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Superior head of human lateral pterygoid muscle: Single motor unit firing rates during isometric force
archives of oral biology 52 (2007) 995–1001
available at www.sciencedirect.com
journal homepage: www.intl.elsevierhealth.com/journals/arob
Superior head of human lateral pterygoid muscle: Single motor unit firing rates during isometric force Supanigar Ruangsri 1, Terry Whittle, Greg M. Murray * 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
article info
abstract
Article history:
The superior head of the human lateral pterygoid muscle (SHLP) has been classically
Accepted 28 February 2007
considered to have functions that are independent of the inferior head of the lateral pterygoid (IHLP). Recent evidence however suggests that some of the functional properties
Keywords:
of the SHLP are similar to those of the IHLP. The aim was to determine whether the
Isometric force
functional properties in terms of single motor unit (SMU) firing rates within the SHLP vary
Computer tomography
with horizontal isometric force (400–800 gwt) and direction (i.e., contralateral (CL), protru-
Single motor unit
sive (P), ipsilateral (IL) and intermediate directions, CL-P, IL-P) in a manner similar to those
Lateral pterygoid muscle
identified for the IHLP, and as would be expected if both SHLP and IHLP should be regarded as
Electromyogram
one muscle. In eight subjects, the firing rates of 40 SMUs were recorded from computer
Firing rates
tomography (CT)-verified SHLP sites while each subject exerted horizontal isometric forces with their lower jaw onto a force transducer in the five directions. Firing rates increased significantly with horizontal isometric force from 400 to 800 gwt. Firing rates also changed significantly ( p < 0.01) with direction with CL, CL-P and P having comparable firing rates (13.3, 12.6 and 12.6 impulses/s, respectively) which were significantly higher than IL-P. The similarity of these data to previous IHLP data, provide additional support for the hypothesis that the SHLP and the IHLP should be regarded as two parts of one muscle. # 2007 Elsevier Ltd. All rights reserved.
1.
Introduction
The SHLP and the IHLP have been classically regarded as separate muscles (for reviews,1–3). Thus, the SHLP is said to be involved in jaw closing, jaw retrusion (i.e., pulling the jaw backwards) and ipsilateral jaw movements (i.e., lateral jaw movements to the same side as the SHLP side being studied), and not to play a role in jaw opening, jaw protrusion (i.e., forward jaw movement) and contralateral jaw movements. Recent evidence however indicates that SHLP and IHLP share many similar functional properties, and therefore suggest, as has been previously proposed,4 that SHLP and IHLP should be
regarded functionally as parts of one muscle. Recordings from CT-verified sites within SHLP5 have shown that many SMUs were active during the same low-force horizontal jaw movement tasks with the teeth apart as IHLP SMUs.6 Further, recent data suggest that many SHLP SMUs were active during isometric force generation in the contralateral and protrusive directions7 just as have been identified for the IHLP.8,9 We also recently provided detailed evidence for similarities in some functional properties of SMUs recorded from the SHLP and IHLP during the performance of low-force horizontal jaw movement tasks. These similarities included the demonstration of similar SMU thresholds to onset of firing during
* Corresponding author. Tel.: +61 2 9845 6380; fax: +61 2 9633 2893. E-mail addresses: [email protected] (S. Ruangsri), [email protected] (G.M. Murray). 1 Present address: Oral Biology, UCLA School of Dentistry, Los Angeles, CA 90095, USA. Tel.: +1 310 825 6509; fax: +1 310 794 7109. 0003–9969/$ – see front matter # 2007 Elsevier Ltd. All rights reserved. doi:10.1016/j.archoralbio.2007.02.010
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archives of oral biology 52 (2007) 995–1001
contralateral and protrusion tasks, as well as evidence for functional heterogeneity within both heads of the muscle.5,6,10 The hypothesis that both heads should be considered functionally as parts of one muscle is also consistent with the nerve supply to the lateral pterygoid which does not support an independent supply to each head but rather indicates that the muscle is best considered as a single unit made up of independent functional musculo-aponeurotic layers.11 In addition, a separate SHLP and IHLP are not always identifiable anatomically with there being reports of a third head and even no distinction into separate heads being clearly apparent.12 The earlier studies of IHLP8,9 characterised in detail the functional properties of IHLP single motor units in association with force level and direction during isometric horizontal force tasks. These data clearly showed that SMUs within IHLP significantly increased with isometric force levels up to 7.8 N8 and that their firing rates were significantly affected by direction with the highest activity being contralateral, that is, at the direction opposite to the side from which the IHLP was recorded.9 There is no information, however, as to whether the functional properties of SHLP SMUs also vary with force and direction in a manner similar to IHLP and as would be expected if indeed, both SHLP and IHLP should be regarded functionally as one muscle. Given the previous SMU data demonstrating comparabilities between many of the functional properties of SMUs within SHLP and IHLP, we hypothesised that SHLP SMUs will exhibit graded relations with horizontal forces in a manner similar to those which have been identified for the IHLP.8,9 The objectives of the present study therefore were (a) to define the firing rates of SMUs within SHLP during isometric contractions in a range of horizontal directions, and (b) to compare these data with similar data that have already been acquired for the IHLP.
2.
Materials and methods
Eight students (age 22–28 years; mean 24.3 2.9 years; six males, two females) without history of chronic pain or neuromuscular condition, or other medical problem, volunteered. Each volunteer gave informed consent and all experimental procedures were approved by the Western Sydney Area Health Service Ethics Committee of Westmead Hospital and the Human Ethics Committee of the University of Sydney. Most of the procedures have been previously described in detail5,7–9,13,14 and therefore the following will only briefly review the methods. The data presented here were derived from the eight out of eleven of the same subjects and experimental sessions as previously described.7
2.1. Intramuscular electrode placement into the SHLP and EMG recording Sterilised bipolar fine-wire electrodes were placed within the SHLP via a standard extraoral approach aided prior to and verified after the experiment by computer tomography. The actual recording sites have been previously documented.7 The data-acquisition equipment was the micro1401 from Cambridge Electronic Design (CED; Cambridge, England) and the
Fig. 1 – Force transducer set-up on casts on articulator. The force rod and transducer could be swivelled horizontally to achieve five isometric force directions.
sampling rate was 10,000 or 20,000 samples/s, and bandwidth 100 Hz to 10 kHz. SMUs were discriminated with Spike21 software from the CED and each action potential was verified by visual inspection. Power spectral analysis revealed that the highest frequency component of the SMU spike train was <4 kHz. Therefore, although our highest sampling frequency in some of our recordings was less than twice the low-pass filter setting, we do not believe that there was any significant aliasing of the SMU signal. A CT scan at the end of each recording session verified electrode location within SHLP.
