Jaw Function and Orofacial Pain Research Unit, Faculty of Dentistry, University of Sydney, Westmead Centre for Oral Health, Westmead Hospital, Westmead, NSW 2145, Australia
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ABSTRACT |
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Phanachet, I., T. Whittle, K. Wanigaratne, and G. M. Murray. Functional Properties of Single Motor Units in Inferior Head of Human Lateral Pterygoid Muscle: Task Relations and Thresholds. J. Neurophysiol. 86: 2204-2218, 2001. The aim of this study was to clarify the normal function of the inferior head of the human lateral pterygoid muscle (IHLP). The hypothesis was that an important function of the IHLP is in the fine control of horizontal jaw movements. The activities of 99 single motor units (SMUs) were recorded from IHLP (22 recordings from 16 subjects). Most recording sites were identified by computer tomography (CT). All 99 SMUs were active during contralateral jaw movements with the teeth apart, and protrusive jaw movements with the teeth apart, and 81% (48 of 59 units studied during all 3 tasks) were active during submaximal jaw-opening movements. None were active on maximal ipsilateral or retrusive jaw movements with the teeth apart nor on jaw closing/clenching in intercuspal position; nor were they spontaneously active when the jaw was at the clinically determined postural jaw position. Thresholds of SMUs ranged from <0.2 mm of contralateral or protrusive horizontal displacements to 61-89% of the maximum contralateral or protrusive displacement, respectively. For the 35 units continuously active during the contralateral task, 23 (66%) were recruited within 2 mm of contralateral displacement [25 (63% of 40 units) for protrusion]. Recruitment thresholds (mm) of some of the units were rate dependent with thresholds significantly decreasing with increasing rate of horizontal jaw movement in protrusion and contralateral movements. At eight recording sites where up to six SMUs were able to be discriminated, the average thresholds of successively recruited SMUs were within a 1-mm increment of horizontal jaw displacement. After dividing IHLP into four regions, the SMUs recorded in the superior-medial zone exhibited significantly lower mean threshold values than for the SMUs recorded in the other zones (no units were recorded in the inferior-lateral zone). This provides suggestive evidence supporting previously proposed notions of functional heterogeneity within IHLP. Taken together, the data suggest that specific regions of the IHLP are capable of selective activation in a finely controlled manner to allow the application of the appropriate force vector (magnitude and direction) to effect the required condylar movement needed for the generation and control of horizontal jaw movements.
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INTRODUCTION |
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The human lateral
pterygoid muscle (LP) has been implicated as playing an important role
in the control of jaw movements and, by virtue of its direct insertion
into the condyle and disk-capsule complex of the temporomandibular
joint (TMJ), in the control of TMJ function (Dubner et al.
1978; McNamara 1973
; Wilkinson
1988
). The LP consists of two heads or bellies, an upper or
superior head (SHLP) and a lower or inferior head (IHLP). In general
terms, many electromyographic (EMG) studies suggest that the IHLP plays a role in opening, protrusion, and contralateral jaw movements, that
the SHLP plays a role in closing, retrusion, and ipsilateral jaw
movements, and that there is a reciprocal relationship between the
activity of the SHLP and the IHLP (Hannam and McMillan
1994
; Hiraba et al. 1995
, 2000
; Kamiyama
1961
; Klineberg 1991
; Miller 1991
). However, there is a very limited understanding, and
controversy between studies, as to the precise role that both heads of
the muscle play in jaw and TMJ function. For example, some studies indicate activity in IHLP on clenching in intercuspal position (Mahan et al. 1983
; Widmalm et al. 1987
)
while others suggest that IHLP is inactive in these circumstances
(Murray et al. 1999a
; Wood et al. 1986
).
Further, some previous studies suggest that both heads of the muscle
always act independently (Grant 1973
; Juniper
1984
; Mahan et al. 1983
; McNamara
1973
) while others suggest synchronous activity in both heads
during certain jaw movements (Sessle and Gurza 1982
;
Widmalm et al. 1987
; for reviews, Hannam and
McMillan 1994
; Miller 1991
).
There are a number of possible reasons for the uncertainty and limited
understanding of normal LP function. First the absence of reliable
verification of electrode location within the muscle in most previous
human studies suggests that some of these earlier recordings may have
been from other jaw muscles or from LP but incorrectly attributed to a
particular head of the muscle (Hannam and McMillan 1994;
Orfanos et al. 1996
; Widmalm et al.
1987
). Second, most previous human studies have not accurately
recorded jaw movement to correlate with LP activity, and this has
undermined the ability to identify the task relations of the LP. Third,
recordings have been made of multi-unit activity where it is more
difficult to draw conclusions as to the relative levels of activity in
each head of the LP.
We have recently addressed some of the limitations of previous studies
by recording multi-unit EMG activity from sites verified by computer
tomography (CT) to be correctly located within the LP and from subjects
in which jaw movements have been accurately recorded in 6 df
(Murray et al. 1999a, 2001
). These studies have supported the hypothesis that the LP plays an important role in the
fine control of horizontal jaw movements. Close associations were
observed between multi-unit LP EMG activity and condylar movement
during contralateral and protrusive jaw movements (Murray et al.
1999a
). In this previous study, most recordings from IHLP were
not verified by CT, although the recordings from SHLP were verified.
