An electromyographic analysis of orofacial motor activities during trained tongue-protrusion and biting tasks in monkeys

Arths oral Bid. Vol. 39, No. I I, pp. 955-965, I994 Copyright 0 1994 Elsevier Science Ltd

Pergamon

0003-9969(94)00067-O

Prmted in Great Britain. All rights reserved 0003-9969/94 $7.00 + 0.00

AN ELECTROMYOGRAPHIC ANALYSIS OF OROFACIAL MOTOR ACTIVITIES DURING TRAINED TONGUE-PROTRUSION AND BITING TASKS IN MONKEYS E. M. MOUSTAFA,’ L.-D. LIN,* G. M. MURRAY’ and B. J. SESSLE’* ‘Faculty of Dentistry, University of Toronto, Toronto, Ontario, Canada, ‘School of Dentistry, National Taiwan University. Taipei, Taiwan and ‘Department of Prosthetic Dentistry, University of Sydney, Surrey Hills, NSW, Australia (Accepted 14 July 1994) Summary-This study sought to characterise the electromyographic (EMG) activity patterns of orofacialmuscles during trained tongue-protrusion and biting tasks in two awake monkeys (Macacafascicularis). Chronic or acute EMG electrodes were placed in the anterior digastric (DIG), genioglossus (GG), masseter (MASS), platysma (PLAT), zygomaticus major (ZYGO), orbicularis oris superior (OOS), and orbicularis oris inferior (001) muscles and their EMG activity as well as the force signals of the tongue-protrusion and biting tasks were recorded. A total of 327 tongue-protrusion task trials and a total of 210 biting-task trials were successfully completed in several recording sessions and the EMG patterns were generally consistent between the different sessions. For the tongue task, the mean onset time of increase in GG activity significantly (p < 0.0001) led the mean onset time of increase in the force. The DIG, GG, and 001 (and also the 00s in one of the monkeys) showed a significant (p < 0.0001) increase in mean EMG amplitude during the holding phase, but the GG in both monkeys had the highest mean EMG amplitude ratio (MAR), i.e. the mean EMG amplitude during the holding or dynamic phase divided by the mean EMG amplitude during the pre-trial period. A similar EMG pattern was documented for different directions of the tongue-protrusion task (right, symmetrical, and left) and changes in the levels of EMG activities occurred in GG and 001 as the direction of the tongue-protrusion task changed from left to right, The task at different forces was associated with no apparent change in MAR for the holding phase for each muscle recorded. However, during the dynamic phase, only the GG showed a significant increase in EMG activity as the forces were increased. For the biting task, the mean onset times of the MASS activity and force were not significantly different. The MASS and ZYGO muscles (and the PLAT in one of the monkeys) showed a significant increase in mean EMG amplitude during the holding phase compared with the pre-trial period, and the MASS showed the highest MAR. It was also the only muscle showing a significant increase in the EMG activity when the bite-force level was increased. These findings reveal that certain orofacial muscles are selectively recruited during the two different orofacial tasks. Based on the EMG activity pattern during different directions or force levels of the task, the data suggest that, of the muscles recorded, the principal agonist for the tongue task is the GG and that for the biting task is the MASS; the other muscles that may be active appear to serve as accessories to the task. Key words:

monkey,

tongue

protrusion,

biting.

electromyographic,

INTRODUCIION

There is an extensive body activities of the jaw-closing

of information and -opening

about

the

muscles during mastication and biting in man (e.g. Ahlgren, 1966; Gibbs et al., 1981; Moller, 1974; Schieppati, Di Francesco and Nardone, 1989; Van Eijden et al., 1990; Wood, 1986) monkeys (Byrd and Garthwaite, 198 1; Byrd, Milberg and Luschei, 1978; Hylander and Crompton, 1986; Hylander and Johnson, 1985, 1989; Lindauer, Gay and Rendell, 1993; Luschei and Goodwin. 1974; McNamara, 1974; Miller, 1991;

*To whom correspondence should be addressed. Abbreviations: ANOVA, analysis of variance; EMG, tromyographic.

elec-

muscles.