2.2.
Horizontal isometric tasks
Volunteers initially performed simple jaw movements (i.e., ipsilateral, contralateral, protrusive, open–close, clench) to confirm that one or more SMUs could be discriminated from the SHLP. An isometric horizontal task involved exertion of isometric horizontal force via a force rod, secured to the lower teeth by an acrylic bite block, onto a force transducer (LM-5KA; Kyowa Dengyo, Japan) that projected from another bite block attached to the upper teeth (Fig. 1). The apparatus attached to the bite blocks could be swivelled horizontally in five directions: contralateral (CL), ipsilateral (IL), protrusive (P) and two intermediate directions (CL-P and IL-P) in relation to the side on which the SHLP electrodes were placed (for more details, see7). The angulation of the CL direction to the sagittal plane was 608 (see also,8) and the intermediate directions were 308 to the sagittal plane. The average opening with the bite blocks compared with postural jaw position was 5.7 mm, range 3–8 mm. Each subject monitored a video screen to perform a task that consisted of five, 5-s force steps that increased by 100 gwt (0.98 N) at each force step. These force ranges allowed SMU discrimination and represented 10–20% of the horizontal maximum voluntary contraction (horizontal MVC is 35–40 N; Uchida, personal communication). Equivalent values in Systeme Internationale units of each force step are: 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). The force vector generated was parallel with the intended force direction and perpendicular to
archives of oral biology 52 (2007) 995–1001
the face of the force transducer at each direction as the force rod (that projected from the acrylic bite block attached to the lower jaw) contacted a small hemispheric button (radius 1 mm) that projected from the flat face of the transducer (9 mm dia.). 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/s and at a bandwith of 0–500 Hz. Each task was repeated 5–10 times, was undertaken in random order and was separated by a 1 min rest period.
2.3.
Data analysis
Recordings containing discriminatable SMUs were obtained from the SHLP in the eight subjects. These eight are from the 11 subjects from whom other SHLP data have been previously reported7; in 3 of the 11, SMUs were not able to be discriminated reliably. The criteria for discriminating each SMU were similarities in amplitude and waveform and a regular time of occurrence of the SMU action potential; template-matching software was used to facilitate discrimination. SMUs from the most stable 2-s holding periods were analysed for mean firing rates. The most stable period was defined as the continuous 2 s period containing the least number of force trace fluctuations and where the force level remained within the range of force of 30 gwt from each force step (400–800 gwt). Firing rate (impulse/s) at a particular force level was defined as the number of action potentials counted in 2 s divided by 2. Inter-spike intervals >160 ms were discarded from the analysis before averaging the data. This criterion was used previously6 and was based on the minimal firing rate of 6 impulses/s for temporalis muscle motor units.15 This criterion was a more conservative approach for analysis of significant firing rate changes with increases in force level. The mean firing rate was usually calculated from at least five trials of each task. Statistical analysis involved univariate analyses of variance (ANOVA) with least significant difference (LSD) as the post hoc adjustment for multiple pairwise comparisons (SPSS, Version 12). A significance level <0.05 was applied throughout the analyses. Firing rate was the dependent variable, the tasks and force levels were fixed factors, and the SMUs were random factors. Where a particular SMU was not active during a particular task trial but was active in other trials, a value of zero was included for that trial in the statistical analysis. However, the absence of SMU activity, for example, when there was no activity of a particular SMU at 400–600 gwt, was included only when there was SMU activity of other force steps (e.g., 700–800 gwt). It should be pointed out that the data presented here for SHLP were qualitatively compared with previous data8,9 collected with the same methodology from IHLP, although in a different cohort of individuals.
3.
Results
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shows the superimposition of five force traces at each force direction. A different subject was chosen at each direction. The right panel shows the close matching of the average force traces (continuous line) at each direction with the target force (thick lines). Subjects generally noted that it was easier to track and hold the force levels at the lower forces, for example 400– 600 gwt. Raw EMG data have been presented elsewhere.7
3.2.
Firing rates of the SHLP SMUs
Forty out of 48 SMUs discriminated from the 8 subjects were included in the firing rate statistical analysis. The remaining 8 SMUs were not included because of difficulties of motor unit discrimination. The task activities of SMUs have been previously documented.7 The firing rates of all SMUs in all subjects (n = 8) increased significantly with an increase in force from 400 to 800 gwt ( p < 0.02). Fig. 3 is a graphical representation of the data showing the mean values for all subjects in all directions grouped together that clearly show the increase of mean firing rates as force increases from 400 to 800 gwt (note that the two-way interaction is significant, see below).
3.3. Firing rates for increments of force between 400 and 800 gwt When SMU firing rate values from all subjects were pooled there were significant effects of task, force and SMUs ( p < 0.001) as well as two-way interactions among these variables (task by force, task by SMU, force by SMU) that showed statistical significance ( p < 0.001). However, a threeway interaction of task by force by SMU did not show statistical significance ( p = 0.207). There was a significant increase of firing rate with increase of force with the means (S.E.) being 7.4 (0.34), 9.9 (0.33), 12.8 (0.34), 13.9 (0.36) and 17.8 (0.40) impulses/s in relation to 400, 500, 600, 700 and 800 gwt, respectively ( p < 0.001). A pairwise comparison of all possible pairs of force levels indicated significant differences between all force levels ( p < 0.05). Fig. 4A displays the mean firing rates for all subjects in relation to force level for each task. Firing rate changed significantly with direction with the means (S.E.) being 13.3 (0.32), 12.6 (0.33), 12.6 (0.29), 9.8 (0.51) and 11.1 (0.96) impulses/s in relation to CL, CL-P, P, ILP and IL, respectively ( p < 0.001). Pairwise comparisons between each task indicated that CL, CL-P and P have comparable firing rates, and that CL, CL-P, and P each had significantly higher firing rates than IL-P. Also, CL had a significantly higher firing rate than IL ( p < 0.05) but IL was not significantly different from the other directions. It is suggested that CL, CL-P and P are preferential directions of firing for the SHLP in terms of the direction at which the highest firing rate occurred. Fig. 4B plots the mean firing rates at each force level in association with the different tasks.
