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Functional Activity of Superior Head of Human Lateral Pterygoid Muscle during Isometric Force

¹ Faculty of Dentistry, Khonkaen University, Mittraphab Rd., Muang, Khonkaen, 40002 Thailand, and Faculty of Dentistry, University of Sydney; and
² Jaw Function and Orofacial Pain Research Unit, Faculty of Dentistry, University of Sydney, Level 3, Professorial Unit, Centre for Oral Health, Westmead Hospital, Westmead, NSW 2145, Australia;

Correspondence: ^* corresponding author, gregm{at}usyd.edu.au

	ABSTRACT

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There is controversy as to the jaw tasks for which the superior head of the human lateral pterygoid muscle (SHLP) becomes active. The aim was to describe the functional activities of SHLP single motor units (SMUs) during horizontal isometric force tasks. In 11 subjects, 48 SMUs were recorded from computer-tomography-verified SHLP sites during generation of horizontal isometric force in the contralateral (CL), protrusive (P), and ipsilateral (IL) directions and intermediate directions (CL-P, IL-P). In eight subjects, SHLP SMUs were active in CL, CL-P, and P. Qualitatively, SHLP EMG activity increased with increased isometric force. Forty-two SMUs were active in directions other than IL; 6 exhibited activity at IL and other directions. The similarity of these data to previous human lateral pterygoid (IHLP) data supports the notion that SHLP and IHLP should be regarded as a single muscle, with activities shaded according to the biomechanical demands of the task.

Key Words: isometric force • computer tomography • single motor unit • lateral pterygoid muscle • electromyogram

	INTRODUCTION

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Isometric contractions can occur in masticatory muscles during parafunctional jaw activities such as tooth-grinding and clenching. Although the generation of isometric force in the masticatory system is the result of activity in more than one muscle, the predominantly horizontal arrangement of fibers in the lateral pterygoid muscle indicates a major role for the lateral pterygoid in the generation and fine control of the horizontal forces generated in mastication or parafunctional grinding (Miller, 1991; Hannam and McMillan, 1994; Uchida et al., 2001, 2002; Murray et al., 2004). Jaw-closing-muscle isometric contractions have been studied extensively (Clark et al., 1988; van Eijden et al., 1990, 1993; Junge and Clark, 1993; Nickel et al., 2003). There is, however, little information about isometric contraction in the lateral pterygoid muscle, although there is evidence for the involvement of this muscle in the development of isometric horizontal force vectors toward the end of the intercuspal phase of chewing (Wood et al., 1986), as well as evidence that the muscle is active during voluntary tooth-grinding or gnashing (Widmalm et al., 1987).

A recent EMG study of the inferior head of the human lateral pterygoid (IHLP) during isometric contraction (Uchida et al., 2001, 2002) has provided data, consistent with data from previous studies (for review, see Miller, 1991; Hannam and McMillan, 1994), that the IHLP plays a major role in the generation and fine control of horizontal forces, especially in the contralateral direction, and as required in masticatory and parafunctional activities. There are controversial data, however, as to the jaw tasks for which the superior head of the human lateral pterygoid muscle (SHLP) becomes active and delivers force to the condyle and disc/capsule complex of the temporomandibular joint (TMJ) (for review, see Murray et al., 2001, 2004). For example, most studies have concluded that the SHLP demonstrates reciprocal activity with the IHLP, and is active on closing, retrusion, and ipsilateral jaw movements. In light of the current view that the SHLP inserts predominantly or exclusively into the condyle (e.g., Møller, 1966; Mahan et al., 1983; Christo, Wilkinson, Townsend, personal communication, 2004), it is hypothesized that a major function of the SHLP is in the generation and fine control of forces to the TMJ as required during the generation of contralaterally directed and protrusively directed jaw forces, and to play a much less important role in intercuspal clenching and ipsilaterally directed jaw forces. This proposal is consistent with the recent findings of activity in SHLP during contralateral and protrusive isotonic contractions with the teeth apart (Phanachet et al., 2003), which pointed to a role for the SHLP in controlling horizontal jaw movements.

Given the limited information available on the function of the SHLP, the aim of the present study was to describe the functional activity of SMUs recorded from the SHLP during isometric force tasks. Analysis of the data presented helps clarify the normal function of the SHLP. The new information is important in view of the controversial role of the SHLP in normal function and the frequent claim, although unsubstantiated, of a functional disturbance in the lateral pterygoid muscle in patients with temporomandibular disorders.

