1Department of Physiology, 2First Department of Prosthodontics, and 3Department of Orthodontics, School of Dentistry, Aichi-Gakuin University, Chikusa 1-100, Nagoya 464-8650, Japan
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ABSTRACT |
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Hiraba, Katsunari, Kazuto Hibino, Kenji Hiranuma, and Takefumi Negoro. EMG Activities of Two Heads of the Human Lateral Pterygoid Muscle in Relation to Mandibular Condyle Movement and Biting Force. J. Neurophysiol. 83: 2120-2137, 2000. Electromyographic (EMG) activities of the superior (SUP) and inferior heads (INF) of the lateral pterygoid muscle (LPT) were recorded in humans during voluntary stepwise changes in biting force and jaw position that were adopted to exclude the effects of acceleration and velocity of jaw movements on the muscle activity. The SUP behaved like a jaw-closing muscle and showed characteristic activity in relation to the biting force. It showed a considerable amount of background activity (5-32% of the maximum) even in the intercuspal position without teeth clenching and reached a nearly maximum activity at relatively lower biting-force levels than the jaw-closing muscles during increment of the biting force. Stretch reflexes were found in the SUP, the function of which could be to stabilize the condyle against the biting force that pulls the condyle posteriorly. This notion was verified by examining the biomechanics on the temporomandibular joint. The complex movements of the mandibular condyle in a sagittal plane were decomposed into displacement in the anteroposterior direction (Ac) and angle of rotation (RAc) around a kinesiological specific point on the condyle. In relation to Ac, each head of the LPT showed quite a similar behavior to each other in all types of jaw movements across all subjects. Working ranges of the muscle activities were almost constant (Ac <3 mm for the SUP and Ac >3 mm for the INF). The amount of EMG activity of the SUP changed in inverse proportion to Ac showing a hyperbola-like relation, whereas that of the INF changed rather linearly. The EMG amplitude of the SUP showed a quasilinear inverse relation with RAc in the hinge movement during which the condyle rotated with no movement in the anteroposterior direction. This finding suggests that the SUP controls the angular relationship between the articular disk and the condyle. On the other hand, the position of the disk in relation to the maxilla, not to the condyle, is controlled indirectly by the INF because the disk is attached to the condyle by tendinous ligaments.
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INTRODUCTION |
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The grinding movement of the mandible is a most important movement in mastication and requires a bilaterally distinct pattern of action of the temporomandibular joint (TMJ). On the working side where the food is crushed between the upper and lower molars, stiffness of the TMJ is required. The mandibular condyle must be kept stable in the temporomandibular fossa against the biting force produced by the jaw closing muscles. In contrast, on the contralateral nonworking side, the condyle has to move widely and smoothly in the medioanterior direction. In addition, the coordinated movements of the condyle and the articular disk are necessary for smooth movements of the mandible.
In these movements of the TMJ, the lateral pterygoid muscle (LPT) plays
a crucial role. The LPT has two heads, the superior (SUP) and inferior
(INF) heads in man and monkey. The SUP originates from the
infratemporal fossa and is inserted mainly into the articular disk of
the TMJ, whereas the INF arises from the lateral surface of the lateral
pterygoid plate and is inserted into the condylar neck of the mandible
(Heylings et al. 1995; Honée 1972
;
Ress 1954
; Schmolke 1994
;
Wilkinson 1989
). On the basis of such anatomic arrangements of the two heads, it has long been believed that the SUP
and INF are synchronously active only during jaw opening to displace
anteriorly the disk and the condyle, respectively. However, the
electromyographic (EMG) activities obtained by Kamiyama (1961)
in man and McNamara (1973)
in the monkey
disagree with this view. The SUP was active mainly during clenching of
the teeth and the INF during jaw opening, suggesting nonsynchronous
functioning of the two heads in the movements of the condyle and the disk.
A number of EMG studies on the LPT suggest that the SUP functions like
a jaw-closing muscle, whereas the INF functions like a jaw-opening
muscle (Gibbs et al. 1984; Lehr and Owens
1980
; Luschei and Goodwin 1974
; Mahan et
al. 1983
; Miller et al. 1982
; Sessle and
Gurza 1982
; Widmalm et al. 1987
; Wood et
al. 1986
). However, the EMG patterns of either head of the LPT
reported in these studies are quite variable. Furthermore none of them
has analyzed the EMG in relation to the condylar movement.
Because of the deep location and small size of the LPT, it is difficult
to place the electrodes correctly in the target head. Even with a
careful stereotaxic technique, the electrode advanced toward the SUP or
INF is misplaced easily in or very close to the head, which is not the
target. It is not surprising that previously reported EMG patterns of
each head are markedly different. Actually, McNamara
(1973) stated that the EMG patterns differed widely depending on the position of the electrodes in the LPT. In living humans, however, there is no reliable means for confirming electrode placement. Accordingly, it would be practicable to select the EMG data on the
basis of the EMG pattern rather than the position in the LPT from which
the EMG is recorded and then to analyze the pattern-identified EMG
activities in relation to the oral functions, such as biting force and
movements of the incisor and condyle of the mandible.
The movement of the human mandibular condyle is rather complex because
rotational condylar movement is more or less associated with
displacement of the condyle. The trajectory of condylar movement shows
a wide variation depending on the position of the reference point on
the condyle. However, a simple jaw-opening, -closing movement on the
sagittal plane can be decomposed into displacement and rotation by the
use of the "kinematic axis," which connects a specific point on the
condyle on both sides (Kohno and Ishiwara 1971;
Yatabe et al. 1995
). It was reported that the trajectory of condylar movement with reference to the kinematic axis showed a
narrow belt-shaped form, the width of which was 0.7 mm on the average.
The mandibular movement on the sagittal plane consists of a rotation
around the axis and the displacement of this axis. If the rotational
angle of the condyle is calculated with reference to that specific
point, it will be possible to reconstruct the jaw movement two
dimensionally in the sagittal plane on the basis of two parameters:
displacement of the condyle and "rotational angle of the condyle" (RAc).