3.1. Association between exerted force and target force level
3.4. Firing rates for increments of force between 400 and 600 gwt
All subjects closely matched the force traces with the target force at each force direction. For example, Fig. 2 (left panel)
The firing rates at the 700 and 800 gwt did not fit the analysis model, that is, an inspection of the firing rates (Fig. 4A and B)
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archives of oral biology 52 (2007) 995–1001
Fig. 2 – (Left panel) Superimposition of five force traces from representative subjects at each direction of isometric contraction. A different subject was chosen at each direction. (Right panel) Average force trace at each force direction (continuous lines) superimposed over the target force and was within W30 gwt (0.294 N) of the actual target force (dotted straight lines). Duration of each holding phase: 5 s; force increments between steps: 100 gwt (0.98 N).
indicate a difference of effect at the 700 and 800 gwt level in comparison with the 400–600 gwt levels. This may reflect the substantially fewer discriminated SMUs at higher force levels because of the difficulty in discriminating units at higher force levels when a greater number of SMUs were recruited and fired concomitantly. Therefore, firing rates at 700–800 gwt were omitted for the following analysis. There was a significant two-way interaction between task and SMU only ( p < 0.001) and significant effects of the individual variables of force, task
and SMU ( p < 0.001). There was a significant increase of firing rate with force ( p < 0.001) with significant differences between all force levels ( p < 0.001). In addition, firing rate significantly changed with direction ( p < 0.001) with the means being 11.5, 10.0, 9.5, 7.6 and 9.7 impulses/s in relation to CL, CL-P, P, IL-P and IL, respectively. Pairwise comparisons between each task indicated significant differences of firing rates only for CL with CL-P, CL with P, CL with IL-P, CL-P with IL-P, and P with IL-P ( p < 0.05).
archives of oral biology 52 (2007) 995–1001
Fig. 3 – Mean firing rate of all discriminated SMUs in each subject (total eight subjects) at all force directions. Some firing rate values at 400 or 500 gwt (3.92 or 4.9 N) were below 6 impulses/s, because zero firing rate was included in the analyses (see Section 2).
4.
Discussion
Electromyographic recordings from CT-verified sites within the SHLP in the present study demonstrated graded changes in SMU activity with increase of force and with changes of horizontal force direction. As the magnitude of force increased from 400 to 800 gwt, there was an increase in the frequency of firing of SMUs and an increase in the numbers of SMUs that were active.7 This close relation between SHLP EMG activity and force developed during horizontal isometric contraction suggests that, just as has been proposed for the IHLP,8,9 the SHLP plays an important role for the generation and control of horizontal isometric forces as required in mastication and parafunctional activities. The close relation between EMG activity and force has been previously described in limb muscles16,17 and jaw closing muscles.18
4.1.
Firing rate and different directions
The SMUs of the SHLP altered their firing rates with different directions of horizontal isometric force. Given the small data set used for the analysis in the IL direction, the data in the IL direction were excluded for the following discussion of directional relations. In the following, preferred direction is
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defined as the direction at which SMUs within the SHLP exhibited the highest firing rate at a given force level and this is consistent with previous definitions of preferred direction (e.g.,19). From the 400–600 gwt analysis (that is, excluding the higher 700 and 800 gwt levels), the contralateral task was the preferred direction for the SHLP. A similar conclusion was also previously stated for the IHLP.9 When the 700 and 800 gwt levels were included in the analysis (Fig. 4A and B), the firing rates at the CL-P and P directions were comparable to those at the CL direction and were significantly higher than the firing rates at the IL-P direction. This latter analysis suggests that, when higher forces are generated (i.e., at 700 and 800 gwt), SHLP contributes equally to force in the CL, CL-P and P directions. The anatomy of the SHLP may provide an explanation for this broad range of preferred direction of firing. The muscle fibres within the SHLP, as a group, are aligned 268 to the sagittal plane.20 The CL-P direction (308 to the sagittal plane, see Section 2) therefore is very close to the overall orientation of 268 for SHLP.20 If all muscle fibres within SHLP were oriented at about 268 to the sagittal plane, then CL-P might be expected to be the preferred direction of firing for SHLP. However, there is good evidence for a broad range of muscle fibre directions in the horizontal plane within SHLP (e.g.,21) that may cover most of the range of isometric force directions from CL to P used in the present study. Our recording sites covered the entire mediolateral width of the SHLP,7 and therefore, could well have recorded from SMUs in parts of the SHLP with different orientations to the sagittal plane and with different preferred directions that may well cover the range from CL to P. Therefore, in the overall analysis with all units grouped together in all subjects, it is possibly not unexpected that similar firing rates were observed at CL, CL-P and P. In a previous study, most units within IHLP exhibited a single preferred direction of firing at CL and this was consistent with the overall analysis of these IHLP units.9 Most muscle fibres within IHLP are oriented along the overall direction of the IHLP22 which is 458 to the sagittal plane.20 Such an arrangement of muscle fibres would be consistent with a single preferred direction of firing at CL in the horizontal plane. Together with the conclusions concerning the preferred directions for SHLP, namely force level dependence and tendency to cover a broader range of directions from CL through to P, we believe our data are consistent with the notion that, functionally, SHLP and IHLP should be regarded as a single muscle. Further, the functional complex-
Fig. 4 – (A and B) The mean firing rates of all subjects’ SMUs as force increases from 400 to 800 gwt (3.92–7.84 N) (A) and as direction changes from CL through to IL (B). CL: contralateral, CL-P: contralateral protrusion, P: protrusion, IL-P: ipsilateral protrusion and IL: ipsilateral.
