studied in conditions of voluntary muscle actions.45–47 However, little information is available on the influence of muscle fatigue on the jaw-stretch reflex. In our previous study, in the same experimental condition as the present one, it was found that the averaged peak-to-peak reflex amplitude of the last 20 out of 40 sweeps was similar to that of the first 20 sweeps.7 This suggests that recording of the jaw-stretch reflex, evoked at a 5-s interval at 15% MVC, is not confounded by fatigue or other neuromuscular adaptation. Another issue is that the surface electrodes used in present study, located over MAR and TAR muscles, recorded the EMG activity predominantly from superficial rather than the deep muscle fibres. The wide jaw gape could have different lengthening effects on the jaw-closing muscles. Goto et al.48 demonstrated that during maximum jaw-opening, the largest increases in muscle length occurred in the medial part of the deep masseter (34–83%), whereas the smallest changes occurred in the posterior-most, superficial masseter (2–19%). Given this limitation of the surface EMG recordings, the outcome from this study might represent only the superficial part of the elevator muscles. The function of the LPR muscle in normal function is still controversial.17,18 The superior head is active on closing, retrusion, and ipsilateral jaw movements, while the inferior head is active on opening, protrusion and contralateral jaw movement.17,18 The lateral pterygoid muscle is therefore likely to play an important role in parafunctional excursive jaw movements and possibly a role in influencing the jaw position.18 The stretch reflex has been observed in the lateral pterygoid muscle in cats13 and humans14,16 and it has been indicated that the evoked stretch response in human muscle is probably a monosynaptic reflex triggered by muscle spindles.16 In this present study, bipolar wire electrodes were used to record the EMG activity of the LPR muscle and ADR. Because of its deep location and the small size of the LPR, it may be difficult to place the electrodes into the inferior head. Previous researchers reported that the EMG patterns differ widely, depending upon the position of the electrodes in the LPR muscle. Furthermore, the wire electrodes as used here might have the potential to move after insertion, especially with major motion of the mandibular condyle during wide opening. The implication is that the recording electrodes may also have provided interference signals from multi-fibre activity from the close-approximating elevator muscle fibres.18 A computed tomography (CT) was used to clarify the normal function of the lateral pterygoid muscle during a single motor unit recording of the muscle.49 In living humans, there is no reliable means for confirmable electrode placement other than CT scans which is, however, not easily accessible at most research labs. It was therefore difficult to prove that the recording of the LPR was exactly from the target muscle alone.16 A stretch reflex in
568
archives of oral biology 52 (2007) 562–570
the ADR muscle was not generally supported by the findings in this study. The result was expected since jaw-opening muscles have no clear background EMG activity during biting and, as previously shown, there are few muscle spindles in the jaw-opening muscles.12 The recorded EMG (Fig. 5C), and reflex responses (Figs. 2C and 3C) in the LPR, which was coincident with the strong elevator reflex responses, and in ADR, which was observed in only two subjects, might be the results of cross-talk from adjacent jaw elevator fibres.
4.2.
Influence of jaw gape on the stretch reflex
Firstly, the relationship between the amplitude of stretch reflex and the jaw gape is muscle-dependent. In the MAR muscle, the amplitude of the stretch reflex increased from 6 to 10 mm, and reached its highest value at 14 mm, after which it decreased with further increases in jaw gape (Fig. 2A). In the TAR muscle, the amplitude of the stretch reflex increased with increases the jaw gape up to 34 mm (Fig. 2B). There was, however, no significant change in the amplitude of stretch reflex with changes of the jaw gapes in the LPR muscle. The different changes in the three muscles likely depend on the direction of the muscle fibres and different functions at each biting task.29 Secondly, the jaw gape did affect the amplitude of the jawstretch reflex in jaw-closing muscles. In previous studies, we have found that the amplitude of the reflex was increased with an increased vertical dimension.7 The increased amplitude reached its highest value at 14 mm, and then decreased again at 24 mm.4 In this present study, the reflex was recorded at jaw gapes varying from 6 to 38 mm, at a 4-mm intervals. It seems likely that an increase in muscle spindle excitability at larger jaw gapes (and thus at larger muscle lengths) is responsible for the larger reflex amplitudes. It was marginally, but significantly (P = 0.038) larger at 14 mm than other jaw gapes in MAR, whereas the reflex amplitude is highest at 34 mm in the TAR. Our previous study7 showed that an increase in jaw gape by 2.5 mm resulted in significantly larger reflex amplitudes compared with the initial jaw gape, which corroborates the results of the present study. The position with an increased vertical dimension leads to an increase in the length of the masseter muscle fibres. Generally, muscle spindles are highly sensitive to small changes in muscle length.50 Thus, an increase in the muscle spindle excitability at longer muscle length may have been responsible for the larger reflex amplitude.29 Van der Bilt et al.20 studied the modulation of the jaw-stretch reflex during rhythmic open-close movements. They found larger reflex amplitudes at a jaw gape of about 20 mm, the maximum gape in their study, than at smaller jaw gapes during the opening phase. The reflex amplitudes, however, were not correlated with jaw gape during the jaw closing phase. Functionally, the larger amplitudes at a larger jaw gape may reflect a preparation of the masticatory system for possible unexpected events during food handling in the subsequent closing phase. A comparable explanation has been formulated for the reflex modulation that was observed during human locomotion in terms of a preparation for unexpected ground conditions.36 Another factor to be taken into account is the possible influence of temporomandibular joint (TMJ) receptors on the