The purpose of the present study is to investigate the roles of the SUP and INF in controlling the condylar movement and in stabilization of the condyle against the biting force in humans. For this purpose, coordination of the activities of the SUP with those of the jaw-closing muscles, masseter and temporalis muscles, was investigated during a controlled biting task, and the activities of the two heads of the LPT were analyzed in relation to the jaw-movement parameters, such as anterior displacement of the condyle (Ac) and RAc during a stepwise mode jaw-positioning task. We designed the jaw-positioning task in a stepwise manner so that the effect of movement velocity on the EMG activity was negligible. The functional significance of the two heads of the LPT was ascertained by the findings on the biomechanical properties of the TMJ investigated in cadavers. In addition to the EMG data in voluntary movements, stretch reflex responses of the two heads of the LPT were compared with those of the jaw closing muscles.
A part of this study appeared in an abstract form (Hiraba et al.
1991).
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METHODS |
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Subjects and sessions
The subjects were seven male volunteers aged 27-33 yr. All the subjects had normal and complete dentition and no history of mandibular dysfunction. They gave informed consent to this study. The experiments were conducted in accord with the Code of Ethics of the World Medical Association (Declaration of Helsinki) for Human Experimentation.
The present study consisted of two series of experiments carried out on separate days. The main point of the first series was to examine the coordination pattern of the SUP with the jaw-closing masseter and temporalis muscles during biting tasks and to compare the reflex responses of the two heads with those of these jaw-closing muscles during stretching of the respective muscle. The second series aimed at analyzing the relationship between the condyle movement and the EMG activities of the two heads recorded simultaneously, especially during three types of stepwise changes in jaw position. In both experimental series, several kinds of jaw movements and tasks were performed to reveal the basic characteristics of the EMG activity of each head: movements of jaw opening and closing, anteroposterior, lateral, clenching, and chewing, and tasks of stepwise changes in jaw position and biting force. These movements and tasks were performed in this order. In some cases, hinge jaw-opening, -closing movements were added to the habitual movements.
EMG recording
In the first series, bipolar surface electrodes (interpolar distance: 2.5 cm) were placed on the skin over the masseter and temporalis muscles. The activities of these muscles were recorded simultaneously with those of the SUP, and of the INF in a few cases, on the subject's habitual chewing side. In the second series, EMG recordings were made from the unilateral SUP and INF.
To record a well-isolated EMG activity of each head of the LPT, the
proximal part of the LPT, 0.5-1.5 cm from the origin, was selected as
the recording site because at this region the cross-sectional area of
the SUP is maximum and the muscle bellies of the SUP and INF clearly
are separated by a septum of connective tissue (Widmalm et al.
1987).
To precisely insert the recording electrode into the SUP and INF region, we developed a stereotaxic method. A hypodermic needle (60 mm in length, 23 gauge) containing two fine wire electrodes (ø 60 µm) was inserted extraorally from the mandibular incisure toward the LPT. The tips of the two fine wire electrodes were exposed by 0.5 mm, and one was bent back at 5 mm and the other at 3 mm from the tip. The needle for the INF was directed parallel to both the coronal and horizontal planes, and that for the SUP was inclined by 20° to the horizontal plane. For stereotaxic control of electrode orientation a face-bow was applied to the head of the subject (Fig. 1A). This method was established by anatomic identification of the injected dye spots in 12 cadavers. The insertion point on the skin over the mandibular incisure was 40 mm anterior to the center of the external acoustic meatus and 5 mm below the Camper plane (naso-auricular plane) for the SUP and 5 mm below the SUP point for the INF. The needle was advanced medially until its tip made contact with a bony structure and then pulled back 5 mm to inject dye. The dye spots were correctly placed in 11 of 12 SUPs and in all of 12 INFs (Fig. 1B).
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The subject sat in a dental chair with a headrest. To minimize
artifacts in EMG recordings and dislocation of the electrodes by
condylar movements, the subject was instructed to open the jaw
maximally and then the electrode was inserted anterior to the
mandibular condyle, which was maintained at the anterior-most position
(Mahan et al. 1983). At the end of the first recording, the tip of the indicator bar of the face-bow was clamped at the insertion point on the skin as the landmark for insertion of the electrodes in subsequent recordings. The distance from the surface of
the skin to the recording point of the SUP was 42-48 mm (46.5 on
average) and 35-50 mm (46.0) for the INF.
STEPWISE CHANGE IN JAW POSITION AND BITING FORCE. The vertical component of the position of the lower incisor was displayed on the oscilloscope in front of the subject. The most closed jaw position at which all posterior teeth contact with opposing molars by means of cusps and fossae is referred to as the intercuspal position (ICP). In the ICP, the mandible is fixed in the anteroposterior and lateral as well as vertical directions. From the ICP, the subject was asked to open the jaw by an amount corresponding to the distance between two horizontal grid lines of the oscilloscope and keep the position as steadily as possible for ~2 s by the aid of visual feedback of the jaw position. In the next step, the subject opened the jaw wider in the same manner. Thus the subjects changed the jaw position in a stepwise manner throughout the range between the intercuspal and the maximally open positions (stepwise jaw-movement task). The activities of the SUP were characterized by the presence of background activity in the ICP and its rapid change in inverse proportion to interincisal distance in a range of 10-15 mm. This range corresponded to a very narrow range, 3-5 mm of Ac. To examine the relation of the SUP EMG to the Ac in detail, the amount of stepwise change in jaw position must be small, especially near the ICP. Therefore at the jaw positions near the ICP, the incisor position was monitored on the oscilloscope with a high gain in which one step corresponded to an interincisal distance of ~1.0 mm. At nearly maximally open positions, interincisal distance was monitored with a low gain in which one step corresponded to a distance of ~5.0 mm. At the intermediate jaw positions, one step corresponded to an interincisal distance of ~2.0 mm.