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archives of oral biology 52 (2007) 995–1001
ity identified within SHLP and IHLP5,6,10 suggest that there is a gradation of functional properties from IHLP to SHLP. Further data is needed to clarify the contribution to IL from SHLP. It is nonetheless recognised that the comparison data from IHLP were recorded from a different group of subjects and a more rigorous argument for the proposal, that SHLP and IHLP should be regarded as one muscle, would come from recordings from both heads of the muscle in the same individuals, albeit technically very difficult.
4.2.
protrusive jaw movements.14 Therefore, we believe that, during chewing, SHLP will deliver horizontal force vectors on the condyle to move the condyle in a range of contralateral and protrusive directions in the horizontal plane. We also have no data as to the effects of variations in musculoskeletal form on SHLP activity patterns and this could be an aspect for future studies. In addition, future studies could more precisely define the SMUs being recorded by characterizing SMU anatomy through magnetic resonance images.
A comment on rate coding and recruitment 4.4.
Human jaw muscles seem to rely more on rate coding than on recruitment of SMUs to increase contraction23 but in limb muscles, motor units were recruited over the entire range of the contraction.24 In this study, the force ranges allowed SMU discrimination over 10–20% of the horizontal maximum voluntary contraction (horizontal MVC: 35–40 N, Uchida, personal communication). We were able to identify clearly the presence of SMUs that increased firing rates as force increased from a lower step level to higher force levels (low and high threshold units) and also SMUs that were recruited during the dynamic phases when the force levels rapidly increased at the higher force levels (i.e., at 700 and 800 gwt, higher threshold units; see7). Therefore, up to 20% of horizontal maximum voluntary contraction, the SHLP relies on both rate coding and recruitment to increase voluntary contraction.
4.3.
Limitations and future studies
The use of a standard force level across the five directions of force application may be a factor influencing the changes in EMG activity observed across the five directions. It is possible that the relative contributions of all the jaw muscles involved in the tasks may change with force direction (see8,9). Thus in one direction, SHLP’s function may be to contribute proportionally greater to the force generated, in relation to the other jaw muscles, than in another direction. This issue could be addressed in future studies by calculating force levels as a proportion of jaw muscle EMG activity at maximum voluntary contraction. Another limitation was that the data in the present study were compared qualitatively with previous studies8,9 whose data was collected several years earlier. However, in both these earlier and the present studies the protocol, equipment and data analyses were the same, as were most of the experimenters. Therefore, we believe the data to be essentially comparable. Another limitation of the study relates to the general applicability of these and other data from our laboratory to the way the SHLP and IHLP functions under other movements such as chewing, speech, etc. It is not possible to address this issue definitely as we have not published data on the functional properties of SHLP SMUs during chewing, however, the properties observed in SHLP SMUs during this isometric task are consistent with data previously reported for SHLP for an isotonic task.5 Further, we have previously shown that multi-unit EMG activity from SHLP exhibits graded relations with displacement as the teeth were slid against each other during contralateral and
Conclusions: SHLP and IHLP as one muscle
Given the similarities in functional properties between the present isometric force data and previous isometric force data from the IHLP,8,9 together with the similarities in functional properties of SMUs in SHLP and IHLP during jaw movements5,6,10,25, we interpret these data as supporting the hypothesis4 that the lateral pterygoid should be regarded as a . . .system of fibers (that) acts as one muscle, with varying amounts of evenly graded activity throughout its entire range, with the distribution shaded according to the biomechanical demands of the task.
Acknowledgments This investigation was supported by the National Health and Medical Research Council of Australia (Grants #990460 and 302005), the Australian Dental Research Foundation Inc., the Dental Board of NSW, and an AusAID scholarship to Dr Supanigar Ruangsri. We also acknowledge the Department of Radiology, Westmead Hospital for the computer tomography scans. Dr Supanigar Ruangsri on leave from Faculty of Dentistry, Khonkaen University, Mittraphab Road, Muang, Khonkaen 40002, Thailand. The research was based on a thesis submitted to the Faculty of Dentistry, University of Sydney, for the MScDent degree.
references
1. Klineberg IJ. The lateral pterygoid muscle: some anatomical, physiological and clinical considerations. Ann R Aust Coll Dent Surg 1991;11:96–108. 2. Miller AJ. Craniomandibular muscles: their role in function and form. Boca Raton: CRC Press; 1991. 3. 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. 4. Hannam AG, McMillan AS. Internal organization in the human jaw muscles. Crit Rev Oral Biol Med 1994;5:55–89. 5. Phanachet I, Whittle T, Wanigaratne K, Klineberg IJ, Sessle BJ, Murray GM. Functional heterogeneity in the superior head of the human lateral pterygoid. J Dent Res 2003;82: 106–11. 6. Phanachet I, Whittle T, Wanigaratne K, Murray GM. Functional properties of single motor units in inferior head of human lateral pterygoid muscle: task relations and thresholds. J Neurophysiol 2001;86:2204–18.
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7. Ruangsri S, Whittle T, Wanigaratne K, Murray GM. Functional activity of superior head of human lateral pterygoid muscle during isometric force. J Dent Res 2005;84:548–53. 8. Uchida S, Whittle T, Wanigaratne K, Murray GM. The role of the inferior head of the human lateral pterygoid muscle in the generation and control of horizontal mandibular force. Arch Oral Biol 2001;46:1127–40. 9. Uchida S, Whittle T, Wanigaratne K, Murray GM. Activity in the inferior head of the human lateral pterygoid muscle with different directions of isometric force. Arch Oral Biol 2002;47:771–8. 10. Bhutada MK, Phanachet I, Whittle T, Wanigaratne K, Peck CC, Murray GM. Threshold properties of single motor units in superior head of human lateral pterygoid muscle. Arch Oral Biol 2007;52:552–61. 11. Akita K, Shimokawa T, Sato T. Positional relationships between the masticatory muscles and their innervating nerves with special reference to the lateral pterygoid and the midmedial and discotemporal muscle bundles of temporalis. J Anat 2000;197:291–302. 12. Naohara H. The macroscopic and microscopic study of the human lateral pterygoid muscle. Tsur Shig 1989;15:1–26. 13. Orfanos T, Sarinnaphakorn L, Murray GM, Klineberg IJ. Placement and verification of recording electrodes in the superior head of the human lateral pterygoid muscle. Arch Oral Biol 1996;41:493–503. 14. Murray GM, Orfanos T, Chan JCY, Wanigaratne K, Klineberg IJ. Electromyographic activity of the human lateral pterygoid muscle during contralateral and protrusive jaw movements. Arch Oral Biol 1999;44:269–85. 15. McMillan AS. Task-related behaviour of motor units in the human temporalis muscle. Exp Brain Res 1993;94:336–42.