stretch reflex responses even though we did not find any influence on the stretch amplitude by blocking the afferent sensory input from the TMJ in our previous study.4 The amount of loading of the TMJ may have influenced the jawstretch reflex during different biting tasks.51 Moreover, the influence of the higher central nervous system should also be considered. Biting at different jaw gapes, descending signals from higher centres, may have influenced motoneurons, primary afferents, or the fusimotor system in the reflex pathways, and could have contributed to the observed results.29 The onset latency of the stretch reflex was not influenced by the jaw gape in this study. The observed reflex duration, with a range of 8–10 ms, was as in accordance with our previous studies using the same experimental equipment.5–8 The duration of the jaw-stretch reflex was not significantly changed at different jaw gapes, except at the biggest opening in MAR and TAR (Fig. 4). The onset latency of the stretch reflex was also not influenced by the jaw gape.
4.3.
Influence of jaw gape on MVB-EMG
Measurement of the MVC-EMG is an attempt to quantify the total force of the jaw-closing muscles. The present study showed that the EMG activity is much higher when biting at the intercuspal position (MVC-EMG) than biting on the jaw-bar with incisors (MVB-EMG) in all muscles (Fig. 5). The specific direction of the bite force determines the pattern of EMG activity in the jaw-closing muscles.50 It was reported that the EMG activity declined to 47% in the deep masseter and to 86% in the superficial masseter during incisor clenching.52 When biting on the bar with the incisors, the EMG activity during MVB was significantly higher at the smaller gapes of 6, 10, and 14 mm compared to bigger gapes of 26, 30, 34, and 38 mm (Fig. 5). Many physiological factors, i.e. size, composition and mechanical advantage of jaw-closing muscles, sensitivity of the teeth, muscle and TMJ may have influenced the generation of MVB-EMG.53 The maximum bite force appears to be different when measured at different jaw gapes.54–56 As shown by Manns et al.,54 bite force increases up to jaw gapes of 15–20 mm and thereafter decreases as long as the EMG activity level is constant. On the other hand, when the bite force maintained is at a constant value, the EMG activity of the jaw-closing muscle decreases with increase in the vertical dimension.57 This change could be related to a change in the bite direction. Paphangkorakit and Osborn58 reported that the average biting force increased as the jaw was opened, reached a plateau between 14 and 28 mm of incisal separation, and then decreased at wider jaw openings. The initial forward bite direction with respect to the mandibular occlusal plane shifted backwards during jaw opening, while the EMG activity of the masseter muscles declined and that of the temporalis muscles was largely unchanged, resulting in an increase of the ratio between the EMG activity in temporalis and masseter muscles.
4.4.
Clinical significance
Clinically, changes in the occlusal vertical dimension (OVD) have often been associated with certain problems, such as
archives of oral biology 52 (2007) 562–570
temporomandibular disorders,59 and headache.60 Although more recent reviews have questioned the relationships, the control of jaw movements and jaw position is performed by inputs from periodontal and mucosal mechanoreceptors, muscle spindles, Golgi tendon organs, and joint receptors.61,62 The jaw-muscle spindles are sensitive to muscle length and would be responsible for the perception of jaw position and jaw gapes.63 Neurons in the trigeminal mesencephalic nucleus (MesV) play an important role in the regulation of the OVD, because the MesV receives the projection from jaw-closing muscle spindles and periodontal mechanoreceptors.64 The muscle activity could be significantly changed when clinical changes are made to the OVD.65 Changes of OVD may be related in many situations, such as in the orthodontic treatment of mild Class III and deep anterior overbite cases, or in the prosthetic rehabilitation of advanced attrition. Increasing the OVD has also been used to treat disorders involving muscular hyperactivity, such as certain types of TMD.65,66 Recently it was shown in an animal study that when the OVD increase in rats represented 30% of the maximum jaw opening, the sensitivity of masseter muscle spindles was reduced.64 This was supposed to be about the same percentage as the physiological rest position reported for humans.54 In conclusion, the jaw gapes influence the sensitivity of the human muscle spindle afferents in jaw-closing muscles with a distinct peak, which is within normal jaw gapes during function. This new knowledge may add additional pieces of physiological information to the clinical situation with changes in occlusal vertical dimension.