Given that the IHLP has a broad origin and converges onto a narrow
insertion site, it is possible that different IHLP recording sites may
yield different functional characteristics. We have recently provided
evidence that the IHLP is functionally heterogeneous, that is, that
selective activation of subcompartments within the IHLP can occur to
allow the application of the appropriate force vector (direction and
magnitude) to effect the required condylar movement (Murray et
al. 1999c
). This concept is also consistent with a previous
proposal of LP function (Hannam and McMillan 1994
). It
is possible therefore that only part of the IHLP might exhibit a role
in the fine control of horizontal jaw movements and that recordings at
different sites might yield different functional characteristics.
Evidence supporting the hypothesis of functional heterogeneity would be
apparent, for example, if there were to be a preferential grouping to
one part of the IHLP of single motor units (SMUs) with a low threshold
to a particular task and a preferential grouping to another part of the
IHLP of SMUs with a significantly higher threshold to the same task.
The LP has also been implicated as playing an important role in
temporomandibular disorders (TMDs) (Hiraba et al. 2000;
Lund 2000
; Okeson 1998
) that are a
major cause of nondental orofacial pain. These disorders are
characterized by pain in and about the TMJ, limitation of jaw movement,
and TMJ sounds (DeBoever and Carlsson 1994
). The
view that there is hyperactivity or incoordination between the two
heads of the LP is a widespread dental clinical opinion that at least
partly underpins some current modes of treatment of TMD (Hiraba
et al. 2000
; Juniper 1984
, 1987
; Okeson
1998
). However, our understanding of LP function in TMD
patients is even less than our limited understanding of its normal
function, with no reliable studies having ever been performed in TMD
patients. It would be valuable therefore to have baseline information
on the functional properties of SMUs from the LP during standardized tasks in control subjects without TMD. These data could provide the
basis for the design of future studies of the possible involvement of
the LP in TMD.
We have therefore initiated studies to provide rigorous baseline data
on the normal function of the human LP. We chose to study the IHLP
first given previous controversy as well as the uncertainty in our
previous multi-unit EMG study (Murray et al. 1999a) as
to the spatial location of recording sites within IHLP. In the present
paper, we use precise quantification of SMU activity at spatially
identified sites during standardized tasks to address the
hypothesis that the IHLP is concerned with the generation and fine control of horizontal jaw movements. This hypothesis is
proposed because of the following lines of evidence. First, our
previous multi-unit EMG data (Murray et al. 1999a
;
Phanachet and Murray 2000
) supported this hypothesis of
fine control. Second, the arrangement of IHLP muscle fibers suggests
that they are well suited to generating significant horizontal force
vectors on the condyle. Third, the IHLP contains a relatively high
proportion (~80%) of type I muscle fibers (Mao et al.
1992
) that seem best suited to providing continuous work at low
forces. Recruitment thresholds and firing rates are two common features
of SMU activity that may be precisely quantified during tasks and both
have been well described in the limb motor system (Freund
1983
). For example, recruitment thresholds have been shown to
decrease with increasing rate of limb movements (Freund
1983
) and to vary with the direction of a limb movement
(Herrmann and Flanders 1998
). If IHLP is
indeed concerned with the fine control of horizontal jaw movements,
then thresholds should vary in association with different rates
and/or directions of horizontal jaw movement.
The aims of this paper therefore are as follows: to identify
unequivocally the task relations of individual SMUs verified to be
located within IHLP; to identify SMU thresholds in standardized horizontal jaw movement tasks and to determine whether these thresholds vary with the rate or direction of movement as would be expected if
these units were involved in the fine control of these tasks; and to
identify whether there is a relation between CT-verified location and
threshold consistent with a proposal for functional heterogeneity
within IHLP. Some of these data have been briefly reported
(Murray et al. 2001; Phanachet et al.
2000
).
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METHODS |
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Sixteen human volunteers without signs and symptoms of TMD (age
20-41 yr; 12 males, 4 females) and without any history of chronic pain
or neuromuscular condition, participated in this study. All subjects
gave informed consent and all experiment 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 methods have been previously described in detail
(Murray et al. 1999a,b
; Orfanos et al.
1996
; Peck et al. 1997
; Phanachet and
Murray 2000
; Phanachet et al. 2001
), and the
following will review these methods and detail those methods not
previously described.
Electrode placement within IHLP
The method for electrode placement within IHLP (modified from
Wood et al. 1986) involved inserting a sterilized,
precurved needle containing two Teflon-coated, stainless-steel fine
wires through the oral mucosa above the level of the upper second molar tooth. Topical anesthetic was placed around the insertion site prior to
needle insertion. The wires were cut with sterile scissors immediately
prior to placement to provide fresh cut-wire ends for recording. The
needle was advanced to contact the lateral surface of the lateral
pterygoid plate. The needle was then withdrawn, leaving the wires
within the IHLP, and the wires were secured to the buccal surface of
the upper first molar tooth with a small piece of Stomahesive wafer
(ConvaTec, Victoria, Australia) and led out through the angle of the
mouth. At the end of each recording session, five to nine CT-axial
slices (1-3-mm thick) were taken inferior to and parallel with the
clinically approximated Frankfort horizontal plane. The Frankfort
horizontal plane is the plane of best fit to four points on the skull:
the lowermost border of the infraorbital rim bilaterally and the
uppermost border of the bony external auditory meatus bilaterally. An
example of verification data is shown in Fig.