In addition to the habitual stepwise jaw movements, two different modes of stepwise movements were performed in the second series. In the "intent-retrusive jaw-opening -closing movement" (Int-Ret JM), the subject moved the jaw while paying attention so as to maintain the position of the condyle at the ICP as much as possible particularly in the early stage of jaw-opening and the late stage of jaw-closing movements. In the "intent-protrusive jaw-opening, -closing movement" (Int-Pro JM), the subjects moved the jaw while paying attention so as to protrude the condyle as much as possible in the same stages as in the Int-Ret JM. The subject changed the biting force stepwise, as in the stepwise jaw-movement task, between 0 and ~80% of the maximum biting force under visual feedback from the oscilloscope on which the biting force was displayed linearly. Each step lasted ~2 s (stepwise biting task). The maximum biting force was measured in advance by the use of metal biting plates (see following text) without insertion of EMG recording electrodes.STRETCH REFLEXES. To stretch the LPT, pressure was applied to the menton with the thumb by an experimenter in the posterosuperior direction so that the mandible was passively moved posteriorly. In this test, the metal biting plates were not in place, and the subject was instructed to be relaxed and to take a rest position of the mandible. The stretch reflex-like response of the SUP that was elicited by tapping the menton was compared with the stretch reflexes simultaneously recorded in the masseter and temporalis muscles. The menton tapping was done with an electrically controlled mechanical stimulator. The duration and interval of stimulus were controlled: 5 ms in duration, 30 stimuli at 1-s intervals (Dia Medical System, DPS-250 SH). To monitor tapping force, a force transducer was attached at the tip of the mechanical stimulator. Magnitude of displacement of the stimulator probe was adjusted so that the tapping force was ~4.9 N (500g weight) in each trial.
Monitoring jaw movements
In the first series, the movement of the incisor point was monitored three dimensionally by detecting the position of a small magnet (6 × 13 mm, 3-mm thick) attached to the labial surface of the lower central incisors. The sensors were mounted on an eyeglass frame (Myo-tronics, MKG system, K5).
In the second series, the movements of the central incisor and condyle of the mandible were recorded on the sagittal plane, with two semiconductor-position detectors responding to infrared ray from light-emitting diodes (LEDs). The position detectors were mounted on the subject's head with a headgear (Tokyo-Shizaisha, Saphon Visi-traner system, C-II). The minimum detection sensitivity was <0.01 mm, and a rectilinear relation between the position and the output of the detector was <2%. The LED carrier was fixed to the labial surface of the lower anterior teeth with cyanoacrylate (Fig. 1C). One LED was placed 3 cm anterior to the lower central incisor on the occlusal and mid-sagittal planes, and an additional LED was 4 cm lateral to the skin over the mandibular condyle. The position of the LED on the condyle was adjusted to minimize the difference in the forward and backward courses of the LED during tapping and opening-closing movements. The kinesiological reference point was determined ultimately by computer simulation of the mandibular movements as described in the following text.
At the end of each recording trial, a 20-mm-thick wooden stick was interposed between the upper and lower incisors. By means of interpolation and extrapolation of the output value from the jaw tracking system at 20 mm jaw opening, the "vertical displacement of the incisor" (Vi) at any jaw position was calculated as interincisal distance in millimeters. Because there is no serious disparity between the actual condylar position and LED position on the sagittal plane during simple jaw-opening, -closing movements, the displacement of the condyle was represented as that of the LED.
Measurements of biting force
In the stepwise biting task, two metal biting plates similar to
those used in dental clinics for the intraoral gothic arch tracing
(Bailey and Winkler 1979) were fixed on the maxillary and mandibular dentition with cyanoacrylate. The upper plate had a
screw in the center of the plate, and only the tip of the screw made
contact with the lower plate so that on biting the opposing teeth were
apart by 2-3 mm interincisal distance. A strain gauge was attached to
the upper plate. The output of the strain gauge amplifier was linear
490 N (50 kg). To measure the biting force at a fixed jaw position
that corresponded to the ICP, the position was determined previously by
the gothic arch tracing method (Bailey and Winkler
1979
). A dimple was drilled at this position on the lower
plate. When biting, the subject was asked to fit the tip of the screw
to the dimple.
Dissection of the temporomandibular joint and the LPT muscle in cadavers
In 12 cadavers, after removing the temporalis muscle and
coronoid process, the lateral surface of the LPT was exposed. The condyle with the attaching disk, disk ligaments, and LPT was isolated from the glenoid and infratemporal fossae by dissecting the peripheral surrounding tissue of the superior joint space, the posterior bilaminar
zone, and the origin of the LPT at the lateral pterygoid plate
(Wilkinson 1989). The cut ends of the bellies of the SUP and INF were pulled manually, and the effects on the positions of the
disk and condyle were examined visually.
Data analysis
The data were stored on six-channel FM tapes driven at 9.5 cm/s (flat frequency response: 0-1.25 kHz), and played back on an eight-channel thermal array recorder (Nippon Denki Sanei, 8 M24).
The data of rectified and low-pass filtered (7 Hz low-pass, 24 dB/oct) EMGs of tested muscles, jaw positions, and biting force were fed into a personal computer (NEC, PC-9801 VX) through an A/D converter (sampling at 100 Hz, 12-bit resolution). The mean values of the rectified EMG amplitude, the incisal and condylar positions, and the biting force were determined during the steady state at each step of the stepwise motor tasks. The mean amplitude of the EMG activity was expressed as a percentage of that recorded during maximal clenching of the teeth for the SUP, masseter, and temporalis muscles and during maximal jaw opening for the INF. The raw EMG responses to taps of the menton were A/D converted (sampling at 10 kHz, 12-bit resolution) and averaged 30 times using the onset of tapping as the trigger.
ROTATIONAL ANGLE OF THE CONDYLE. The trajectories of the incisor and condyle on the sagittal plane were visualized as lines connecting the points representing the mean values of consecutive steps. The mandibular movement on the sagittal plane was computer-simulated by originally designed software simulating the movement of a right triangle, in which the incisor and condylar points were represented by its two apexes (Fig. 2). Using this computer simulation of the mandibular movements, fine adjustment of the position of the kinesiological reference point on the condyle was carried out by trial and error so that the trajectories of the condyle showed the narrowest belt-shaped configuration throughout stepwise opening-closing movements. By the use of this point as the kinesiological point, the RAc was calculated, and then the condyle movements were transformed into two-dimensional movements (compound condyle movements, CCM), by using the RAc and Ac as the two axes of coordinates.
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RESULTS |
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Classification of EMG patterns of the LPT
A total of 47 EMG records were obtained from the two heads. In the first series, EMG recordings were made from 15 SUPs and 4 INFs. In the second series, 14 pairs of EMGs were simultaneously recorded from the SUP and INF. Recordings were made two to eight times in each subject.