Miller, Vargervik and Phillips, 1985) and subprimates (Gorniak and Gans, 1980; Hiiemae and Crompton, 1985). However, little attention has been given to the functional role of other orofacial muscles such as the perioral facial during mastication and biting, especially in monkeys. Similarly, while there is detailed information on the activity of several tongue muscles during motor functions such as mastication, swallowing, licking, and tongue protrusion (Dubner, Sessle and Storey, 1978; Lowe, 1981; Smith and Kier, 1989; Thexton and McGarrick, 1989) the activity patterns of the perioral facial muscles and the jaw muscles during these functions have not been investigated in detail in monkeys. Therefore, we have now sought to clarify the activity of these muscles in some of these functions in the awake monkey. We chose to examine their

E. M. MOUSTAFAet ul

956

activity in well-controlled motor functions involve biting and tongue protrusion.

that

METHODS

The investigation was made on two female monkeys (Mucaca jkscicularis: H5, H6; weight, 3-3.5 kg), which were maintained in accordance with the guidelines of the Canadian Council for Animal Care. The methods have been described in detail by Murray et al. (1991) and will only be briefly outlined here. Monkeys were first trained to bite with the incisor teeth on to two stainless-steel plates fixed to a straingauge force transducer. The transducer was rigidly mounted to a beam on the ‘primate’ chair in which the animal sat. The output from the transducer controlled the vertical position of a cursor on a video monitor placed 1 m in front of the monkey (see Murray et al., 1991). A baseline ‘window’ was controlled by a target-control computer and appeared at the beginning of a trial at the bottom of the video screen. After a pre-trial period (see below), the window was displaced instantaneously to a preset target level located above the baseline. The appearance of the target window was the visual cue for the monkey to bite with the incisor teeth on to the transducer so that the cursor was moved into the window. The monkey was required to produce a force of 20 N in order to keep the cursor within the centre of the target. To determine the primary muscle(s) contributing to changes in the bite-force levels, one of the monkeys (H6) was also trained to bite on to the biting-task transducer at two additional bite forces (I 7 and 23 N, as well as 20 N; i.e. the pre-set target level was 7.5 and 10.5 cm, as well as 9 cm above the baseline). The tongue-protrusion task involved the same computer and task functions as the biting task (see Murray rt al., 1991). It required the monkey to protrude its tongue symmetrically out of the mouth towards a cone-shaped plate attached to a force transducer mounted rigidly to the chair. One monkey (H6) was also required to produce a force of I .O N to maintain the cursor within the centre of the target window. The monkey was also trained to perform this symmetrical tongue-protrusion task (T,) at additional protrusive forces (0.85 and 1.35 N), and also to perform the tongue-protrusion task to the right and left of the midsagittal plane at a 1.0-N force (Murray and Sessle, 1992b) in order to determine which of the muscles contributed to changes in tongue force and direction. The following periods were defined for the tongueprotrusion and biting tasks (see Murray rt al., 1991): a pre-trial period (randomly varied between 1.0 and I .5 s) during which the baseline window remained at the bottom of the video screen; the reaction time, being the period from target window appearance to the onset of significant rise (see below) in the EMG activity or force-output signal associated with the application of force on to the transducer; a dynamic phase, which was the period from the end of the reaction time to the moment the cursor entered the target window; a force-holding phase, which was the period from entry of the cursor into the target

window to the end of the predetermined holding phase; and a reward delivery phase, which was the l-s period following the end of the holding phase during which the reward (0.4 ml fruit juice) was delivered via a tube attached to each transducer. A single trial was defined for a tongue-protrusion or a biting task as the period from the appearance of the baseline window at the bottom of the video screen to the end of the reward phase. A successful trial was defined as having occurred (and was rewarded) only if all the following criteria were met: the cursor remained within the baseline window during the pre-trial period; the cursor left the baseline window within 3 s of target appearance; and the cursor remained within the target window for a minimum 0.5 s force-holding period. Unsuccessful trials were not rewarded and could occur if any of the above criteria were not fulfilled. As described previously (Murray ef (II., 199 1; Sessle and Gurza, 1982), chronic and acute EMG electrodes were placed in a variety of orofacial muscles. Chronically placed EMG electrodes were implanted in the left anterior digastric, genioglossus, and masseter muscles, and acute EMG electrodes were placed in the left platysma, zygomaticus major, orbicularis oris superior, and orbicularis oris inferior muscles. These seven muscles were chosen because earlier anatomical and physiological studies in man and monkeys had shown that these are the most likely to be involved in the two tasks; others might also be involved but were not accessible by non-invasive means (DuBrul, 1988; Lowe, 1981; Luschei and Goldberg, 1981; Narin, 1975). The placement of the EMG electrodes was confirmed by observing the nature of the movements evoked by stimulation of each pair of electrodes (single square pulse, 0.2 ms), by the nature of the recorded muscle activity patterns appropriate to the different functional orofacial movements made by the animal (see Dubner at ul., 1978; Lowe, 1981; Marller. 1966; Wiejnen, Wouters and van Hest, 1984) and, in the case of the chronically implanted EMG electrodes, by autopsy examination of the electrode sites. Recording