1. The horizontal CT slice (1-mm thick) in A is through the electrode fine-wire tips (black arrow) 7 mm below the roof of the infratemporal fossa. The reformatted images in
B and C (arrows: fine-wire tips) were parallel to
the long axis of the IHLP (B) or through the frontal plane
(C) as indicated in the lowermost CT images. These data
confirmed electrode location within the IHLP and showed the location
within the muscle relative to the boundary of the IHLP. The
data-acquisition equipment was the micro1401 from Cambridge Electronic
Design (Cambridge, UK), the sampling rate was 10,000 samples/s, and
bandwidth was 100 Hz to10 kHz. SMUs were discriminated with Spike2
software from Cambridge Electronic Design. Power spectral analysis
revealed that the highest frequency component of the SMU spike train
was <4,000 Hz.
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Recording of condylar and mid-incisor point movement during standardized tasks
The movement of the mid-incisor point (MIPT, the point between
the incisal edges of the lower central incisor teeth) was recorded with
an optoelectronic jaw-tracking system (JAWS3D, Metropoly AG, Zurich,
Switzerland) (Mesqui and Palla 1985) with a sampling rate limited to 67 samples/s. One lightweight target frame, containing three
light-emitting diodes (LEDs) arranged in a triangle, was attached to
the maxilla and the other to the mandible by custom-made metal clutches
with a rigid rod that projected out of the mouth with minimal
interference to lip competence. The plane of each target frame was
oriented parallel to the sagittal plane, and the longer arm of each
target frame was oriented parallel with the Frankfort horizontal plane.
Cameras monitored the spatial locations of the LEDs. For the data
reported in this paper, the origin of the coordinate system for jaw
displacement was the MIPT. During all recordings, the subjects sat in
an upright position without head support. Since mandibular jaw movement
was recorded in relation to the maxilla, any associated head movement
did not influence the lower jaw motion measurement. The position of the subject's MIPT in the horizontal plane was displayed as a dot (termed
MIPT dot) on a video screen positioned in front of the subject. All jaw
movements were performed with the teeth apart, and movements started
from the postural jaw position. Subjects were instructed to swallow and
relax their jaws with their lips lightly touching to achieve the
postural jaw position. The error of the JAWS3D system bench tested was
0.1 mm (Airoldi et al. 1994
)
for the purposes of the
present study, the spatial resolution was conservatively estimated to
be ~0.2 mm for threshold estimation (Peck et al.
1997
).
Jaw movements were standardized by having the subject move the position of the MIPT dot so as to track a computer-controlled target (Fig. 2A). The target in these standardized tasks was an LED as part of a linear bank of LEDs positioned over the video screen and to the side of the trajectory of the MIPT dot (Fig. 2A). The trajectory of the MIPT dot in the horizontal plane was displayed on the video screen. The LEDs were controlled by scripts written in Spike2 software [Cambridge Electronic Design (CED)] and run on the CED system that was also used to record SMUs (see following text). Only one LED was illuminated at any one time. Movement of the MIPT dot from the location at one illuminated LED to the location at the next illuminated LED corresponded to 0.65 or 1.3 mm of movement at the subject's MIPT depending on the display gain on the video screen. The subject was instructed to perform a few trials of contralateral or protrusive jaw movement to become accustomed to the task. A contralateral movement was defined as a movement of the jaw from postural jaw position to the side opposite to the IHLP recording side followed by a return of the jaw to postural position. A protrusive movement was defined as a movement of the jaw from postural jaw position forward followed by a return to postural position. Both movements were performed without tooth contact. Although subjects were instructed to move the jaw in protrusion, some subjects displayed a deviation to one side or the other. However, these protrusive movements were always distinctly different from the contralateral movements. The linear bank of LEDs was then oriented along the direction of movement of the MIPT dot, which was displayed on the screen in the horizontal plane. The Spike2 software illuminated the LEDs in sequence, and the subject was instructed to move the jaw so the MIPT dot on the screen followed the illuminated LED as smoothly as possible. This program allowed adjustment to the rate and magnitude of jaw movement by changing time-off duration between each LED (e.g., a in Fig. 2B), and time-on duration of each LED (b in Fig. 2B). Three rates were defined: 6.5 mm/s (fast, f in Fig. 2B), 2.2 mm/s (intermediate, s in Fig. 2B), and 1.3 mm/s (slow). The desired amount of displacement could be controlled by varying the highest LED in the bank that was illuminated.
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Standardized tasks
Each movement started with the jaw in postural position for 2-3
s (Fig. 2). During standardized protrusive or contralateral excursion
or jaw opening, the subject was instructed to move the MIPT dot
smoothly and track the target at the rate and magnitude of jaw
displacement controlled by the Spike2 software. The amount of jaw
displacement during each task was determined by the experimenters' ability to discriminate one or more SMUs throughout the task. The
criteria for defining a SMU were similarities in amplitude and waveform
between all representatives of an identified SMU. Then the LEDs were
aligned along the trajectory of MIPT movement, and the LED
corresponding to the required displacement was programmed. Each subject
was required to hold the MIPT dot as much as possible within the
boundaries of the LED that was illuminated for the holding-phase period
of the step displacement. The jaw was then returned to the postural
position again following the return targets, and this concluded the
trial. This standardized task was termed the single-step
task. To study the effects of rate of jaw movement on the
threshold of SMUs, the subject was instructed to track the target at
fast, intermediate, and slow rates (see preceding text). The fastest
rate of movement was about the fastest that our subjects found
comfortable to perform. Although subjects could move slower than the
slowest rate of movement, this rate was also comfortable for the
subjects. Each task was repeated five to seven times with a rest period
of 1 min between trials. By changing the alignment of the linear bank
of LEDs, it was possible to change the direction along which the
subjects moved their jaw. Thus subjects tracked the targets so as to
move the jaw to the side contralateral to the side of IHLP EMG
recording, or with a change in the orientation of the LEDs, in
protrusion or jaw opening. A multiple-step task involving two to three
step levels was also performed in which the rate of illumination of the
LEDs required subjects to move the jaw in the horizontal plane to two
to three sequential holding phases or step levels (3-5-s duration)
(Phanachet et al. 2001
). The multiple-step task was not
used for standardized jaw opening.