Acknowledgements The Danish National Research Foundation supported the present study. The participation of volunteers is greatly appreciated.
references
1. Lobbezoo F, Van der Glas HW, Buchner R, Van der Bilt A, Bosman F. Gain and threshold of the jaw-jerk reflex in man during isometric contraction. Exp Brain Res 1993;93:129–38. 2. Lobbezoo F, Van der Glas HW, Buchner R, Van der Bilt A, Bosman F. Jaw-jerk reflex activity in relation to various clenching tasks in man. Exp Brain Res 1993;93:139–47. 3. Lobbezoo F, van der Glas HW, van der Bilt A, Buchner R, Bosman F. Sensitivity of the jaw-jerk reflex in patients with myogenous temporomandibular disorder. Arch Oral Biol 1996;41:553–63. 4. Lobbezoo F, Wang K, Aartman IHA, Svensson P. Effects of TMJ anesthesia and jaw gape on jaw-stretch reflexes in humans. Clin Neurophysiol 2003;114:1656–61. 5. Wang K, Svensson P, Arendt-Nielsen L. Effect of tonic muscle pain on short-latency jaw-stretch reflexes in humans. Pain 2000;88:189–97. 6. Wang K, Arendt-Nielsen L, Svensson P. Excitatory actions of experimental muscle pain on early and late components of human jaw stretch reflexes. Arch Oral Biol 2001;46:433–42. 7. Wang K, Svensson P. Influence of methodological parameters on human jaw-stretch reflexes. Eur J Oral Sci 2001;109:86–94.
569
8. Svensson P, Macaluso GM, De Laat A, Wang K. Effects of local and remote muscle pain on human jaw reflexes evoked by fast stretches at different clenching levels. Exp Brain Res 2001;139:495–502. 9. Hannam AG. Effect of voluntary contraction of the masseter and other muscles upon the masseteric reflex in man. J Neurol Neurosurg Psychiatry 1972;35:66–71. 10. Lund JP, Lamarry Y, Lavigne G, Duquet G. Human jaw reflexes. Adv Neurol 1983;39:739–55. 11. Hannam AG, McMillan AS. Internal organization in the human jaw muscles. Crit Rev Oral Biol Med 1994;5:55–89. 12. Rowlerson AM. Specialization of mammalian jaw muscle: fiber type compositions and the distribution of muscle spindles. In: Taylor A, editor. Neurophysiology of the jaws and teeth. London: Macmillan; 1990. p. 1–15. 13. Kawamura Y, Kato I, Miyoshi K. Functional anatomy of the lateral pterygoid muscle in the cat. J Dent Res 1968;47:1142–8. 14. Widmalm SE, Lillie JH, Ash Jr MM. Anatomical and electromyographic studies of the lateral pterygoid muscle. J Oral Rehabil 1987;14:429–46. 15. Luschei ES, Goldberg LJ, Neural mechanisms of mandibular control: mastication and voluntary biting. In: Brooks VB, editor. Motor control. Handbook of physiology sect 1 The nervous system, vol. II, part2. Bethesda: MD: American Physiological Society; 1981. p. 1237–74. 16. Hiraba K, Hibino K, Hiranuma K, Negoro T. EMG activities of two heads of the human lateral pterygoid muscle in relation to mandibular condyle movement and biting force. J Neurophysiol 2000;83:2120–37. 17. Murray GM, Phanachet I, Uchida S, Whittle T. The role of the human lateral pterygoid muscle in the control of horizontal jaw movements. J Orofac Pain 2001;15. p. 279–92; 292–305, Review. 18. Murray GM, Phanachet I, Uchida S, White T. The human lateral pterygoid muscle: a review of some experimental aspects and possible clinical relevance. Aust Dent J 2004;49:2–8. Review. 19. Ostry DJ, Gribble PL, Levin MF, Feldman AG. Phasic and tonic stretch reflexes in muscles with few muscle spindles: human jaw-opener muscles. Exp Brain Res 1997;116: 299–308. 20. van der Bilt A, Ottenhoff FAM, van der Glas HW, Bosman F, Abbink JH. Modulation of the mandibular stretch reflex sensitivity during various phases of rhythmic open-close movements in humans. J Dent Res 1997;76:839–47. 21. Dworkin SF, LeResche L. Research diagnostic criteria for temporomandibular disorders. Review, criteria, examinations and specifications, critique. J Craniomandibular Disord Facial Oral Pain 1992;6:301–55. 22. Miles TS, Poliakov AV, Flavel SC. An apparatus for controlled stretch of human jaw-closing muscles. J Neurosci Methods 1993;46:197–202. 