und dato analysi.s

Experiments were made over a period of 1 year in both animals in seven recording sessions; 6-8 weeks elapsed between each recording session. Detailed descriptions of methods for data analysis are provided in Murray et ul. (1991). In brief, the following variables were assessed for each animal during the tongue-protrusion and biting tasks. (1) The mean amplitude of the force trace and the mean EMG amplitude under the rectified and smoothed EMG signals during the holding phase, the dynamic phase, and the pre-trial period for each trial; a value expressed in ‘A/D units’ reflecting the digital representation of the amplitude of the rectified and smoothed EMG signal. (2) The mean EMG amplitude ratio for the holding phase, which was defined as the mean EMG amplitude of the rectified and smoothed EMG signal during that phase divided by the mean EMG amplitude of the rectified and smoothed EMG signal during the pre-trial period for each trial. (3) The mean EMG surface area under the rectified and smoothed EMG signal during the

Orofacial

muscle activities

dynamic phase of the task. (4) The mean EMG amplitude ratio for the dynamic phase, which was defined as the mean EMG amplitude of the rectified and smoothed EMG signal during that phase divided by the mean EMG amplitude of the rectified and smoothed EMG signal during the pre-trial period. (5) Time onset of increases in EMG muscle activities (and force) after the appearance of the visual cue on the video screen. An increase in EMG and force signals was defined as one exceeding two standard deviations above the mean background activity level present during the pre-trial period. Statistical analyses involved one-way and two-way ANOVA. Least-square means and least-square differences between the means were used for multiple comparison of means (p < 0.05 was considered significant). A total of 327 successful trials were analysed from both animals for the tongue-protrusion tasks (T,, T,, and T,,), and a total of 210 successful trials were analysed from both animals for the biting tasks. Symmetrical tongue-protrusion and biting tasks at different forces for monkey H6 were analysed from data collected in two separate recording sessions. Session

% 2

957 RESULTS

Features

of the symmetrical

tongue-protrusion

Session B

A m

PTP

m

Holding

phase

Holdmg

*

phase

2 200 %

1 MASS

DIG GG

001

ZYGO

PLAT

DIG

GG

00s

ZYGO MASS 00s PLAT

001

Muscle Session Session

DIG GG

D

*

C

m

Holding

Muscle

m

phase

ZYGO MASS 00s PLAT

001

task

A total of 80 (monkey H6) and 33 (monkey H5) successful trials of the symmetrical tongue-protrusion task performed in four and three recording sessions, respectively, were analysed. Some of these data for monkey H6 were recorded in sessions studying the task at different forces and different directions and so were also used in the subsequent analysis of force and direction data (see below). For monkey H6, the digastric, genioglossus, orbicularis oris superior and inferior muscles (80 trials) showed a significant (p < 0.0001) increase in the mean EMG amplitude during the dynamic and holding phases compared with the pre-trial period (Fig. 1). The mean EMG amplitude ratio was also significantly (p < 0.0001) higher in these muscles than in the other muscles and the highest mean EMG amplitude ratio occurred in the genioglossus and orbicularis oris inferior (p < 0.0001). The patterns were generally consistent between different recording sessions (e.g. Figs 1 and 2) and indeed, for each muscle, there was no significant difference in mean

PTP Holding

phase

001

ZYGO

DIG’ GG

PLAT

90s

Muscle

Fig. 1. The mean (*SD) EMG amplitude during the symmetrical tongue-protrusion task of monkey H6. There were 80 trials in the sessions A, B, C and D. Asterisks indicate statistically significant differences (p < 0.0001) between the mean EMG amplitude (values expressed in ‘A/D units’) during the dynamic and holding phases and the mean EMG amplitude during the pre-trial period (PTP). In this and subsequent figures, muscles are masseter (MASS), genioglossus (GG), digastric (DIG), platysma (PLAT), zygomaticus major (ZYGO), orbicularis oris superior (OOS), and orbicularis oris inferior (001). Note that the mean EMG amplitudes of the DIG, GG, OOS, and 001 were significantly increased during the dynamic and holding phases in all sessions, although, in only one session (D), the PLAT showed a significant increase during those phases.