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16. Lippold OCJ. The relation between integrated action potentials in a human muscle and its isometric tension. J Physiol (Lond) 1952;117:492–9. 17. De Luca C, LeFever RS, McCue MP, Xenakis AP. Behaviour of human motor units in different muscles during linearly varying contractions. J Physiol (Lond) 1982;329: 113–28. 18. Goldberg LJ, Derfler B. Relationship among recruitment order, spike amplitude, and twitch tension of single motor units in human masseter muscle. J Neurophysiol 1977;40:879–90. 19. Theeuwen M, Gielen CCAM, Miller LE, Doorenbosch C. The relation between the direction dependence of electromyographic amplitude and motor unit recruitment thresholds during isometric contractions. Exp Brain Res 1994;98:488–500. 20. Hone´e GLJM. The anatomy of the lateral pterygoid muscle. Acta Morphol Neerl-Scand 1972;10:331–40. 21. Troiano MF. New concept of the insertion of the lateral pterygoid muscle. J Oral Surg 1967;25:337–40. 22. Widmalm SE, Lillie JH, Ash MM. Anatomical and electromyographic studies of the lateral pterygoid muscle. J Oral Rehabil 1987;14:429–46. 23. Clark RW, Luschei ES, Hoffman DS. Recruitment order, contractile characteristics, and firing patterns of motor units in the temporalis muscle of monkeys. Exp Neurol 1978;61:31–52. 24. De Luca C. Control properties of motor units. J Exp Biol 1985;115:125–36. 25. Phanachet I, Whittle T, Wanigaratne K, Murray GM. Functional properties of single motor units in the inferior head of human lateral pterygoid muscle: task firing rates. J Neurophysiol 2002;88:751–60.
available at www.sciencedirect.com
journal homepage: www.intl.elsevierhealth.com/journals/arob
Superior head of human lateral pterygoid muscle: Single motor unit firing rates during isometric force Supanigar Ruangsri 1, Terry Whittle, Greg M. Murray * 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
article info
abstract
Article history:
The superior head of the human lateral pterygoid muscle (SHLP) has been classically
Accepted 28 February 2007
considered to have functions that are independent of the inferior head of the lateral pterygoid (IHLP). Recent evidence however suggests that some of the functional properties
Keywords:
of the SHLP are similar to those of the IHLP. The aim was to determine whether the
Isometric force
functional properties in terms of single motor unit (SMU) firing rates within the SHLP vary
Computer tomography
with horizontal isometric force (400–800 gwt) and direction (i.e., contralateral (CL), protru-
Single motor unit
sive (P), ipsilateral (IL) and intermediate directions, CL-P, IL-P) in a manner similar to those
Lateral pterygoid muscle
identified for the IHLP, and as would be expected if both SHLP and IHLP should be regarded as
Electromyogram
one muscle. In eight subjects, the firing rates of 40 SMUs were recorded from computer
Firing rates
tomography (CT)-verified SHLP sites while each subject exerted horizontal isometric forces with their lower jaw onto a force transducer in the five directions. Firing rates increased significantly with horizontal isometric force from 400 to 800 gwt. Firing rates also changed significantly ( p < 0.01) with direction with CL, CL-P and P having comparable firing rates (13.3, 12.6 and 12.6 impulses/s, respectively) which were significantly higher than IL-P. The similarity of these data to previous IHLP data, provide additional support for the hypothesis that the SHLP and the IHLP should be regarded as two parts of one muscle. # 2007 Elsevier Ltd. All rights reserved.
1.
Introduction
The SHLP and the IHLP have been classically regarded as separate muscles (for reviews,1–3). Thus, the SHLP is said to be involved in jaw closing, jaw retrusion (i.e., pulling the jaw backwards) and ipsilateral jaw movements (i.e., lateral jaw movements to the same side as the SHLP side being studied), and not to play a role in jaw opening, jaw protrusion (i.e., forward jaw movement) and contralateral jaw movements. Recent evidence however indicates that SHLP and IHLP share many similar functional properties, and therefore suggest, as has been previously proposed,4 that SHLP and IHLP should be
regarded functionally as parts of one muscle. Recordings from CT-verified sites within SHLP5 have shown that many SMUs were active during the same low-force horizontal jaw movement tasks with the teeth apart as IHLP SMUs.6 Further, recent data suggest that many SHLP SMUs were active during isometric force generation in the contralateral and protrusive directions7 just as have been identified for the IHLP.8,9 We also recently provided detailed evidence for similarities in some functional properties of SMUs recorded from the SHLP and IHLP during the performance of low-force horizontal jaw movement tasks. These similarities included the demonstration of similar SMU thresholds to onset of firing during
* Corresponding author. Tel.: +61 2 9845 6380; fax: +61 2 9633 2893. E-mail addresses: [email protected] (S. Ruangsri), [email protected] (G.M. Murray). 1 Present address: Oral Biology, UCLA School of Dentistry, Los Angeles, CA 90095, USA. Tel.: +1 310 825 6509; fax: +1 310 794 7109. 0003–9969/$ – see front matter # 2007 Elsevier Ltd. All rights reserved. doi:10.1016/j.archoralbio.2007.02.010
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contralateral and protrusion tasks, as well as evidence for functional heterogeneity within both heads of the muscle.5,6,10 The hypothesis that both heads should be considered functionally as parts of one muscle is also consistent with the nerve supply to the lateral pterygoid which does not support an independent supply to each head but rather indicates that the muscle is best considered as a single unit made up of independent functional musculo-aponeurotic layers.11 In addition, a separate SHLP and IHLP are not always identifiable anatomically with there being reports of a third head and even no distinction into separate heads being clearly apparent.12 The earlier studies of IHLP8,9 characterised in detail the functional properties of IHLP single motor units in association with force level and direction during isometric horizontal force tasks. These data clearly showed that SMUs within IHLP significantly increased with isometric force levels up to 7.8 N8 and that their firing rates were significantly affected by direction with the highest activity being contralateral, that is, at the direction opposite to the side from which the IHLP was recorded.9 There is no information, however, as to whether the functional properties of SHLP SMUs also vary with force and direction in a manner similar to IHLP and as would be expected if indeed, both SHLP and IHLP should be regarded functionally as one muscle. Given the previous SMU data demonstrating comparabilities between many of the functional properties of SMUs within SHLP and IHLP, we hypothesised that SHLP SMUs will exhibit graded relations with horizontal forces in a manner similar to those which have been identified for the IHLP.8,9 The objectives of the present study therefore were (a) to define the firing rates of SMUs within SHLP during isometric contractions in a range of horizontal directions, and (b) to compare these data with similar data that have already been acquired for the IHLP.