	MATERIALS & METHODS

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Eleven human volunteers (ages, 22–28 yrs; mean, 24.4 ± 2.6 yrs; eight males, three females), without history of chronic pain or neuromuscular condition, participated. All subjects gave informed consent, and experimental procedures were approved by the Western Sydney Area Health Service and University of Sydney Human Ethics Committees. Most procedures have been previously described (Orfanos et al., 1996; Murray et al., 1999a,b; Uchida et al., 2001, 2002).

EMG Recording
Computer tomography (CT) provided craniometric measurements for fine-wire electrode placement via a sterilized spinal needle directed below the zygomatic arch and retracted to leave the wires within the muscle. A CT scan at the end of the recording session verified electrode location within SHLP. Data were acquired at a sampling rate of 10,000 or 20,000 samples/sec and a bandwidth of 100 Hz-10 kHz. SMUs were discriminated with Spike2^® software (Cambridge Electronic Design, Cambridge, England). Bipolar surface electrodes were placed over the anterior middle part of the right masseter muscle.

Tasks
An isometric horizontal task involved the subject exerting isometric horizontal force via a force rod secured to the lower teeth and onto a force transducer projecting from the upper teeth (Fig. 1A). The apparatus could be swiveled horizontally in 5 directions—contralateral (CL), ipsilateral (IL), protrusive (P), CL-P, and IL-P directions—in relation to the SHLP electrode. Each subject monitored a video screen to perform a task that consisted of 5 five-second force steps, that increased by 100 gwt (0.98 N) at each force step. These force ranges allowed for SMU discrimination and represented ~ 10–20% of the horizontal maximum voluntary contraction (35–40 N; S. Uchida, personal communication). Equivalent values in SI units of each force step are: 100 gwt (0.98 N), 400 gwt (3.92 N), 500 gwt (4.9 N), 600 gwt (5.88 N), 700 gwt (6.86 N), and 800 gwt (7.84 N). We are confident that the force vector generated was parallel with the intended force direction and perpendicular to the face of the force transducer at each direction, because the force rod (that projected from the acrylic block attached to the lower jaw) came into contact with a small hemispheric button (radius, 1 mm) that projected from the flat face of the transducer (9-mm diam.). If the force was not exerted perpendicular to the transducer’s face, the force rod would slip off the hemispheric button on the transducer. The force signal was sampled at 1000 samples/sec and at a bandwith of 0–500 Hz. Each task was repeated 5–10 times, was undertaken in random order, and was separated by ^> one-minute rest periods. In separate trials, nine subjects also clenched at 100% maximum voluntary jaw-closing contraction for 5 sec.

View larger version (59K): [in this window] [in a new window]   Figure 1. Task apparatus, CT verification, and recording site location. (A) (Upper) Force transducer. The force bar and rod could be swiveled horizontally. (Lower) The custom-made upper acrylic bite block. Five isometric force directions were used: P, protrusive; CL, contralateral; IL, ipsilateral; CL-P, contralateral protrusive; and IL-P, ipsilateral protrusive. Ipsilateral refers to the side of the SHLP recording electrode. The average opening with the bite-blocks compared with postural jaw position was 5.7 mm (range, 3–8 mm). (B) Example of CT-verified electrode placement within the SHLP. (Upper) Horizontal slice (1 mm thick) and (lower) reformated oblique sagittal image through the long axis of the SHLP, showing electrode tip within the SHLP. (C) Two-dimensional mapping of electrode location in the SHLP in all subjects. Lower Fig. was taken along the long axis of the lateral pterygoid. Horizontal axis represents the long axis of the SHLP; the vertical axis represents the supero-inferior dimension of the SHLP. Task relations: O+, SMUs were active during CL, CL-P, P, and IL-P, with or without IL; +, SMUs were active during CL, CL-P, and P; P, SMUs were active during P only; and –, no activity. (D) Same data as in C, but plotted in the horizontal plane.

	RESULTS

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Task Relations of SHLP SMU Activity
From the SHLPs of 11 subjects, 48 SMUs were active during at least 1 of the isometric tasks. None was active with the jaw at the postural jaw position. A representative trial of protrusive isometric contraction (Fig. 2) shows 4 SMUs (Figs. 2B, 2C) discriminated from the filtered EMG (Fig. 2A) from the SHLP (Fig. 1B). Whether at least 1 SMU was active at a site for each task and subject is shown (Table). In eight (/11) participants, activity was apparent for CL, CL-P, and P. In seven, activity was present at IL-P and/or IL, and in five of nine subjects tested, activity was present during intercuspal clenching. Of the 48 SMUs, 34 (71%) SMUs were active at CL, 33 (69%) at CL-P, 32 (67%) at P, 17 (35%) at IL-P, and 6 (13%) SMUs were active at IL.