E. M. MOUSTAFA et al

958

0

Session

B T

[ASS

DIG

ZYGI PLAT 00s

ASS

001

ZYGO PLAT

00s

Muscle

Muscle

rl MASS

DIG GG

ZYGO PLAT 00s

DIG

001

MASS GG

001

ZYGO PLAT

00s

Muscle

Muscle

Fig. 2. The mean (k SD) EMG amplitude ratio during the dynamic and holding phases of the symmetrical tongue-protrusion task of monkey H6. There were 80 trials in the sessions A, B, C and D. Note that in all the recording sessions the highest mean EMG amplitude ratios occurred in the GG and 001.

EMG

amplitude

ratio

between

different

recording

sessions. On the other hand, the masseter. platysma (left), and zygomatic major displayed no significant changes except that the platysma showed a significant (p < 0.0001) increase in mean EMG amplitude during the dynamic and holding phases in one session (Fig. I). The mean onset times of orbicularis oris increases in genioglossus, superior and inferior, activities in monkey H6 were not significantly different from each other, but were significantly (p < 0.0001) earlier than those of the force and increased digastric activity, which were not significantly different from each other (Table I). The EMG patterns recorded from monkey H5 were also consistent between different recording sessions, and showed a significant increase in the mean EMG amplitudes from the digastric, genioglossus, and orbicularis oris inferior during the holding and dynamic phases. The mean EMG amplitude ratio was also significantly higher in these than other muscles, and the highest mean EMG amplitude ratio occurred in the genioglossus. The mean onset times of increases in digastric and genioglossus activities were not significantly different but were significantly shorter than those of the force and inferior orbicularis (Table I).

Three

directions

C$ the tongue-protrusion

task

For the three directions of the tongue-protrusion task at 1.0-N, a total of 120 successful trials (in two recording sessions) by monkey H6 and 70 successful trials (in two recording sessions) by monkey HS were

Table I. The mean onset times (ms) of increased activity and tongue force for the three directions tongue-protrusion task Muscle

I -Force 2-DIG 3-GG 4-00s 5-001

I -Force 2-DIG 3-GG 4-001

Right

side

Svmmetrical

muscle of the

Left side

+ f k + k

Monkey H6 72.0 533.3 f 59.7 489.6 k 74.8 353.9 + 75.3 339.0 * 12.7 303.0 i

63.6 63.8 62.4 85.0 80.4

525.0 496.0 332.5 368.7 350.7

& 71.0 + 86.9 + 61.8 k 84.5 L 88.8

43 I .o * 265.0 & 245.0 f 411.0 f

Monkey H5 54.0 426.9 k 30.6 250.0 k 33.0 246.0 + 72.7 406.5 f

52.3 29.8 31.8 71.4

439.0 272.0 239.0 430.0

* k 2 *

535.3 495.0 323.3 329.0 316.0

49.0 36.9 34.8 75.5

The values represent the mean (*SD) onset latency of increase in the EMG and force signals from the visual cue. DIG, digastric; GG, genioglossus; 00s and 001. orbicularis oris superior and inferior, respectively.

Orofacial

Holding

DIG

phase

ZYGO

MASS GG

muscle activities

PLAT

001 00s

Muscle

s 300r

*

s .Z

-2 E

200

Holding phase

G E w 100

In both monkeys the mean onset times of increases in EMG activity and force were not significantly different between the three directions of the tongueprotrusion task (Table 1). Moreover, the mean force amplitude during the holding phase was not significantly different between the three directions of the tongue-protrusion task for each recording session in both monkeys. Analysis of the dynamic and holding phases for all three directions of the tongueprotrusion task in both monkeys, however, demonstrated a significant (p < 0.01) difference between the left and right tasks in the mean EMG amplitude ratio (e.g. Fig. 4) and mean EMG areas of the genioglossus and inferior orbicularis but not of the other muscles; there was a significant increase in both these variables as the direction of the task changed from left to right. Tongue protrusion at different protrusive fi)rce levels