A wide variety of EMG patterns was observed even in the same subject when the insertion of the electrodes was made on different days. The patterns were classified into four types on the basis of EMG activities of the SUP and INF during jaw-opening, -closing movements. A pattern, in which strong activity appeared only in the closing phase, but no activity in the opening phase, was classified as CL type. The closing phase is the period from the most-opened position to the most-closed position; the opening phase is the period from the most-closed position to the most-opened position. In contrast, a pattern in which strong activity appeared only in the opening phase, with no activity in the closing phase was classified as OP type. The remaining intermediate types, in which EMG activities were found in both phases were classified as either CL>OP type or OP>CL type depending on the phase in which larger EMG activity was present.
Table 1 shows an example of variation of the EMG pattern of the SUP and INF observed in the same subject. In some subjects, all three types of SUP EMG activities, except for the OP type, could be recorded on different days. Among the types of the SUP, no OP type was found in any subject, and the majority was the CL type (59%, Table 2). Among the types of the INF, the majority was the OP type (61%, Table 2). The SUP of the CL type could be recorded at least once in each subject and the INF of the OP type in six of seven subjects. Occurrence of CL>OP and OP>CL types, regardless of SUP and INF, was not restricted to specific subjects. Such deviation of incidence of each EMG type depends significantly on the position of the electrodes in the LPT (Probability was finally estimated by Fisher's exact probability test: P < 0.01). In the following description, we use, instead of "SUP" and "INF", the terms "stereotaxic SUP" (str-SUP) and "stereotaxic INF" (str-INF). This is because although we believe that we often have recorded genuine activity patterns of the SUP and INF, in some cases the records seemed to be a mixture of the activities of the two heads.
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First we will present the typical features of the CL type of the str-SUP and the OP type of the str-INF. Then the EMG activities of the other types of the str-SUP and str-INF will be shown.
Figure 3 shows examples of simultaneously recorded EMGs of the str-SUP of the CL type and str-INF of the OP type. The str-SUP had a tonic background activity at the rest position of the mandible as well as in the ICP. This background activity disappeared during jaw-opening (Fig. 3A), anterior (Fig. 3C), and contralateral movements (Fig. 3D), whereas the activity increased or persisted during jaw-closing (Fig. 3A), posterior (Fig. 3C), and ipsilateral movements (Fig. 3D). In contrast, the str-INF showed no activity at all in the ICP but was strongly active during jaw-opening (Fig. 3A), anterior (Fig. 3C), and contralateral movements (Fig. 3D). It showed no activity during jaw-closing (Fig. 3A), posterior (Fig. 3C), and ipsilateral movements (Fig. 3D). During chewing of gum, the two heads of the LPT showed, regardless of the chewing side, a completely reciprocal and monophasic burst activity. The str-SUP was active only in the jaw closing phase, and the str-INF in the jaw opening phase (Fig. 3B). Thus the str-SUP of the CL type and str-INF of the OP type are active clearly in a reciprocal manner during various kinds of movements as well as during chewing.
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Figure 4 shows EMG activities of the str-SUP of the CL type recorded simultaneously with the masseter and temporalis muscles during jaw-opening, -closing movements, chewing, and clenching of the teeth. In these movements, the str-SUP was always active synchronously with those of the jaw closing muscles.
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Figure 5 shows an example of EMG activities of the str-INF classified as the OP type (Fig. 5A), but its EMG activity was present not only in the opening phase but also in the closing phase during chewing (Fig. 5B) as if it was the OP>CL type. This means that the jaw-opening, -closing movement alone is not suitable to test whether the str-INF EMG record is contaminated by the EMG activity of high-threshold motor units in the str-SUP that are to be active only during chewing and clenching in which a greater activity of the str-SUP is required. Therefore we tested whether the str-INFs of the OP type show activities in the closing phase of chewing or not. As the result, smaller amplitude EMGs were found in the closing phase of chewing in 5 of 11 str-INF EMGs of the OP type that were classified based on the activity during jaw-opening, -closing movements.
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If not specifically mentioned, the OP type of str-INF referred to in the following paragraphs showed negligible EMG activity in the closing phase of chewing.
Relationships of the EMG amplitude of the str-SUP to the biting force and interincisal distance
During the stepwise increment of biting force, the EMG activity of the str-SUP increased rapidly to reach a quasiplateau earlier than that of the masseter muscle in which the rate of increase in EMG activity to the increase in biting force was low at lower biting force levels and became progressively higher at higher biting force levels (Fig. 6, A and B). The results obtained from four subjects in 10 recording sessions are shown collectively in Fig. 6, C and D. The str-SUP was clearly different from the masseter and temporalis muscles in that it showed a substantial background activity in the ICP (Vi = 0, 5-32% of the maximum; Fig. 6C). Because the metal biting plates caused jaw opening by 2-3 mm, the EMG amplitude at biting force = 0 was usually lower than that in the ICP without clenching.
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When the subject started to open the jaw, the background activity of
the str-SUP in the ICP diminished rapidly and disappeared at ~5 mm Vi
(offset point, i.e., the jaw position at which the EMG activity
disappears; Fig. 7, left,
). In the jaw-closing phase, however, the EMG activity reappeared at
20 mm Vi (onset point, i.e., the jaw position at which the EMG activity
reappears; Fig. 7, left,
). In the Int-Ret JM (Fig. 7,
right), which was performed with a slower velocity, the
disparity of these two points was smaller. The onset and offset points
of the str-INF were, regardless of the type of movement, very close to
the offset and onset points of the str-SUP, respectively.
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To exclude the effect of velocity of jaw movements on the onset and offset points, muscle activities of the two heads were examined in stepwise jaw movements. Figure 8 shows three types of stepwise jaw movements and EMG activities recorded in the same subject. Because the magnitude of each step in Vi was controlled by visual feedback of the output of the jaw tracking system, the trajectories of Vi of the opening and closing phases were symmetric. In contrast, those of Ac were widely different among the stepwise movements.