We have previously established criteria for successful performance of a
task by subjects (Phanachet et al. 2001). Trials that did not meet these criteria were not included in further analysis. Figure 2B, for example, illustrates a close match between
target lines (
) and averaged MIPT traces (- - -) during jaw
movement without tooth contact in one subject. The diameter of each LED (2.8 mm) is represented as the shaded area and, during jaw movements, subjects tracked the target by moving the dot to any point within the
diameter of an LED (e.g., center or the boundary of the LED). A MIPT
trace was considered acceptable during the holding phases of a task
when, from a minimum of five trials, at least part of the shaded target
area fell within 1 SD of the mean MIPT displacement for at least two
mean data points calculated at 750-ms intervals and in addition was
always <2 SDs of the mean at any data point. The same criterion was
used for each dynamic phase of each movement, that is, the outgoing
phase and the return phase of a movement.
Before the standardized tasks were performed, EMG activity from IHLP was studied during nonstandardized maximal contralateral, protrusive, and retrusive jaw movement and submaximal jaw-opening movements, and clenching in intercuspal position (normal biting between the teeth). These tasks were performed to provide an overall assessment of the motor activity to which the units at the site were related. These movements were termed the nonstandardized tasks as there was no visual feedback to the subject of the movement. All except two SMUs were characterized during standardized horizontal isotonic displacements contralateral to the recording side and in protrusion. Some units were also studied during standardized jaw-opening movements although wide jaw opening in both standardized and nonstandardized movements was avoided to minimize the danger of losing units. The remaining two units were only studied during nonstandardized contralateral, ipsilateral, protrusive, and jaw-opening movements in which the subject was instructed to move the jaw as far as comfortable in each movement task. All SMUs recorded during single-step and/or multiple-step displacements were included in the analysis as to the tasks to which the SMUs were related.
In this paper, thresholds are reported in terms of MIPT displacement. To provide an indication of SMU thresholds in relation to condylar displacement, an assessment was made of condylar displacement at each 1 mm of MIPT displacement. During the contralateral movement in the horizontal plane, there was on average a 35 ± 5° difference between the average trajectory made by the MIPT and the average trajectory along which the condyle moved. The trajectory along which the condyle moved was determined on the axial CT scans as coincident with the long axis of the lateral pterygoid muscle. The MIPT trajectory was determined as the line of best fit through the MIPT displays on horizontal plots. The relative displacements in three dimensions were calculated at 1-mm intervals for both the MIPT and the clinically palpated lateral condylar pole in a representative trial of contralateral movement in each subject. The clinically palpated lateral condylar pole was included as an additional reference in each subject prior to recording. The mean ratio of lateral condylar pole displacement to MIPT displacement at each 1-mm interval of contralateral displacement was 0.67 ± 0.22, range = 0.21-1.02 mm [3-dimensional (3D) coordinates], which indicates that on average, the condyle moved ~70% of the displacement at the MIPT. Although both condyles ideally move forward symmetrically during a protrusive movement, many subjects MIPTs deviated with protrusion and the mean ratio of lateral condylar pole displacement to MIPT displacement at each 1-mm interval for protrusion was 0.70 ± 0.20 mm, range = 0.33-1.02 mm (3D coordinates).
For the purposes of assessing location of electrode recording site
within IHLP, the muscle was arbitrarily divided mediolaterally into
medial and lateral regions, and superior-inferiorly into superior and
inferior regions. Location was assessed by viewing the electrode tip in
relation to muscle boundaries on a horizontal CT scan through the
electrode tips. The amount of bend back of the wires (2-3 mm) was
taken into account when assigning location. Previous histological
studies have indicated that the SHLP is ~5-mm thick
superior-inferiorly (Meyenberg et al. 1986;
Moritz and Ewers 1987
; Widmalm et al.
1987
; R. Hawthorn, personal communication), and we therefore
adopted this criterion for identifying the upper boundary of the IHLP.
The remainder of the LP extending inferiorly to the lower border of the
lateral pterygoid plate was considered to be IHLP.