2 2

959

0 MASS’

DIG GG

ZYGO PLAT

001 00s

Muscle

There was no significant change in the mean EMG amplitude ratio and mean EMG amplitude for any of the muscles during the holding phase of the task when the protrusive force was changed from 0.85 to I.0 to 1.35 N (monkey H6, 110 successful trials). Analysis of the dynamic phase for all muscles during the different forces showed no change in the mean EMG amplitude ratio and mean EMG amplitude for each muscle as the protrusive force was‘changed from 0.85 to 1.O to 1.35 N, but the mean EMG surface area of the genioglossus was only significantly increased when the force was increased (Fig. 5). Features cf the biting task

DIG

ZYGO

MASS GG

PLAT

001 00s

A total of 85 (monkey H6) and 45 (monkey H5) successful trials of the biting task at 20 N in four and three recording sessions, respectively, were analysed.

Muscle Fig. 3. The mean (*SD) EMG amplitude for each muscle during the three directions of the tongue-protrusion task (top, right; middle, symmetrical; bottom, left) in two recording sessions of monkey H6. A total of 120 trials were analysed. Asterisks indicate a statistically significant difference (p < 0.0001) between the mean EMG amplitude (values expressed in ‘A/D units’) during the dynamic and holding phases and the mean EMG amplitude during the pre-trial period (PTP) for the left DIG, GG, 00s and 001. Note that in all three directions the mean EMG amplitudes of the DIG. GG, OOS, and 001 were significantly increased during the holding phase.

In monkey H6, the mean EMG amplitudes (Fig. 3) of the digastric, genioglossus, and orbicularis muscles during the dynamic and holding phases were significantly (p < 0.0001) higher than those of each corresponding muscle during the pre-trial period for all three directions. Moreover, the mean EMG amplitude ratio was significantly (p < 0.0001) higher in those muscles than in the other muscles. The highest mean EMG amplitude ratio occurred in the genioglossus and inferior orbicularis. These patterns were generally consistent between different recording sessions. Similar findings were noted in monkey H5, except that no significant EMG increase in the superior orbicularis oris was noted and the highest mean EMG amplitude ratio occurred in the genioglossus.

*

TT

analysed.

DIG

ZYGO

MASS GG

PLAT

001 00s

Muscle Fig. 4. The mean EMG amplitude ratio (k SD) during the dynamic and holding phases of the three directions of the tongue-protrusion task. Note that there was a significant increase (p < 0.01) in mean EMG amplitude ratio for the GG and 001 as the direction of the task changed from left to right.

E. M. MOUSTAFA et al.

Some of the biting trials for monkey H6 were also used in the analysis of the biting task at different bite forces (see below). For monkey H6, only the masseter, platysma (left), and zygomaticus major muscles showed a significant (p < 0.0001) increase in mean EMG amplitude during the dynamic and holding phases compared with the pre-trial period (Fig. 6). The mean EMG amplitude ratio was also significantly (p < 0.0001) higher in these than other muscles and the masseter showed the highest mean EMG amplitude ratio; this pattern was consistent between different recording sessions and indeed for each muscle there was no significant difference in mean EMG amplitude ratio between different recording sessions (e.g. Fig. 7). The mean onset times of increase in the masseter, zygomaticus, and platysma activities were not significantly different and the mean onset time of increase in the masseter activity lagged behind that of the increase in foice by 10 + 31 ms; this difference was not significant. Similar findings were noted in monkey H5, except that no significant EMG increase occurred in the platysma and the mean EMG amplitudes of the digastric and genioglossus during the dynamic and

rALil_ 1.00N

0.85N

Force

N

I.35

levels

Fig. 5. The mean (+SD) EMG surface area of GG activity at different protrusive forces during the dynamic phase of the force. The data were collected in 120 trials in two recording sessions from monkey H6. Asterisks indicate a significant increase (p < 0.0001) in the mean EMG surface area at forces of 1.OO and I .35 N compared to 0.85 N.

200

300 Sessson

Session

= m

5 150 .Z -& 5 ”

A Holding

phase

m

PTP

m

Holding

phase

5 .=: Td, 200 5

100 :

2 2 E: Q

B

PTP

e 50

IO0

4

0

0 PLAT

GG

MASs

DIG’

‘001’

DIG

GG

00s

Muscle

Muscle

200

‘.