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In the stepwise habitual movement (Fig. 8, left), the wide disparity of the offset and onset points of the str-SUP still remained. However, in the stepwise Int-Ret JM (Fig. 8, middle), there was no appreciable difference between these points. They were roughly equal at ~20 mm Vi. In this stepwise Int-Ret JM, both the opening and closing movements within 20 mm Vi were pure rotation because of no measurable change in Ac (shown by 2 segments of a horizontal line in the middle of the panel). During this rotational movement of the mandible, the mean amplitude of the str-SUP was nearly inversely proportional to Vi. On the other hand, in the Int-Pro JM (Fig. 8, right), the offset point of the str-SUP shifted to 3 mm Vi. Although the presence of a small motor unit of the str-SUP activated at 10 mm in the closing phase made the onset point of the str-SUP at 10 mm Vi, it was apparent that the major part of the working period of the str-SUP was restricted in a narrower range of Vi than the other types of movements.
Regardless of the type of movement, the onset and offset points of the str-INF changed in parallel with the corresponding points of the str-SUP. The activity of the str-INF increased in parallel with the amount of Ac. For example, in the stepwise Int-Pro JM (Fig. 8, right), both the offset point of the str-SUP and onset point of the str-INF in the opening phase shifted to 3 mm Vi so that the working period of the str-SUP became shorter and that of the str-INF longer. The activity of the str-INF showed a very similar profile with the trajectories of the Ac.
These findings strongly suggest that the disparity of the onset and offset points of the str-SUP and str-INF that typically was found in the habitual movements are attributable to the difference in the mandibular movements performed in opening and closing phases. In addition, it appears that muscle activity of the str-SUP may be primarily correlated with rotation of the condyle and that of the str-INF may be correlated with Ac.
Correlation coefficients of the EMG activities of the str-SUP and str-INF to jaw-movement parameters
To estimate the correlation between the EMG activities of the two heads and the jaw-movement parameters, the "mean amplitude of the EMG activities of the str-SUP (EMGSUP) and str-INF (EMGINF)" in each step during stepwise movements was plotted against the Vi, Ac, and RAc. Figure 9 shows examples during the stepwise habitual movement. There are significant correlations between the EMG activities of the two heads and the jaw movement parameters. The EMGINF is positively and the EMGSUP is negatively correlated with all three parameters (Table 3).
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Correlation coefficients also were estimated during Int-Ret JM. In this
type of movement, there was a tendency that correlation coefficients of
the EMGSUP with Ac were weaker than in the
stepwise habitual movement, and in some cases they were nonsignificant. Even in these cases, however, EMGSUP still
exhibited a significant correlation to the RAc as well as Vi. In every
case, regardless of jaw-movement type, Vi strongly correlated with RAc
with correlation coefficients 0.98. These findings indicate that the
significant high correlation between the EMGs and Vi is attributable to
this inherent correlation of Vi with RAc and that
EMGSUP correlates primarily with RAc.
Relationships of EMG activities of the str-SUP and str-INF to movements of the incisor and condyle
To study the relationships of the EMG activities of the two heads of the LPT to the movements of the incisor and condyle, the trajectories of the incisor and condylar points were imposed on the sagittal view of the mandible (Fig. 10, middle). In association with their sagittal movements, EMGSUP and EMGINF were plotted against the Vi and Ac, individually. With respect to Vi, EMGSUP and EMGINF were plotted by taking the Vi as the downward-ordinate and EMG as the abscissa (Fig. 10, bottom); with respect to Ac, EMGSUP and EMGINF were plotted by taking the Ac as the leftward-abscissa and EMG as the ordinate (Fig. 10, top).
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Figure 10 illustrates an example obtained from a subject. The movements of the incisor point were clearly different among the three types of stepwise movements. In addition, the onset and offset points of the EMG activities of both heads and the curves of the EMGSUP and INF/Vi relations were widely different depending on the types of movement. Although there seemed no appreciable difference in the trajectories of the incisor movements between opening and closing phases of stepwise habitual movements (bottom, dashed and dotted lines, INC), it was found that there was a marked difference in the curves of the EMGSUP/Vi relations between opening and closing phases as well as a wide disparity between the onset and offset points of the SUP.
In spite of wide difference in the movements of the incisor point among
the three types of stepwise movements, the trajectories of the condylar
point were virtually the same (Fig. 10, middle, dashed and
dotted lines, CND). The relationships between the muscle activities of
the two heads and Ac also showed no marked difference among the three
types of jaw movements. EMGSUP plotted against Ac
showed a hyperbola-like relation, and EMGINF was
more or less linear. The working range of the str-SUP was between 0 and
3 mm Ac (shaded area) and that of the str-INF 3 mm Ac (Fig. 10).
Rotation and displacement of the condyle
The reconstructed compound condylar movement (CCM) revealed a clear difference in the mandibular movement between the closing and opening phases in the range <3 mm Ac, i.e., the working range of the str-SUP (Fig. 11, shaded vertical area). In the final closing phase of the stepwise habitual movement (Fig. 11, top), there was no change in Ac (thick lines), indicating that the mandible only rotates in this phase. In contrast, in the initial stage of the opening phase, Ac changed in parallel with RAc (thin lines), indicating that both displacement and rotation of the mandible take place. In the stepwise Int-Ret JM (Fig. 11, middle), the movements in the initial stage of jaw opening and final stage of jaw closing (RAc <8°) were rotation only because there was almost no change in Ac. In the stepwise Int-Pro JM (Fig. 11, bottom), the CCMs in the initial stage of opening and the final stage of closing were accompanied by displacement (shaded vertical area in CCM). As already shown in Fig. 10, it is to be noted that whatever types of jaw movement were performed, the working ranges of the two heads were almost constant (Ac <3 mm for the str-SUP and Ac >3 mm for the str-INF). It could be concluded that the str-SUP and str-INF work with a considerable steady relation to the Ac.
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Individual difference in usage of the str-SUP and str-INF
The jaw movements and EMG activities recorded from three subjects were compared in the jaw-closing (Fig. 12) and -opening (Fig. 13) phases of the stepwise habitual movement. In general, interindividual differences in the relationships between the EMG amplitude and the jaw-movement parameters, especially Vi and RAc, were larger in the closing phase than in the opening phase. In addition, the positions of the onset and offset of the EMGs in the jaw-closing phase were markedly different among the subjects (Fig. 12).