Data analysis
For each subject, MIPT displacement data for each task-defined movement were plotted along the anterior-posterior (x, + posteriorly), mediolateral (y, + to right), and superior-inferior (z, + superiorly) axes for lateral and protrusive jaw movement, respectively. An analysis of the general features of task relations was conducted for all SMUs recorded during single-step and/or multiple-step displacements. An assessment of threshold was made only for the units that fired continuously throughout the single-step task and without a significant interruption in firing rate (i.e., all interspike intervals <160 ms) for the duration of the holding phase. Threshold was defined as the magnitude of jaw displacement when the first action potential occurred (Fig. 3). An action potential was disregarded for threshold assessment if it occurred >160 ms before the next action potential. Threshold values were averaged over at least five trials. Jaw displacement was calculated as the shortest distance in three dimensions from postural jaw position to the position of the jaw at which the unit started firing. Threshold was also calculated along the y axis for contralateral movement, and x axis for protrusion. Most values are reported as the shortest distance in three dimensions unless specified along a particular axis. In this paper, thresholds are reported below in terms of MIPT displacement to provide IHLP data in relation to a commonly used reference point on the mandible. Thresholds of each SMU at different rates were compared by using the Kruskal Wallis test (KWT) for three rates and Mann-Whitney U test (MWU) for two rates, given that the threshold values were not normally distributed. For the analysis of the differences in displacement between successively recruited SMUs recorded at any one site, continuously active units were analyzed.
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RESULTS |
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General features of task relations
A total of 99 SMUs were discriminated from the right IHLP in 22 recording sessions from 16 subjects. Verification by CT was obtained in 17 of the 22 recording sessions. All 99 SMUs were examined for activity at postural jaw position, and during clenching in the intercuspal position, and nonstandardized retrusion and ipsilateral jaw movement. Of the 99 units, 97 were examined for activity during standardized (i.e., single-step and/or multiple-step displacements) protrusion and contralateral movement while two units were studied during nonstandardized protrusion and contralateral movements.
None of the 99 units was spontaneously active when the jaw was in the clinically determined postural jaw position whether assessed at the beginning, during, or at the end of a 4-h recording session. None of the units were active during the nonstandardized tasks of retrusion, ipsilateral jaw displacements or clenching in intercuspal position. All 99 units were active during contralateral and protrusive jaw movements. Of these 99 SMUs, 59 were examined for activity during jaw opening. Of these 59 units, 48 (81%) were active during all three movements (contralateral, protrusion, and jaw-opening), and 11 (19%) were active on contralateral and protrusive movements only. Six of these 11 units only gave brief bursts of activity during the tasks while the other 5 were continuously active units with higher thresholds than the other units. Since the 59 units were tested for activity during jaw opening that ranged from 22 to 58% of maximum jaw opening, it is possible that these 11 units would become active at greater magnitudes of jaw opening.
Figure 3 shows representative SMU data of the 81% that were active during protrusion (A), a contralaterally directed jaw movement (B), and an open-close jaw movement (C). The same three SMUs were recorded simultaneously during each movement. Each short vertical line is a spike-train pulse that indicates the time of occurrence of a SMU action potential. Raw data from the segment delineated by the dotted vertical lines in A are displayed at the bottom of A with the units labeled 1-3 corresponding to the appropriately labeled spike-train pulses. The top three traces in each panel show displacement. This subject consistently deviated the jaw to the ipsilateral side during protrusion (A, top; see METHODS). However, the SMU activity was considered to relate to protrusive jaw displacement because there was no activity during ipsilateral movement in any subject.
Threshold of firing of SMUs
For the study of SMU threshold, only the units that fired tonically during the holding phases of single-step displacements were analyzed. According to this criterion, 35 of 99 units were analyzed during contralateral displacements, 40 were analyzed during protrusive displacements, and 29 of the units were studied during both contralateral and protrusive displacements. The units not meeting this criterion, that is they were either not studied in the single-step task or exhibited a phasic and sporadic pattern of firing during the dynamic phase only, were however assessed for task relations, as indicated in the preceding text.
RANGE OF THRESHOLDS FOR FIRING. The sample of SMUs from IHLP exhibited a range of activation thresholds. The dotted line labeled T in Fig. 3 represents displacement threshold for unit 1. The threshold of firing of SMUs exhibited a broad range from <0.2 mm of displacement, the level of resolution of the JAWS3D tracking system (see METHODS) to a contralateral displacement of 6.2 mm or a protrusive displacement of 7.3 mm when assessed at the intermediate rate of movement (see following text). As the average maximum displacements of the MIPT of subjects in contralateral movement and protrusion were 10.2 ± 1.6 mm (range: 8-12 mm) and 8.2 ± 2.0 mm (range: 6-10.5 mm), respectively, the thresholds of the population of SMUs ranged from very low (supporting a role in fine control) to ~61 or 89% of the maximum possible range of contralateral or protrusive horizontal displacements.
Figure 3B shows two units that commenced firing near the onset of movement (units 1 and 2). It also shows a unit (3) commencing firing at the end of a 7-mm contralateral displacement. Figure 4 shows frequency histograms of the thresholds of the 35 IHLP units recorded in contralateral movement (A) and the 40 units in protrusion (B). Each graph exhibits a bimodal distribution with a peak at both low and high thresholds. Of the 35 units in A, 23 (66%) were recruited within 2 mm of contralateral displacement [25 (63%) for protrusion]. The remaining 12 units (34%) were recruited at >2 mm of contralateral displacement [15 units (37%) for protrusion]. This bimodal distribution probably reflects sampling bias toward more easily discriminable small, low-threshold units rather than the observed low frequency of higher-threshold units.
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DEPENDENCE OF THRESHOLD ON RATE OF MOVEMENT.