Session

Session C

* m a

PTP Holding

phase

” I50 .=: ii EJ ” 100

iYGd ‘001’ PLAT 00s

D

m

Holding

phase

2 2 e, E

50

0 DIG

MASS ZYGO PLAT GG 00s Muscle

001

DIG GG

MASG iYGd ‘001‘ PLAT 00s Muscle

Fig. 6. The mean (*SD) EMG amplitude during the biting task. There were 85 trials in the sessions A, B, C and D from monkey H6. Asterisks indicate a statistically significant (p < 0.0001) difference between the mean EMG amplitude (values are expressed in A/D units) during the dynamic and holding phases and the mean EMG amplitude during the pre-trial period (PTP). Note that the mean EMG amplitudes of the MASS, PLAT, and ZYGO were significantly increased during the holding phase.

Orofacial

muscle activities 6

Session

DIG

MASS GG

ZYGO PLAT 00s

A

001

DIG GG

Muscle

iYGb PLAT 00s

001'

Muscle

6

0 DIG

ASS GG

ZYGO PLAT 00s

001

DIG GG

Muscle

MASS ZYGO PLAT 00s

001

Muscle

Fig. 7. The mean EMG amplitude ratio (*SD) for the holding phase of the biting task. The data are based on 85 trials in sessions A, B. C and D from monkey H6. Note that the highest mean EMG amplitude ratio occurred in the MASS.

holding phases decreased significantly (p < 0.02). The mean onset time of increase in the masseter activity lagged behind that of the increase in force by 20 f 30 ms. The mean onset times of the increase in force, masseter and zygomatic activities were not significantly different. Biting task at difSerent bite forces A total of 120 successful trials of the biting task at three different levels performed by monkey H6 in two recording sessions were analysed. There was a significant (p < 0.0001) increase in the mean EMG amplitude ratio and mean EMG amplitude for the masseter during the dynamic and holding phases as the bite force was increased from 17 to 23 N (e.g. Fig. 8). There was no significant change in the mean EMG amplitude ratio or mean EMG amplitude of the digastric, genioglossus, inferior orbicularis, and zygomatic muscles, but these variables of the platysma and superior orbicularis significantly (p < 0.0001) decreased as the bite force was increased from 20 to 23 N (e.g. Fig. 8). This pattern was consistent between the two different recording sessions. DISCUSSION

Symmetrical

tongue-protrusion

This was characterised

task

by a significant

increase

in

the EMG activity of the digastric, genioglossus, and orbicularis oris inferior muscles in both monkeys, although there was a difference between the two animals in the use of the inferior orbicularis (the possible explanations of this difference are discussed below). The onset times of the genioglossus and both orbicularis muscles were significantly earlier than that of the digastric. Our finding of an early onset and increased EMG activity for the genioglossus during the trained tongue-protrusion task are consistent with previous descriptions of increased activity in that muscle during tongue protrusion in cats (Hiiemae and Crompton, 1985; Lowe, 1981; Smith and Kier, 1989; Thexton and McGarrick, 1988, 1989) man (Abd-El-Malek, 1955; Hryschyn and Basmajian, 1972; Takada, Yasuda and Hiraki, 1989) and other species including monkeys (Lowe, Gurza and Sessle, 1976; Lowe, 1978, 1981; Smith and Kier, 1989). Our documentation of the association of genioglossus and inferior orbicularis activities during tongue protrusion is consistent with previous reports in man (Lowe and Johnston, 1979; Lowe, 1980; O’Dwyer et al., 1981), but activity of the inferior orbicularis during tongue protrusion does not appear to have previously been reported Although that muscle showed in monkeys. increased activity during the symmetrical tonguethere was evidence that the protrusion task,

E. M.

MOUSTAFA et al.

jaw (Gay and Ringel, 1988).