2.
Materials and methods
Eight students (age 22–28 years; mean 24.3 2.9 years; six males, two females) without history of chronic pain or neuromuscular condition, or other medical problem, volunteered. Each volunteer gave informed consent and all experimental procedures were approved by the Western Sydney Area Health Service Ethics Committee of Westmead Hospital and the Human Ethics Committee of the University of Sydney. Most of the procedures have been previously described in detail5,7–9,13,14 and therefore the following will only briefly review the methods. The data presented here were derived from the eight out of eleven of the same subjects and experimental sessions as previously described.7
2.1. Intramuscular electrode placement into the SHLP and EMG recording Sterilised bipolar fine-wire electrodes were placed within the SHLP via a standard extraoral approach aided prior to and verified after the experiment by computer tomography. The actual recording sites have been previously documented.7 The data-acquisition equipment was the micro1401 from Cambridge Electronic Design (CED; Cambridge, England) and the
Fig. 1 – Force transducer set-up on casts on articulator. The force rod and transducer could be swivelled horizontally to achieve five isometric force directions.
sampling rate was 10,000 or 20,000 samples/s, and bandwidth 100 Hz to 10 kHz. SMUs were discriminated with Spike21 software from the CED and each action potential was verified by visual inspection. Power spectral analysis revealed that the highest frequency component of the SMU spike train was <4 kHz. Therefore, although our highest sampling frequency in some of our recordings was less than twice the low-pass filter setting, we do not believe that there was any significant aliasing of the SMU signal. A CT scan at the end of each recording session verified electrode location within SHLP.
2.2.
Horizontal isometric tasks
Volunteers initially performed simple jaw movements (i.e., ipsilateral, contralateral, protrusive, open–close, clench) to confirm that one or more SMUs could be discriminated from the SHLP. An isometric horizontal task involved exertion of isometric horizontal force via a force rod, secured to the lower teeth by an acrylic bite block, onto a force transducer (LM-5KA; Kyowa Dengyo, Japan) that projected from another bite block attached to the upper teeth (Fig. 1). The apparatus attached to the bite blocks could be swivelled horizontally in five directions: contralateral (CL), ipsilateral (IL), protrusive (P) and two intermediate directions (CL-P and IL-P) in relation to the side on which the SHLP electrodes were placed (for more details, see7). The angulation of the CL direction to the sagittal plane was 608 (see also,8) and the intermediate directions were 308 to the sagittal plane. The average opening with the bite blocks compared with postural jaw position was 5.7 mm, range 3–8 mm. Each subject monitored a video screen to perform a task that consisted of five, 5-s force steps that increased by 100 gwt (0.98 N) at each force step. These force ranges allowed SMU discrimination and represented 10–20% of the horizontal maximum voluntary contraction (horizontal MVC is 35–40 N; Uchida, personal communication). Equivalent values in Systeme Internationale units of each force step are: 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). The force vector generated was parallel with the intended force direction and perpendicular to
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the face of the force transducer at each direction as the force rod (that projected from the acrylic bite block attached to the lower jaw) contacted a small hemispheric button (radius 1 mm) that projected from the flat face of the transducer (9 mm dia.). 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/s and at a bandwith of 0–500 Hz. Each task was repeated 5–10 times, was undertaken in random order and was separated by a 1 min rest period.
2.3.
Data analysis
Recordings containing discriminatable SMUs were obtained from the SHLP in the eight subjects. These eight are from the 11 subjects from whom other SHLP data have been previously reported7; in 3 of the 11, SMUs were not able to be discriminated reliably. The criteria for discriminating each SMU were similarities in amplitude and waveform and a regular time of occurrence of the SMU action potential; template-matching software was used to facilitate discrimination. SMUs from the most stable 2-s holding periods were analysed for mean firing rates. The most stable period was defined as the continuous 2 s period containing the least number of force trace fluctuations and where the force level remained within the range of force of 30 gwt from each force step (400–800 gwt). Firing rate (impulse/s) at a particular force level was defined as the number of action potentials counted in 2 s divided by 2. Inter-spike intervals >160 ms were discarded from the analysis before averaging the data. This criterion was used previously6 and was based on the minimal firing rate of 6 impulses/s for temporalis muscle motor units.15 This criterion was a more conservative approach for analysis of significant firing rate changes with increases in force level. The mean firing rate was usually calculated from at least five trials of each task. Statistical analysis involved univariate analyses of variance (ANOVA) with least significant difference (LSD) as the post hoc adjustment for multiple pairwise comparisons (SPSS, Version 12). A significance level <0.05 was applied throughout the analyses. Firing rate was the dependent variable, the tasks and force levels were fixed factors, and the SMUs were random factors. Where a particular SMU was not active during a particular task trial but was active in other trials, a value of zero was included for that trial in the statistical analysis. However, the absence of SMU activity, for example, when there was no activity of a particular SMU at 400–600 gwt, was included only when there was SMU activity of other force steps (e.g., 700–800 gwt). It should be pointed out that the data presented here for SHLP were qualitatively compared with previous data8,9 collected with the same methodology from IHLP, although in a different cohort of individuals.