View larger version (28K): [in this window] [in a new window]   Figure 2. Example of SHLP EMG data during one trial of isometric protrusion. (A) Five steps of force-tracking [400 gwt (3.92 N) to 800 gwt (7.84 N)] and filtered EMG. Regions between the vertical lines indicate the defined stable periods (see METHODS) for each force step. (B) Four SMUs were discriminated during the most stable two-second holding period from this trial. Each trace represents the spike train of a SMU. Each short vertical line of the spike train is an action potential of a SMU. The period delineated by the vertical lines in A and B is expanded in (C) and illustrates the waveforms of 4 SMUs and their spike trains.

Association between SMU Activity and Direction of Horizontal Isometric Task
The 48 SMUs exhibited a variety of combinations of directions in which activity was observed. Thus, 5 units in two subjects were active in all directions, while 15 units in six subjects were active in 1 direction only (4 units at CL only [e.g., units 2, 4 in Fig. 3], 3 CL-P, 6 P, 2 IL-P [e.g., units 5, 6 in Fig. 3]). Eight units were active in 2 directions (5 CL and CL-P units; 1 IL-P and IL units; 1 IL-P and P unit; 1 CL-P and P unit), 14 units were active in 3 directions (12 CL, CL-P and P units [e.g., units 1, 3 in Fig. 3]; 1 CL, P and IL-P unit; 1 CL, CL-P and IL-P unit), and 6 units were active in 4 directions, all of which were active for CL, CL-P, P, and IL-P. At any one site, units could exhibit different combinations of directional relations (e.g., Fig. 3).

View larger version (33K): [in this window] [in a new window]   Figure 3. Force tracings, filtered EMG, and spike trains from 6 SMUs (waveforms on right) from 1 representative trial of each direction in one subject. SMUs no. 1, 2, 3, and 4 were active during CL. SMUs no. 1 and 3 were active during CL-P and P. SMUs no. 5 and 6 were active during IL-P. None of these SMUs was active during IL.

Association between SMU Activity and Vertical Isometric Task
In five of nine subjects, there was SHLP activity during 100% MVC. Of the five, two had electrodes in the medial part of SHLP, while in three, the electrodes were in the middle of the SHLP. There was no detectable EMG activity during maximum clench in four subjects. The medio-lateral locations of the recording sites in these subjects were scattered medio-laterally throughout SHLP (2 were lateral, 1 middle, 1 medial).

Electrode Location within the SHLP
CT scan data in the horizontal plane (upper panel) and in a reformated oblique sagittal plane (lower panel) along the long axis of the SHLP show the electrode tips within SHLP (Fig. 1B). The relative locations of the recording sites were plotted in the vertical (Fig. 1C) and horizontal (Fig. 1D, see Table) planes along the long axis of the SHLP. Each symbol represents the task(s) for which the SMUs at that site were active.

There was no activity for any of the horizontal isometric tasks at the 2 lowermost and lateralmost recording sites (Figs. 1C, 1D, Table). The muscle fibers of the SHLP that were active during CL, CL-P, P, and IL-P, with or without IL, were mostly scattered throughout the SHLP, both vertically and horizontally. However, there was some possible evidence for compartmentalization of activity patterns within the SHLP, in that the muscle fibers in the upper part of the SHLP tended not to be active in any of the IL tasks. Further, the mediolateral middle portion of SHLP tended to be the only part of SHLP that was active in the IL task.

	DISCUSSION

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The present study shows that the SHLP is active during horizontal isometric jaw forces in a range of directions. While most SMUs (40/48) were active in directions other than ipsilateral, 8 SMUs were active in a range of directions, including ipsilateral. Qualitatively, the EMG activity of the SHLP increased as the isometric force increased from 400 to 800 gwt. In five subjects (of nine studied), SHLP EMG activity was present during maximum clenching.