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Interindividual differences in the CCM performed in the working range of the str-SUP, <5 mm Ac (Fig. 12, shaded area), were also larger in the closing phase than in the opening phase. In subject 1, the late stage of jaw closing was displacement dominant and the final stage was rotation. In subject 2, rotation was followed by final displacement. In subject 3, the final stage consisted of both rotation and displacement. In spite of such wide difference in the CCM, the relations of the str-SUPs to Ac were basically similar, showing a hyperbola-like relation. In addition, the difference in the working range of the str-SUPs was not so large as could explain the wide interindividual difference in the relationship between the EMG amplitude and the jaw-movement parameters. On the other hand, during jaw opening there was no obvious difference in the CCM within the working range of the str-SUP, i.e., Ac <2 mm (Fig. 13, shaded area).
These findings indicate that a wide interindividual difference, such as a different position of the onset and offset points and a resultant different slope of the EMG/Vi and RAc relation lines, is mainly due to the difference in the CCM within the working range of each head but not due to the difference in nature of the LPT itself among the subjects. Consequently, these interindividual differences can be explained by three factors: the period in which the rotational jaw movement occurs, whether this period is within the working range of the str-SUP or without, and whether this period is without of the working range of the str-INF or within.
EMG activities of the other types of str-SUP and str-INF
OP>CL TYPE OF STR-SUP. In the EMGs of the str-SUP in Fig. 14, two or more unitary activities of different amplitude appeared at jaw positions with large Vi. The activities of those units changed in parallel with the Ac and also with the EMG amplitude of the str-INF (Fig. 14C). In addition, bursts of EMG of the str-SUP occurred in the opening phase of chewing (Fig. 14E). However, both the unitary discharges of the str-SUP and the activity of the str-INF disappeared at the level close to ICP during hinge movement (Fig. 14, B and D). The hinge movement was performed with an effort to open the jaw with minimal anteroposterior displacement of the condyle. On the other hand, the background activity of low amplitude near the ICP, which is characteristic of the str-SUP of the CL type, still persisted.
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CL>OP TYPE OF STR-SUP. The tonic background activity of the str-SUP in the ICP persisted during jaw opening (Fig. 15A) as well as the opening phase of chewing (Fig. 15C). During hinge movement, however, the activity of the str-SUP disappeared completely at a relatively small jaw opening (Fig. 15B). The pattern of EMG of the str-INF of this case was basically typical of the OP type.
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OP>CL, CL>OP, AND CL TYPES OF STR-INF. EMG activities of the three types of the str-INFs, OP>CL, CL>OP, and CL types, were basically similar to those of the corresponding types of the str-SUPs, OP>CL, CL>OP, and CL types, respectively.
RELATIONSHIPS OF THE EMG AMPLITUDE TO THE INTERINCISAL DISTANCE AND BITING FORCE IN THREE TYPES OF THE STR-SUP. Figure 16 shows the relationships of the EMG amplitude to the interincisal distance and biting force in three types of the str-SUP. The relations in the range of 10-30 mm Vi were extremely different among the three types of str-SUP, whereas the relations of the EMG amplitude to the biting force and the interincisal distance in the range of 0-10 mm Vi were basically similar. The properties that were commonly observed among three types of str-SUP were the background activity in the ICP, earlier development of almost-maximum EMG activity than either MSS or TMP muscles, and inverse relationship between the EMG and Vi in the range of 0-10 mm Vi. These properties are typical for the str-SUP of the CL type. These results obtained from the intermediate types of EMG strongly suggest that EMG activities of these types, OP>CL and CL>OP types, can be explained reasonably as a mixture of the two distinct reciprocal EMG activities that are characteristics for the str-SUP of the CL type and for the str-INF of the OP type and that they are not the third and fourth groups.
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Stretch reflex
When the mandible was pressed on the menton posteriorly by the experimenter, the condyle usually was displaced passively 1-2 mm in posterosuperior direction. Such passively induced movement of the condyle results in longitudinal stretching of the SUP muscle fibers. Figure 17 shows a stretch reflex-like response elicited in the str-SUP classified as CL type. Such sustained posterior pressing of the jaw evoked vigorous reflex EMG response in the str-SUP.
|
Mechanical tap stimulation of the menton evoked reflex responses in the str-SUP after a latency of 7.7 ± 1.1 ms (mean ± SD, n = 4). The latency of the masseter and temporalis muscles evoked in the same manner was 8.0 ± 1.4 and 7.6 ± 0.7 ms, respectively. Figure 18 shows the responses of the str-SUP of the CL type. The averaged reflex responses were of highest amplitude in the ICP (Fig. 18), became smaller at the moderate jaw opening (Fig. 18, B and C), and disappeared at the maximally open position (Fig. 18D).
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No response was found in the str-INF of OP type in response to either sustained passive jaw retrusion or tap stimulation of the menton.
Biomechanics of the temporomandibular joint
The condylar head is capped with the articular capsule and disk.
The disk has two thick parts (anterior and posterior bands) and a
thinner part (intermediate band) lying between them, like a saddle.
These bands converge to the medial and lateral poles of the condyle and
make ligamental attachment. Although the SUP and INF heads are closer
to each other and finally fused at the region near the condylar neck,
the SUP muscle fibers are inserted into mainly the anterior band of the
disk and the INF is inserted into the condylar neck (Fig.
19E) (Heylings et al.
1995; Honée 1972
; Ress
1954
; Schmolke 1994
; Wilkinson
1989
). The mechanical effect of the contraction of each head on
the positional relationship of the disk to the condyle was quite
different (Fig. 19). Because the articular disk was rigidly attached to
the condyle (Fig. 19, E and F), forward pulling
of the muscle belly of the SUP could not produce any more anterior
displacement of the disk, which was at mandibular rest position, but
resulted in fixing the disk onto the condyle (Fig. 19C).
When the pulled SUP muscle belly was released, the disk could roll back
around the axis across the mediolateral poles of the condyle (Fig. 19,
B, D, and F). It should be noted that
forward pulling of the INF muscle belly had no appreciable effect on
this backward rotational movement of the disk (Fig. 19, B
and D).