The strongest influence on recruitment is the speed of a movement
(Freund 1983). Therefore another feature of SMU activity supporting a role for IHLP in the fine control of horizontal jaw movements would be a change in the threshold of recruitment with a
change in the rate of horizontal jaw movement. The thresholds of each
IHLP unit were therefore studied during two to three rates of movement.
For the contralateral movement, analysis of individual units showed
that the threshold of firing of 12 (34%) of 35 units was significantly
different (KWT or MWU; P < 0.05) at different rates of
movement. Figure 5A plots mean
threshold values for these 12 units. For protrusion, the threshold of
firing of 10 (25%) of 40 units were significantly different (KWT or
MWU; P < 0.05) at different rates of movement (Fig.
5B).
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CONTROL FOR EFFECTS OF JAW OPENING. It is considered that there was little or no effect of any slight jaw opening on the threshold values observed in the contralateral or protrusive jaw movement tasks. For the contralateral or protrusive tasks, the mean (±SD) threshold in the z axis (i.e., superior-inferior) for the nine units that were also studied during standardized jaw opening was 0.6 ± 0.4 mm for contralateral movement and 0.9 ± 1.2 mm for protrusion. However, the mean threshold of these units during standardized jaw opening was 4.8 ± 1.7 mm in the z axis. For example, in Fig. 3 during protrusion (A) and contralateral movement (B), the thresholds in the z axis for unit 1 were ~3 and 1 mm, respectively, while the threshold in the z axis during jaw opening (C) for this unit was ~7 mm.
THRESHOLD AND DIRECTION OF MOVEMENT. For 29 SMUs studied in both contralateral and protrusive tasks, the correlation between the recruitment thresholds in protrusion and contralateral displacement was r = 0.69 (P < 0.01). The mean (±SD) threshold value of 2.1 ± 2.2 mm (n = 29) assessed at the intermediate rate of protrusive jaw movement was greater than but not significantly different (P > 0.05; Wilcoxon signed-ranks test) from the value of 1.5 ± 1.1 mm for contralateral movement.
Recruitment features of SMUs during tasks
An assessment was made of the differences in displacement thresholds of successively recruited SMUs to determine whether recruitment is involved in the generation of the small incremental forces required for small increments in jaw displacements. Table 2 shows the mean (±SD) differences in threshold values between successively recruited units. At any one site, the first unit recruited in the displacement was arbitrarily labeled unit 1, the second unit recruited was labeled unit 2, and so on. The data demonstrate the small displacements, close to the level of resolution of the jaw-tracking system, between successively recruited SMUs. For example, at each of the recording sites and over the first ~2 mm of contralateral or protrusive displacement, up to five SMUs could be recruited in a staggered fashion. The small displacements with which units were recruited are also illustrated in Fig. 8, which shows on an expanded time scale the activity of five SMUs recorded during a single-step protrusive displacement. Units were recruited at small displacement increments.
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Locations of units within IHLP and threshold values
Table 3 lists the mean thresholds of SMUs recorded according to site within IHLP during protrusion (A) and contralateral movement (B). Although sample size was small, the SMUs recorded in the superior-medial zone during protrusion and contralateral movement exhibited significantly lower mean threshold values than for the SMUs recorded in the other zones (KWT; P < 0.001). No SMUs were recorded in the inferolateral zone of the IHLP. An assessment was also made as to whether units whose thresholds were affected by the rate or the direction of movement were localized to a specific region. There was no significant association between the location of units and the number of units showing differences of threshold at different directions (P = 0.2; Fisher's exact test; Table 4) or rates (P > 0.05; Fisher's exact tests; Table 5) of movement.
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DISCUSSION |
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Task relations of IHLP SMUs
This paper provides the first detailed description of the
activities of SMUs recorded from CT-identified sites within the human
IHLP. The sample of units allows a clear definition of the task
relations of the IHLP with all units being active during contralateral
and protrusive jaw movements with the teeth apart. Although only a
proportion of units tested were active during jaw opening, it is very
likely that all units would be active at or before maximum jaw opening
since the remaining 19% of units either gave brief bursts of activity
(i.e., phasic units below their tonic threshold) (Freund
1983) or were relatively high-threshold tonic units in
horizontal movement. The sampling of units from a broad distribution
within the muscle suggests that no part of the IHLP makes an active
contribution to ipsilateral and retrusive movements with the teeth
apart nor on jaw closing/clenching in intercuspal position.
The data provide good evidence for an involvement of the IHLP in the
generation of contralateral, protrusive and jaw-opening movements.
These findings are generally consistent with the patterns of activity
reported in the many previous human and experimental-animal multi-unit
EMG studies (for reviews, Hannam and McMillan 1994; Klineberg 1991
; Miller 1991
;
Murray et al. 2001
). For example, the findings are
consistent with previous conclusions that the IHLP is concerned with
pulling the condyle forwards along the articular eminence during
protrusion and contralateral jaw movements (e.g., Miller
1991
; Wilkinson 1988
). In a study where jaw
displacement was recorded but where electrode site verification data
were not obtained (Hiraba et al. 2000
), correlations
were demonstrated between the level of EMG activity in IHLP and
anterior condylar translation.