The presence of SHLP activity during clenching is consistent with the conventional view that one of the functions of the SHLP is to stabilize the head of the condyle and disc against the articular eminence (Widmalm et al., 1987; Osborn, 1995). Other data from the present study were not consistent with other conventional views, however—for example, that the SHLP functions in a manner reciprocal to that of the IHLP (Juniper, 1981, 1984; Gibbs et al., 1984; Hiraba et al., 2000). The present study demonstrates SHLP activities during contralateral and protrusive directions of isometric force, and this is consistent with recent and earlier demonstrations of SHLP activity during lower-force isotonic horizontal contralateral and protrusive movements (Sessle and Gurza, 1982; Murray et al., 1999a; Phanachet et al., 2003). There are abundant data pointing to IHLP activity during isometric and isotonic horizontal tasks in the contralateral and protrusive directions and in jaw opening (Phanachet et al., 2001, 2002; Uchida et al., 2001, 2002). The similarities in the task relations of SMU and multi-unit activity in the SHLP and IHLP support the hypothesis that both SHLP and IHLP should be regarded as parts of one muscle, with the distribution of activity shaded according to the biomechanical demands of the task (Hannam and McMillan, 1994).

The long muscle fibers of the lower region of the SHLP were active for contralateral, contralateral-protrusive, protrusive, ipsilateral-protrusive, and ipsilateral isometric forces, whereas the shorter muscle fibers in the upper part of the SHLP were less likely to be active for ipsilateral forces. While most of the SHLP appears important for the generation of contralateral and protrusive forces, it is possible that the direction of force applied to the ipsilateral condyle needs to be more horizontally directed, as applied through activation of the lower, more horizontally directed fibers of the SHLP, than the upper fibers of the SHLP, which are more vertically directed. During an ipsilateral jaw movement, the lower fibers may play a more important role on the ipsilateral side in stabilizing the condyle and/or disc-capsule complex, and preventing excessive posterior displacement and trauma to the highly innervated and vascularized posterior attachment tissues. The inferior-most and lateral-most fibers of the SHLP may be inactive for isometric force at the level used in the present study, although there were units active for isotonic horizontal movements. It is possible that the above three groups of activity patterns may be associated with specific fiber bundle orientations and/or lengths that may be biomechanically best-suited to specific horizontal isometric forces. It is possible that these groups of fibers could be selectively activated—that is, the SHLP is functionally heterogeneous (Hannam and McMillan, 1994; Foucart et al., 1998; Phanachet et al., 2003; Murray et al., 2001). This concept is consistent with SHLP muscle fiber anatomy, where fiber alignment changes from a broad origin, at the roof of the infratemporal fossa and lateral pterygoid plate, toward a small insertion site on the condylar fovea and disc-capsule complex (Mahan et al., 1983; Widmalm et al., 1987; Bittar et al., 1994; Heylings et al., 1995; Akita et al., 2000). The concept is also consistent with the presence of non-parallel fiber bundles within SHLP (Troiano, 1967), and a complex neural distribution within the SHLP (Foucart et al., 1998).

We did not observe any systematic influence on SHLP EMG activity from different changes in vertical dimension between and among subjects. For example, the only subject who had activity only during protrusion had an opening of 5.0 mm, close to the mean value of 5.7 mm. A related issue is that it remains to be determined whether periodontal activation during masticatory movements leads to SHLP EMG activity patterns different from those observed in the present study. Another issue is that it is unlikely that the lateral recordings from the SHLP recorded activity from the mid-medial bundle of the temporalis muscle (Akita et al., 2000) that inserts directly into the disc adjacent to the SHLP, because there was no clenching or ipsilateral activity at these most lateral recording sites (see Table). In addition, recording sites were in the anterior half of the SHLP (Figs. 1C, 1D), well clear of the insertion of the mid-medial bundle (Akita et al., 2000).

	ACKNOWLEDGMENTS

 
This investigation was supported by the National Health and Medical Research Council of Australia (Grant #990460), the Australian Dental Research Foundation, Inc., the Dental Board of NSW, and an AusAID scholarship to Dr. S. Ruangsri. We also acknowledge the Department of Radiology, Westmead Hospital, for the computer tomography scans. This paper is based on a thesis submitted to the Faculty of Dentistry, University of Sydney, for the MSc(Dent) degree.

Received for publication September 20, 2004. Revision received December 9, 2004. Accepted for publication February 4, 2005.

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Journal of Dental Research, Vol. 84, No. 6, 548-553 (2005)
DOI: 10.1177/154405910508400612


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This Article Abstract Figures Only Free Full Text (Free PDF) Free Alert me when this article is cited Alert me if a correction is posted Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Add to Saved Citations Download to citation manager Request Permissions Request Reprints Add to My Marked Citations Citing Articles Citing Articles via Google Scholar Citing Articles via Scopus Google Scholar Articles by Ruangsri, S. Articles by Murray, G.M. Search for Related Content PubMed PubMed Citation Articles by Ruangsri, S. Articles by Murray, G.M. Social Bookmarking                         What's this?