3.
Results
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shows the superimposition of five force traces at each force direction. A different subject was chosen at each direction. The right panel shows the close matching of the average force traces (continuous line) at each direction with the target force (thick lines). Subjects generally noted that it was easier to track and hold the force levels at the lower forces, for example 400– 600 gwt. Raw EMG data have been presented elsewhere.7
3.2.
Firing rates of the SHLP SMUs
Forty out of 48 SMUs discriminated from the 8 subjects were included in the firing rate statistical analysis. The remaining 8 SMUs were not included because of difficulties of motor unit discrimination. The task activities of SMUs have been previously documented.7 The firing rates of all SMUs in all subjects (n = 8) increased significantly with an increase in force from 400 to 800 gwt ( p < 0.02). Fig. 3 is a graphical representation of the data showing the mean values for all subjects in all directions grouped together that clearly show the increase of mean firing rates as force increases from 400 to 800 gwt (note that the two-way interaction is significant, see below).
3.3. Firing rates for increments of force between 400 and 800 gwt When SMU firing rate values from all subjects were pooled there were significant effects of task, force and SMUs ( p < 0.001) as well as two-way interactions among these variables (task by force, task by SMU, force by SMU) that showed statistical significance ( p < 0.001). However, a threeway interaction of task by force by SMU did not show statistical significance ( p = 0.207). There was a significant increase of firing rate with increase of force with the means (S.E.) being 7.4 (0.34), 9.9 (0.33), 12.8 (0.34), 13.9 (0.36) and 17.8 (0.40) impulses/s in relation to 400, 500, 600, 700 and 800 gwt, respectively ( p < 0.001). A pairwise comparison of all possible pairs of force levels indicated significant differences between all force levels ( p < 0.05). Fig. 4A displays the mean firing rates for all subjects in relation to force level for each task. Firing rate changed significantly with direction with the means (S.E.) being 13.3 (0.32), 12.6 (0.33), 12.6 (0.29), 9.8 (0.51) and 11.1 (0.96) impulses/s in relation to CL, CL-P, P, ILP and IL, respectively ( p < 0.001). Pairwise comparisons between each task indicated that CL, CL-P and P have comparable firing rates, and that CL, CL-P, and P each had significantly higher firing rates than IL-P. Also, CL had a significantly higher firing rate than IL ( p < 0.05) but IL was not significantly different from the other directions. It is suggested that CL, CL-P and P are preferential directions of firing for the SHLP in terms of the direction at which the highest firing rate occurred. Fig. 4B plots the mean firing rates at each force level in association with the different tasks.
3.1. Association between exerted force and target force level
3.4. Firing rates for increments of force between 400 and 600 gwt
All subjects closely matched the force traces with the target force at each force direction. For example, Fig. 2 (left panel)
The firing rates at the 700 and 800 gwt did not fit the analysis model, that is, an inspection of the firing rates (Fig. 4A and B)
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Fig. 2 – (Left panel) Superimposition of five force traces from representative subjects at each direction of isometric contraction. A different subject was chosen at each direction. (Right panel) Average force trace at each force direction (continuous lines) superimposed over the target force and was within W30 gwt (0.294 N) of the actual target force (dotted straight lines). Duration of each holding phase: 5 s; force increments between steps: 100 gwt (0.98 N).
indicate a difference of effect at the 700 and 800 gwt level in comparison with the 400–600 gwt levels. This may reflect the substantially fewer discriminated SMUs at higher force levels because of the difficulty in discriminating units at higher force levels when a greater number of SMUs were recruited and fired concomitantly. Therefore, firing rates at 700–800 gwt were omitted for the following analysis. There was a significant two-way interaction between task and SMU only ( p < 0.001) and significant effects of the individual variables of force, task
and SMU ( p < 0.001). There was a significant increase of firing rate with force ( p < 0.001) with significant differences between all force levels ( p < 0.001). In addition, firing rate significantly changed with direction ( p < 0.001) with the means being 11.5, 10.0, 9.5, 7.6 and 9.7 impulses/s in relation to CL, CL-P, P, IL-P and IL, respectively. Pairwise comparisons between each task indicated significant differences of firing rates only for CL with CL-P, CL with P, CL with IL-P, CL-P with IL-P, and P with IL-P ( p < 0.05).
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Fig. 3 – Mean firing rate of all discriminated SMUs in each subject (total eight subjects) at all force directions. Some firing rate values at 400 or 500 gwt (3.92 or 4.9 N) were below 6 impulses/s, because zero firing rate was included in the analyses (see Section 2).
4.
Discussion
Electromyographic recordings from CT-verified sites within the SHLP in the present study demonstrated graded changes in SMU activity with increase of force and with changes of horizontal force direction. As the magnitude of force increased from 400 to 800 gwt, there was an increase in the frequency of firing of SMUs and an increase in the numbers of SMUs that were active.7 This close relation between SHLP EMG activity and force developed during horizontal isometric contraction suggests that, just as has been proposed for the IHLP,8,9 the SHLP plays an important role for the generation and control of horizontal isometric forces as required in mastication and parafunctional activities. The close relation between EMG activity and force has been previously described in limb muscles16,17 and jaw closing muscles.18
4.1.