23. Wood WW, Takada K, Hannam AG. The electromyographic activity of the inferior part of the human lateral pterygoid muscle during clenching and chewing. Arch Oral Biol 1986;31:245–53. 24. Widmalm SE, Lillie JH, Ash Jr MM. Anatomical and electromyographic studies of the digastric muscle. J Oral Rehabil 1988;15:3–21. 25. Svensson P, Bak J, Troest T. Spread and referral of experimental pain in different jaw muscles. J Orofac Pain 2003;17:214–23. 26. Svensson P, De Laat A, Graven-Nielsen T, Arendt-Nielsen L. Experimental jaw-muscle pain does not change heteronymous H-reflexes in the human temporalis muscle. Exp Brain Res 1998;121:311–8. 27. Murray GM, Klineberg IJ. Electromyographic recordings of human jaw-jerk reflex characteristics evoked under standardized conditions. Arch Oral Biol 1984;29:537–49.
570
archives of oral biology 52 (2007) 562–570
28. Cruccu G, Frisardi G, van Steenberghe D. Side asymmetry of the jaw jerk in human craniomandibular dysfunction. Arch Oral Biol 1992;37:257–62. 29. Goldberg LJ. The effect of jaw position on the excitability of two reflexes involving the masseter muscle in man. Arch Oral Biol 1972;17:565–76. 30. Kimura J, Daube J, Burke D, Hallett M, Cruccu G, Ongerboer de Visser BW, et al. Human reflexes and late responses. Report of an IFCN committee. Electroencephalogr Clin Neurophysiol 1994;90:393–403. 31. Cooker HS, Larson CR, Luschei ES. Evidence that the human jaw stretch reflex increases the resistance of the mandible to small displacements. J Physiol (Lond) 1980;308:61–78. 32. Buchner R, Brouwers JE, van der Glas HW, Bosman F. The bilateral amplitude imbalance in the jaw-jerk reflex after a transient mandibular load in patients with myogenous craniomandibular disorders as compared with normal subjects. In: van Steenberghe D, De Laat A, editors. Electromyography of jaw reflexes in man. Leuven, Belgium: Leuven University Press; 1989. p. 377–88. 33. Wang K, Arendt-Nielsen L, Svensson P. Capsaicin-induced muscle pain alters the excitability of the human jaw-stretch reflex. J Dent Res 2002;81:650–4. 34. Wang K, Arendt-Nielsen L, Jensen T, Svensson P. Reduction of clinical temporomandibular joint pain is associated with a reduction of the jaw-stretch reflex. J Orofac Pain 2004;18:33–40. 35. Cairns BE, Wang K, Hu JW, Sessle BJ, Arendt-Nielsen L, Svensson P. The effect of glutamate-evoked masseter muscle pain on the human jaw-stretch reflex differs in men and women. J Orofac Pain 2003;17:317–25. 36. Hellsing G. Human jaw muscle motor behaviour. II. Reflex and receptor mechanisms. Swed Dent J 1988;12:47–56. 37. Hannam AG, Matthews B, Yemm R. Receptors involved in the response of the masseter muscle to tooth contact in man. Arch Oral Biol 1970;15:17–24. 38. van der Glas HW, De Laat A, Carels C, van Steenberghe D. Interactive periodontal and acoustic influences on the masseteric post-stimulus electromyographic complex in man. Brain Res 1988;22:284–94. 39. Sessle BJ, Schmitt A. Effects of controlled tooth stimulation of jaw muscle activity in man. Arch Oral Biol 1972;17: 1597–607. 40. Goldberg LJ. Masseter muscle excitation induced by stimulation of periodontal and gingival receptors in man. Brain Res 1971;32:369–81. 41. Clark GT, Goldberg LJ. Factors influencing the excitatorymasseteric reflex evoked by gingival electrical stimulation in man. Arch Oral Biol 1983;28:1055–8. 42. Poliakov AV, Miles TS. Stretch reflexes in human masseter. J Physiol (Lond) 1994;476:323–31. 43. Lobbezoo F, Verheij JG, Naeije M. Influence of periodontal receptors on the jaw-jerk reflex amplitude in man. Eur J Oral Sci 2001;109:40–3. 44. Erkelens CJ, Bosman F. Influences of periodontal and mandibular-joint receptors on reflex sensitivity of human jaw-closing muscles. Arch Oral Biol 1985;30:450–545. 45. Clark GT, Carter MC. Electromyographic study of human jaw-closing muscle endurance, fatigue and recovery at various isometric force levels. Arch Oral Biol 1985;30: 563–9. 46. Junge D, Clark GT. Electromyographic turns analysis of sustained contraction in human masseter muscles at various isometric force levels. Arch Oral Biol 1993;38:583–8.