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DISCUSSION |
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Although we elaborated the technique for placement of
electrodes precisely in each head of the LPT, the EMG patterns of each head of the LPT were not always reproducible even in the same subject
when examined repeatedly on different days. These EMG activities have
been classified into four types based on their EMG pattern during
jaw-opening, -closing movements. We carefully examined EMG activities
of all types in relation to jaw movements and biting force. The results
indicate that there must be functionally reciprocal components in the
LPT. One is a jaw-closing component, and the other is a jaw-opening
component. Such functionally reciprocal activities typically were found
in the CL type and OP type, respectively. The CL type was recorded from
the topographical SUP region with high incidence (59%) and the OP type
from the INF region (61%). Accordingly we assume that the CL type is
representative of the SUP muscle activity and the OP type is that of
the INF muscle activity. In addition, we also have shown that EMG
activities of other types, OP>CL and CL>OP types, can reasonably be
explained by a mixture of the two distinct reciprocal EMG activities
that are characteristics for the SUP of the CL type and for the INF of
the OP type. It is not likely that the individual difference is
responsible for the OP>CL and CL>OP types because occurrence of these
types of EMG activity was not restricted to specific subjects. The fact
that these various EMG patterns were found even in the same subject
also supports this notion. Circumstantial evidence strongly suggests
that OP>CL and CL>OP types were recorded by the electrodes
inappropriately positioned in the LPT. Consequently it is conceivable
that EMG variation depends critically on the position of the electrodes
in the LPT, as originally claimed by McNamara (1973),
rather than on the anatomic complex, multipinnate muscle structure of
the LPT.
Miller et al. (1982) reported in the monkey that the INF
was active during jaw opening in the range 8-10 mm Vi, whereas the SUP
was active during jaw closing in the range 15 mm Vi. They did not
monitor jaw movements, and the EMG recording was made under the
condition in which the movement velocity could affect the onset point
of the LPT. In a number of previous studies on the EMG of the LPT,
neither the position of the condyle nor biting force was controlled
sufficiently. Particularly was the condyle position ignored.
The present study has analyzed the EMG activities of the two heads of the LPT in relation to the mandibular and condylar movements by using stepwise changes in the jaw position to exclude the influences of velocity of jaw movements. The reconstruction of the complex condylar movement in the form of CCM has enabled us to analyze which factor of the displacement or rotation of the condyle is related primarily to the EMG activity.
Mechanisms for stabilizing the TMJ against biting force
We found that the str-SUP is always coactive with the jaw-closing
muscles during almost every kind of jaw movement and task. However, the
str-SUP is clearly different from the closing muscles with respect to
the biting force and unique in the presence of substantial background
activity as much as 30% of the maximum in the ICP without teeth
clenching. This background activity persisted until interincisal
distance extended beyond 10 mm. Although the presence of background
activity of the SUP was reported by Juniper (1981) in
man, Sessle and Gurza (1982)
in monkeys, and
Kawamura et al. (1968)
in cats, its functional
significance has remained to be clarified.
Grant (1973) has calculated the
mechanical moment of the SUP. In his study, jaw movements were
expressed as a series of successive rotations of the mandible on the
axis of which position changed continuously. The position of the
instantaneous axis of rotation was not always limited in the condyle
but shifted into the ramus of the mandible (Chen 1998
;
Grant 1973
; Koolstra and van Eijden 1997
). Grant (1973)
reported that the human SUP
has a mechanical moment in the closing direction with respect to the
instantaneous axis at rest position.
As confirmed in the dissected TMJ of cadavers in the present
study, the contraction of the SUP fixes the disk to the condyle via the
medial and lateral ligamental attachments and works to pull these
structures as a whole. Development of activity of the str-SUP in
parallel with the biting force level suggests that the str-SUP
stabilizes the condyle in the temporomandibular fossa with its tonic
background activity during the ICP. The str-SUP develops a nearly
maximum activity at relatively low biting-force levels. As a result,
the condyle is pressed strongly against the posterior slope of the
articular eminence and can resist the force pulling the condyle
posteriorly, which is generated by the jaw-closing muscles,
particularly by the temporalis muscle. This notion is strongly
supported by Osborn (1995), who examined the lateral pterygoid muscle activities at the maximum biting force by means of
computer simulation. To set the preparatory stage of the TMJ against
the biting force, it is reasonable that the str-SUP reaches its maximum
activity earlier than other closing muscles.
In combination with such voluntary muscle activity of the str-SUP, the stretch reflex-like response can contribute to maintaining the condyle in the normal position against the force that pulls the condyle posterior during biting and chewing. This is also the case during lateral jaw movements in which the str-SUP and temporalis muscles ipsilateral to the movement direction and the contralateral str-INF and masseter muscles all act as synergists for horizontal rotation of the mandible. The vector of these muscular contraction forces, particularly of the contralateral str-INF and ipsilateral temporalis muscles, functions to displace the ipsilateral condyle laterally and posteriorly. However, during horizontal rotation of the mandible, the str-SUP is so strongly active that the ipsilateral condyle cannot move and stays in the temporomandibular fossa to serve as the axis of horizontal rotation of the mandible (Fig. 20A). It is most likely that the stretch reflex-like response of the str-SUP functions to automatically stabilize the ipsilateral condyle in the temporomandibular fossa during lateral jaw movements, chewing, and biting. Thus the str-SUP and temporalis muscles can be regarded as antagonists in spite of their synchronous activation during various kinds of jaw movements.
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Functions of the str-SUP and str-INF in controlling the condylar movement
It was found that there is a considerable constancy in terms of the range of jaw position when the str-SUP and str-INF are active. The working range of the str-SUP was between 0 and 3-5 mm Ac, and for the str-INF, Ac >2-5 mm. The str-SUP was related inversely with Ac taking a course like a hyperbolic curve, whereas the str-INF correlated with Ac rather linearly. However, the type of jaw movement occurring in that Ac range was widely different among subjects and movement phases even in the same subject. In the subjects whose final stage of closing movement was performed mainly by rotation, the onset point of the str-SUP and the offset point of the str-INF on Vi axis were distant from ICP. In the subjects with a displacement-dominant type of closing, these two points were close to ICP.