Firing rate and different directions
The SMUs of the SHLP altered their firing rates with different directions of horizontal isometric force. Given the small data set used for the analysis in the IL direction, the data in the IL direction were excluded for the following discussion of directional relations. In the following, preferred direction is
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defined as the direction at which SMUs within the SHLP exhibited the highest firing rate at a given force level and this is consistent with previous definitions of preferred direction (e.g.,19). From the 400–600 gwt analysis (that is, excluding the higher 700 and 800 gwt levels), the contralateral task was the preferred direction for the SHLP. A similar conclusion was also previously stated for the IHLP.9 When the 700 and 800 gwt levels were included in the analysis (Fig. 4A and B), the firing rates at the CL-P and P directions were comparable to those at the CL direction and were significantly higher than the firing rates at the IL-P direction. This latter analysis suggests that, when higher forces are generated (i.e., at 700 and 800 gwt), SHLP contributes equally to force in the CL, CL-P and P directions. The anatomy of the SHLP may provide an explanation for this broad range of preferred direction of firing. The muscle fibres within the SHLP, as a group, are aligned 268 to the sagittal plane.20 The CL-P direction (308 to the sagittal plane, see Section 2) therefore is very close to the overall orientation of 268 for SHLP.20 If all muscle fibres within SHLP were oriented at about 268 to the sagittal plane, then CL-P might be expected to be the preferred direction of firing for SHLP. However, there is good evidence for a broad range of muscle fibre directions in the horizontal plane within SHLP (e.g.,21) that may cover most of the range of isometric force directions from CL to P used in the present study. Our recording sites covered the entire mediolateral width of the SHLP,7 and therefore, could well have recorded from SMUs in parts of the SHLP with different orientations to the sagittal plane and with different preferred directions that may well cover the range from CL to P. Therefore, in the overall analysis with all units grouped together in all subjects, it is possibly not unexpected that similar firing rates were observed at CL, CL-P and P. In a previous study, most units within IHLP exhibited a single preferred direction of firing at CL and this was consistent with the overall analysis of these IHLP units.9 Most muscle fibres within IHLP are oriented along the overall direction of the IHLP22 which is 458 to the sagittal plane.20 Such an arrangement of muscle fibres would be consistent with a single preferred direction of firing at CL in the horizontal plane. Together with the conclusions concerning the preferred directions for SHLP, namely force level dependence and tendency to cover a broader range of directions from CL through to P, we believe our data are consistent with the notion that, functionally, SHLP and IHLP should be regarded as a single muscle. Further, the functional complex-
Fig. 4 – (A and B) The mean firing rates of all subjects’ SMUs as force increases from 400 to 800 gwt (3.92–7.84 N) (A) and as direction changes from CL through to IL (B). CL: contralateral, CL-P: contralateral protrusion, P: protrusion, IL-P: ipsilateral protrusion and IL: ipsilateral.
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ity identified within SHLP and IHLP5,6,10 suggest that there is a gradation of functional properties from IHLP to SHLP. Further data is needed to clarify the contribution to IL from SHLP. It is nonetheless recognised that the comparison data from IHLP were recorded from a different group of subjects and a more rigorous argument for the proposal, that SHLP and IHLP should be regarded as one muscle, would come from recordings from both heads of the muscle in the same individuals, albeit technically very difficult.
4.2.
protrusive jaw movements.14 Therefore, we believe that, during chewing, SHLP will deliver horizontal force vectors on the condyle to move the condyle in a range of contralateral and protrusive directions in the horizontal plane. We also have no data as to the effects of variations in musculoskeletal form on SHLP activity patterns and this could be an aspect for future studies. In addition, future studies could more precisely define the SMUs being recorded by characterizing SMU anatomy through magnetic resonance images.
A comment on rate coding and recruitment 4.4.
Human jaw muscles seem to rely more on rate coding than on recruitment of SMUs to increase contraction23 but in limb muscles, motor units were recruited over the entire range of the contraction.24 In this study, the force ranges allowed SMU discrimination over 10–20% of the horizontal maximum voluntary contraction (horizontal MVC: 35–40 N, Uchida, personal communication). We were able to identify clearly the presence of SMUs that increased firing rates as force increased from a lower step level to higher force levels (low and high threshold units) and also SMUs that were recruited during the dynamic phases when the force levels rapidly increased at the higher force levels (i.e., at 700 and 800 gwt, higher threshold units; see7). Therefore, up to 20% of horizontal maximum voluntary contraction, the SHLP relies on both rate coding and recruitment to increase voluntary contraction.
4.3.
Limitations and future studies
The use of a standard force level across the five directions of force application may be a factor influencing the changes in EMG activity observed across the five directions. It is possible that the relative contributions of all the jaw muscles involved in the tasks may change with force direction (see8,9). Thus in one direction, SHLP’s function may be to contribute proportionally greater to the force generated, in relation to the other jaw muscles, than in another direction. This issue could be addressed in future studies by calculating force levels as a proportion of jaw muscle EMG activity at maximum voluntary contraction. Another limitation was that the data in the present study were compared qualitatively with previous studies8,9 whose data was collected several years earlier. However, in both these earlier and the present studies the protocol, equipment and data analyses were the same, as were most of the experimenters. Therefore, we believe the data to be essentially comparable. Another limitation of the study relates to the general applicability of these and other data from our laboratory to the way the SHLP and IHLP functions under other movements such as chewing, speech, etc. It is not possible to address this issue definitely as we have not published data on the functional properties of SHLP SMUs during chewing, however, the properties observed in SHLP SMUs during this isometric task are consistent with data previously reported for SHLP for an isotonic task.5 Further, we have previously shown that multi-unit EMG activity from SHLP exhibits graded relations with displacement as the teeth were slid against each other during contralateral and
Conclusions: SHLP and IHLP as one muscle
Given the similarities in functional properties between the present isometric force data and previous isometric force data from the IHLP,8,9 together with the similarities in functional properties of SMUs in SHLP and IHLP during jaw movements5,6,10,25, we interpret these data as supporting the hypothesis4 that the lateral pterygoid should be regarded as a . . .system of fibers (that) acts as one muscle, with varying amounts of evenly graded activity throughout its entire range, with the distribution shaded according to the biomechanical demands of the task.
Acknowledgments This investigation was supported by the National Health and Medical Research Council of Australia (Grants #990460 and 302005), the Australian Dental Research Foundation Inc., the Dental Board of NSW, and an AusAID scholarship to Dr Supanigar Ruangsri. We also acknowledge the Department of Radiology, Westmead Hospital for the computer tomography scans. Dr Supanigar Ruangsri on leave from Faculty of Dentistry, Khonkaen University, Mittraphab Road, Muang, Khonkaen 40002, Thailand. The research was based on a thesis submitted to the Faculty of Dentistry, University of Sydney, for the MScDent degree.
references
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