47. Gay T, Maton B, Rendell J, Majourau A. Characteristics of muscle fatigue in patients with myofacial pain-dysfunction syndrome. Arch Oral Biol 1994;39:847–52. 48. Goto TK, Langenbach GE, Hannam AG. Length changes in the human masseter muscle after jaw movement. Anat Rec 2001;262:293–300. 49. Murray GM, Phanachet I, Hupalo M, Wanigaratne K. Simultaneous recording of mandibular condylar movement and single motor-unit activity at verified sites in the human lateral pterygoid muscle. Arch Oral Biol 1999;44:671–82. 50. Matthews PB, Stein RB. The sensitivity of muscle spindle afferents to small sinusoidal changes of length. J Physiol (Lond) 1969;200:723–43. 51. Mao J, Osborn JW. Direction of a bite force determines the pattern of activity in jaw-closing muscles. J Dent Res 1994;73:1112–20. 52. Blanksma NG, van Eijden TM. Electromyographic heterogeneity in the human temporalis and masseter muscles during static biting, open/close excursions, and chewing. J Dent Res 1995;74:1318–27. 53. Dean JS, Throckmorton GS, Ellis III E, Sinn DP. A preliminary study of maximum voluntary bite force and jaw muscle efficiency in pre-orthognathic surgery patients. J Oral Maxillofac Surg 1992;50:1284–8. 54. Manns A, Miralles R, Guerrero F. The changes in electrical activity of the postural muscles of the mandible upon varying the vertical dimension. J Prosthet Dent 1981;45: 438–45. 55. Mackenna BR, Turker KS. Jaw separation and maximum incising force. J Prosthet Dent 1983;49:726–30. 56. Lindauer SJ, Gay T, Rendell J. Effect of jaw opening on masticatory muscle EMG-force characteristics. J Dent Res 1993;72:51–5. 57. Morimoto T, Abekura H, Tokuyama H, Hamada T. Alteration in the bite force and EMG activity with changes in the vertical dimension of edentulous subjects. J Oral Rehabil 1996;23:336–41. 58. Paphangkorakit J, Osborn JW. Effect of jaw opening on the direction and magnitude of human incisal bite forces. J Dent Res 1997;76:561–7. 59. Christensen J. Effect of occlusion-raising procedures on the chewing system. Dent Pract Dent Rec 1970;20:233–8. 60. Hellsing E. Increased overbite and craniomandibular disorders—a clinical approach. Am J Orthod Dentofacial Orthop 1990;98:516–22. 61. Lund JP. Mastication and its control by the brain stem. Crit Rev Oral Biol Med 1991;2:33–64. 62. Trulsson M, Johansson RS. Orofacial mechanoreceptors in humans: encoding characteristics and responses during natural orofacial behaviors. Behav Brain Res 2002;135:27–33. 63. Zhang W, Kobayashi M, Moritani M, Masuda Y, Dong J, Yagi T, et al. An involvement of trigeminal mesencephalic neurons in regulation of occlusal vertical dimension in the guinea pig. J Dent Res 2003;82:565–9. 64. Yabushita T, Zeredo JL, Toda K, Soma K. Role of occlusal vertical dimension in spindle function. J Dent Res 2005;84:245–9. 65. Abduljabbar T, Mehta NR, Forgione AG, Clark RE, Kronman JH, Munsat TL, et al. Effect of increased maxillo-mandibular relationship on isometric strength in TMD patients with loss of vertical dimension of occlusion. Cranio 1997;15:57–67. 66. Hagag G, Yoshida K, Miura H. Occlusion, prosthodontic treatment, and temporomandibular disorders: a review. J Med Dent Sci 2000;47:61–6.