The condylar movement requires coordination with that of the articular
disk. As revealed by examining the biomechanical aspects of the SUP,
INF, and articular disk in the present study, the movement of the
articular disk involves rotation on the axis across the mediolateral
poles of the condyle. When the jaw opens, the disk rotates backward
around the condyle. Such positional change of the disk relative to the
condyle is enabled by relaxation of the str-SUP that is tonically
active to fasten the disk onto the condyle in the ICP. Although it is
difficult to describe quantitatively the relative positional changes of
the disk and the condyle, the movements of both the disk and condyle
are rotation only, but in the opposite direction in the hinge movements
during Int-Ret JM. During this rotation, the str-SUP changes its
activity linearly and in inverse proportion to RAc. This suggests that
the str-SUP does not work to change Ac but acts to regulate the angular
relationship between the condyle and disk within its working range
between 0 and 3-5 mm Ac. During Int-Pro JM, however, displacement of
the condyle occurs in addition to its rotation. Although the positional change of the disk associated with displacement of the condyle could
not be directly measured in this study, it is likely that displacement
of the condyle is a principal factor causing the nonlinearity of the
EMGSUP/RAc relation. It can reasonably be concluded that functional significance of the str-SUP for the condylar
movement is to control the relative positional relationship between the
disk and condyle, whereas the position of the disk in relation to the
maxilla, not to the condyle, is controlled indirectly by the str-INF
because the disk is attached to the condyle by tendinous ligaments
(Ress 1954; Schmolke 1994
;
Wilkinson 1989
).
Consequently, the functions of the two heads of the LPT in controlling the movements of the condyle and disk can be summarized as follows. For the jaw to open, the str-SUP has to be relaxed enabling the disk to rotate backward around the condyle. After rotation of the disk, the condyle can rotate around the mediolateral axis (Fig. 20Bb). In this situation activation of the str-INF can move the condyle anteriorly (Fig. 20Bc). At the maximal open position, the str-SUP is completely relaxed and the str-INF is maximally active so that both the condyle and disk are located in the anterior-most position in relation to the maxilla. In this moment, however, the disk is located in the posterior-most position in relation to the condyle (Fig. 20Bd). During jaw-closing movements, the str-INF decreases its activity to allow the condyle to return into the temporomandibular fossa, whereas the str-SUP becomes active to change the position of the disk relative to the condyle.
Stretch reflex
The tap stimulation of the menton has evoked stretch reflex-like
responses in the str-SUP but not in the str-INF. The latency was
comparable to that of the monosynaptic stretch reflex response of the
masseter and temporalis muscles (Goldberg 1971). The
inverse relationship between the interincisal distance and the
amplitude of the reflex responses evoked in the str-SUP, masseter, and
temporalis muscles suggests that these muscles belong to the same
group, i.e., jaw-closing muscles. Stretch reflex-like responses of the LPT have been observed in cats (Kawamura et al. 1968
)
and humans (Widmalm et al. 1987
). In the present
experiment, the amplitude of the EMG of the str-SUP increased in
parallel with the posterior and upward displacement of the condyle
during passive and tonic jaw retrusions (Fig. 17). The condylar
movement in these directions results in stretching the LPT muscle
fibers longitudinally. The presence of muscle spindles in the LPT,
though without specifying the head of the LPT, was shown anatomically
in humans (Gill 1971
; Honée 1966
;
Rakhawy et al. 1971
) and monkeys (Karlsen
1969
). Kubota and Masegi (1977)
reported
topographical details of the location of the spindle in the human LPT.
They reported that muscle spindles were present in the SUP as well as
INF. There is also electrophysiological evidence that the trigeminal
mesencephalic neurons innervating the muscle spindles in the LPT make
monosynaptic excitatory synaptic linkage with the LPT motoneurons in
the guinea pig (Nozaki et al. 1984
, 1985
). Accordingly,
the stretch reflex-like responses elicited in the human str-SUP in the
present study are probably the monosynaptic reflexes triggered by
muscle spindles in the LPT.
Anterior dislocation of the articular disk in TMJ disorders
In many cases of TMJ disorders, the condyle is shifted to the
posterior-most position in the temporomandibular fossa, and the
posterior band of the disk is dislocated to the front of the condyle
due to elongation of the ligaments of the articular capsule connecting
the disk to the condyle (Wilkinson 1989). It seems impossible that the disk moves anteriorly independently of the condyle
because the disk is attached rigidly to the medial and lateral poles of
the condyle by tendinous ligaments (Ress 1954
; Schmolke 1994
). Therefore the force that continuously
pulls the disk anteriorly must be the major cause of the elongation of
those ligaments in the patients with TMJ disorders. The force
responsible for the abnormally anterior displacement of the disk is
generated most probably by the str-SUP because it has a rigid
mechanical connection with the disk and can contract by stretch reflex.
Posterior displacement of the condyle from the normal position in the
temporomandibular fossa would create in front of the condyle a space
into which the posterior band of the disk slips. At the same time the
stretch reflex of the str-SUP evoked by posterior displacement of the condyle will increase the tension of the muscle and facilitate further
anterior displacement of the disk.
A therapeutic appliance, which often is called an "occlusal splint," is used for patients with TMJ disorders. This type of appliance inevitably increases interincisal distance. The subtype of "occlusal splint" that forces the mandible in the position anterior to the habitual position has usually better clinical effects. On the basis of the characteristics of the str-SUP, it is obvious that the increase in Vi and anterior positioning of the condyle results in decreasing the str-SUP muscle activity.
It is most likely that the probable direct cause of anterior dislocation of the disk in TMJ disorders is an abnormal hyperactivity of the str-SUP produced by posterior dislocation of the condyle.
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ACKNOWLEDGMENTS |
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We thank Dr. A. J. Miller for reviewing the earliest version of the manuscript.
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FOOTNOTES |
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Address for reprint requests: K. Hiraba, Dept. of Physiology, School of Dentistry, Aichi-Gakuin University, Kusumoto-cho 1-100, Chikusa-ku, Nagoya 464-8650, Japan.
The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.
Received 16 December 1998; accepted in final form 8 December 1999.
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REFERENCES |
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