Not only do the data demonstrate the task relations of these units, but
the data show these units exhibited a continuous spectrum of thresholds
ranging up to contralateral or protrusive displacements of 61-89% of
the maximum recorded in our subjects. Given that most functional
movements would appear to lie well within the range of 61-89% of
maximum (Lundeen and Gibbs 1982), these data implicate IHLP not only in the generation and control of these contralateral, protrusive, and jaw-opening movements but also most jaw
movements requiring horizontal vector components. For example, chewing
cycles are not simply open-close jaw movements but are usually
associated with jaw movements containing significant horizontal vector
components (Lundeen and Gibbs 1982
). Previous studies
have suggested that the IHLP is active during the late intercuspal
phase and the opening phase of the chewing cycle (Dubner et al.
1978
; Møller 1966
; Wood et al.
1986
). It is proposed that the IHLP is involved in the
generation of those horizontal vector components evident in these
phases of the chewing cycle.
In light of our present findings, it appears that the reports of IHLP
activity on clenching in intercuspal position (Mahan et al.
1983; Widmalm et al. 1987
; Wood et al.
1986
) reflect recordings from units located in other muscles
such as medial pterygoid that has an additional origin from the lateral
surface of the lower border of the lateral pterygoid plate
(Widmalm et al. 1987
). Further studies are needed to
determine whether the reports of IHLP activity during vertically
directed clenches with the jaw positioned to the ipsilateral side or in
protrusion (Mahan et al. 1983
; Wood et al.
1996
) reflect true IHLP activity or whether in fact these activities represent cross-talk from medial pterygoid motor units.
The absence of spontaneous activity in any of the SMUs when the jaw was
in the clinically determined postural jaw position is consistent with
previous descriptions (e.g., Mahan et al. 1983). The
data suggest that at the postural jaw position there is no anteriorly
directed force on the condyle and disk from active muscle contraction
in the IHLP maintaining the condyle in close apposition with the disk
and articular eminence.
Role in fine control of jaw movements
The data also suggest that the IHLP is involved in the fine control of these horizontal jaw movements since SMU activity features varied closely in association with the dynamic parameters of the movement. First, successively recruited SMUs could be recruited at small increments in displacement. Second, the lowest thresholds of the SMUs were <0.2 mm of horizontal jaw displacement, and this suggests an important role in the initiation of the movement. Third, recruitment thresholds of some SMUs were rate dependent, suggesting that these SMUs were intimately concerned with subtle changes in the rate of jaw movement. Not all SMUs exhibited significant rate-dependent features, although a high proportion of the total number of comparisons available between the three rates of movement illustrated decreases in threshold with increases in the rate of movement. Further studies are needed to determine whether, with a larger sample of trials for each SMU recorded, a higher proportion of SMUs would exhibit significant rate differences. Nonetheless, the data suggest that the relevant motor centers (e.g., face motor cortex) are capable of activating the IHLP in a finely controlled manner.
This role for the IHLP in the fine control of horizontal jaw movements
is also consistent with previous descriptions where multi-unit IHLP EMG
activity was shown to modulate in close association with small
fluctuations in condylar movement that reflected variations in the rate
of jaw movement as the teeth slid past each other during contralateral
or protrusive jaw movements (Murray et al. 1999a, 2001
).
Other jaw muscles (masseter, anterior and posterior temporal muscles,
submandibular group) demonstrated weaker associations with the
contralateral and protrusive movements (Murray et al. 1999a
) (see following text).
There is also histochemical evidence supporting such a role for the
IHLP. The SMUs within the IHLP appear to be predominantly aerobic (slow
contracting and fatigue resistant, ~80%) (Mao et al.
1992) and suited to low forces and prolonged contraction times. There is also little evidence for pennation within IHLP that suggests that the IHLP is more suited to isotonic than isometric operational conditions (Hannam and McMillan 1994
; van Eijden
et al. 1995
, 1997
). Thus the presence of long fibers (~22 mm)
(Schumacher 1961
; van Eijden et al. 1995
,
1997
) with many sarcomeres in series arranged in the same line
of action as the bulk of the muscle and with small cross-sectional
areas provides an architecture most suitable for shortening over longer
distances than seen in masseter and medial pterygoid, which are more
suited to high power generation over short distances.
This fine control may extend to the activation of specific regions
within the IHLP given the suggestive evidence provided in this paper
for functional heterogeneity that has been previously put forward by us
and others (Foucart et al. 1998; Hannam and McMillan 1994
; Murray et al. 1999c
, 2001
). Such
a notion of functional heterogeneity is not new to the jaw motor system
as it has already been well characterized in temporalis and masseter
muscles (Blanksma and van Eijden 1990
, 1995
). The
activation of specific regions within IHLP would allow the application
of the appropriate force vector (magnitude and direction) to effect the
required condylar movement. This would provide the possibility of
considerable sophistication of delivery of different force vectors on
the condyle to perform the desired jaw movements. The present paper
provides suggestive evidence supporting this notion in that, for each
task, SMUs with lower thresholds tended to be grouped in the
superior-medial zone within IHLP (see following text). Given possible
sampling bias in different locations as well as the small sample size,
the data are only suggestive of the possibility of differential
activation within IHLP. Further SMU evidence is needed to confirm
whether functional heterogeneity is a feature of IHLP. Good evidence
for functional heterogeneity would be obtained, for example, by
demonstrating reversals of recruitment order among SMUs with changes in task.
Role of other jaw muscles
The present paper studies the role of the IHLP as a contributor to
horizontal jaw movements. The data do not rule out roles for other jaw
muscles in these movements. For example, the masseter, medial pterygoid
and posterior temporalis muscles contain fibers capable of generating
force vectors with horizontal components, and this is in accord with
previous descriptions of the patterns of recruitment of these muscles
during horizontal jaw movements (for reviews, Hannam and
McMillan 1994; Miller 1991
). Although recent
multi-unit EMG data suggest a less notable role than the IHLP for some
of these other jaw muscles in horizontal jaw movement generation
(Murray et al. 1999a
), verified SMU recordings at the same resolution as done in the present study will be needed to determine the role of other muscles in these movements.
Dependence of threshold on rate and direction of movement
Motor units are recruited at successively lower force levels as
the speed of a movement or isometric contraction increases (for
reviews, Freund 1983; Henneman and Mendell
1981
). There have been no detailed studies of such possible
associations in the jaw-motor system. In accordance with the findings
in the spinal motor system, the present study has demonstrated an
association between the rate of horizontal jaw movement and recruitment
threshold. Although we did not measure force in these tasks, we believe
that faster rates of horizontal jaw displacement are associated with increases in the rate of force delivery required to effect the faster
horizontal jaw movement. This increase in the rate of force delivery is
needed given the viscoelastic nature of the tissues attaching the jaw
to the skull (Peck et al. 2000
). The rate data also
showed that the higher threshold units modified their onset thresholds
with rate of movement, but there was not as large an influence of rate
of movement on the threshold of units that have lower overall
threshold. These data are entirely consistent with the findings of
Yoneda et al. (1986)
with different speeds of isometric
contraction in limb muscles.
In this study, movements started at the postural jaw position and all tasks were performed with the teeth apart. It is unlikely that the small amount of jaw opening from tooth contact in lateral movements (2-3 mm) would have had a major affect on the threshold values. This is because threshold for a given unit during jaw opening in the z axis was always much higher than the amount of jaw opening during the contralateral or protrusive jaw movements. Further studies are needed to determine the effect, if any, of horizontal displacement on the opening thresholds of IHLP units.
Directional effects on EMG activity have been observed in other jaw
(Mao and Osborn 1994) and limb muscles (Herrmann
and Flanders 1998
). The small sample size may contribute to the
lack of significant effect of direction of movement on thresholds of
firing of IHLP SMUs. Further studies are needed to determine whether
significant directional relations are observed in the IHLP.
Verification
A major limitation of most previous studies of the human IHLP has
been the absence of reliable verification that electrodes were
correctly located within the IHLP and not other jaw muscles. In the
absence of a reliable verification technique such as CT imaging (e.g.,
Fig. 1), conclusions about IHLP function drawn from these studies are
questionable given the very real possibility of electrode misplacement
in other jaw muscles or the electrodes may have been within IHLP but
incorrectly attributed to a particular head of the muscle
(Hannam and McMillan 1994; Orfanos et al.
1996
; Widmalm et al. 1987
). Therefore despite
recent claims to the contrary (Hiraba et al. 2000
), it
is not possible to rely on EMG patterns as the sole basis for verifying
that electrodes are correctly located within the IHLP.
In our experiments, electrodes were clearly seen in relation to muscle
outlines on the CT scans, and this allowed the confirmation of
electrode location within the IHLP and not within nearby muscles such
as medial pterygoid, temporalis, and SHLP. The separation between SHLP
and IHLP was not, however, always clear on the CT scans, and in such
cases, the SHLP was assigned an arbitrary thickness of 5 mm from the
roof of the infratemporal fossa, and this was based on previous
anatomical studies (Meyenberg et al. 1986; Moritz and Ewers 1987
; Widmalm et al. 1987
; R. Hawthorn, personal communication). However, even using this arbitrary
criterion, the task relations of SMU activity recorded in the superior
part of the muscle were entirely consistent with those of SMUs recorded
in the other zones of the muscle. For those few units at sites where
verification was not obtained, we were still confident that our
electrodes were correctly located within the IHLP as the patterns
observed matched the reliable patterns that we consistently obtained at the verified sites. No EMG activity was ever recorded in IHLP at
intercuspal position clenching in this and all our previous studies
(for review, Murray et al. 2001
). We therefore do not believe that any of our recordings were from SMUs within the medial pterygoid muscle or temporalis, nor indeed SHLP, the most likely muscles from which erroneously attributed recordings could have been made.
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ACKNOWLEDGMENTS |
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We thank P. Sindhusake of Westmead Hospital for excellent statistical advice and T. Bowerman for secretarial assistance. We also acknowledge the Department of Radiology, Westmead Hospital, for the CT scans and the photographic and art services of Westmead Hospital. I. Phanachet was a Royal Thai Government Sponsored Scholar.
This research was supported by the National Health and Medical Research Council of Australia (Grant 990460), the Australian Research Council Small Grants Scheme, the Australian Dental Research Foundation, Inc., the Dental Board of New South Wales, the Dental Alumni Society of the University of Sydney, and the University of Sydney Research Grants Scheme.
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FOOTNOTES |
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Address for reprint requests: G. M. Murray, Jaw Function and Orofacial Pain Research Unit, Faculty of Dentistry, University of Sydney, Level 3, Professorial Unit, Westmead Centre for Oral Health, Westmead Hospital, Westmead, NSW 2145, Australia (E-mail: gregm{at}mail.usyd.edu.au).
Received 5 March 2001; accepted in final form 22 June 2001.
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REFERENCES |
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