=

17N

m

20 N

0

23N

MASS

DIG GG

Tongue-protrusion protrusive forces

ZYGO PLAT

001 00s

Muscle Fig 8. The mean EMG amplitude ratio (*SD) for the holding phase of the biting task at different bite forces. The data were derived from 120 trials at bite forces of 17.20 and 23 N. Asterisks indicate a significant increase (p < 0.0001) in the mean EMG amplitude ratio for the MASS and a significant (p < 0.0001) decrease in the mean EMG amphtude ratio for the 00s and PLAT when the bite force was increased.

increased force output recorded from the tongue force transducer during the task was due to the activity of the genioglossus but not the orbicularis muscles. Visual observations as each monkey performed the task and subsequent inspection of the video-tape recordings clearly showed that the monkey’s upper and lower lips were not touching the transducer. Furthermore, the tongue-protrusion task at different protrusive forces was associated with a significant increase in the EMG surface area of the genioglossus during the dynamic phase of the task as the force was increased, but there was no significant change in the EMG surface area in any of the other muscles. The difference in EMG patterns during the tongueprotrusion task between the two monkeys may be explained by the fact that each may have used a distinctly different movement strategy to contact the tongue transducer and successfully perform the task: monkey HS pushed the transducer with the ventral surface of its tongue, whereas monkey H6 pressed the tongue transducer with the tip of its tongue. Variations in muscle patterns between monkeys and between human subjects performing an orofacial motor task have been reported previously (Doty and Bosma, 1956; Dubner et al., 1978; Miller et al., 1985; Miller, 1991; Lindauer et al., 1993) and similar differences may occur between individuals performing other movements involving, for example, the limb (Brooks, Kennedy and Ross, 1983). This might be due to anatomical differences in muscle form and attachment points (Ingervall and Thilander, 1974) or the use of different motor-programming strategies for the production and regulation of movements of the

Piecuch,

task

1986; Moore,

at d$erent

Smith

and

directions

and

The observation that, at increasing levels of force, an increase occurred in the mean EMG surface area under the integrated genioglossus signal during the dynamic but not during the holding phase of the tongue task could be explained by our recording from genioglossus motor units that were recruited only at the lowest forces and that were associated with rapid changes in the force, which occurred during the dynamic phase, but not with any increase in force during the holding phase. We also have evidence that the directional relations observed in the left genioglossus and orbicularis oris inferior muscles as the direction of the tongueprotrusion task changed from left to right were not due to non-specific factors such as changes in the level of motivation or arousal, or differences in performance for one or more directions of the task. Firstly, the sequence of the three directions of that task was randomly selected. Secondly, the mean force amplitude during the holding phase was not significantly different among the three directions of the task. Thirdly, the mean onset times of increase in the force and EMG activities of each muscle were not significantly different among the three directions of the task. These data suggest that the dynamic and kinematic features were in general comparable for the three directions of the tongue-protrusion task and that the significant changes in the mean EMG surface area of the genioglossus and inferior orbicularis as the direction of the task changed were not due to differences in the way in which the monkeys performed the task in the three directions (see also Murray and Sessle, 1992b). Moreover, the significant changes observed in the levels of EMG activities were consistent with changes observed in EMG activities with isometric torque movements about the forelimb (Buchanan et al., 1986) with forelimb reaching movements in different directions (Schwartz, Kettner and Georgopoulos, 1988) and with head movements in different directions (Keshner et al., 1989). In addition, previous studies have suggested that changes in the levels of activity within the extrinsic musculatures on both sides of the tongue would result in changes in the direction of tongue protrusion (Bennett and Hutchinson, 1946; for review see Lowe, 1981). A recent study in our laboratory recorded neurones within the tongue area of the awake monkey’s motor cortex (tongue-MI) that increased their activities in advance of increased genioglossus activity during the tongue-protrusion task but not during the biting task (Murray and Sessle, 1992a, b). Many of these neurones within tongue-MI also exhibited directional sensitivity, i.e. preferential activity depending on the direction of tongue movement (Murray and Sessle, 1992b). It was suggested that these neurones might drive particular elemental components of tongue movements and effect the appropriate change in tongue shape and position during the different directions of the tongue-protrusion task. While the

Orofacial

muscle

highest mean EMG amplitude ratio occurred in the genioglossus, our present data have shown that not only the genioglossus but also the digastric and orbicularis muscles may demonstrate significant changes in EMG activity during the tongue-protrusion task. The genioglossus and inferior orbicularis showed significant changes in activity during both the dynamic and holding phases as the direction of the tongue-protrusion task changed from left to right, but only the genioglossus showed increases in EMG variables as the tongue-protrusion force was increased. These findings suggest that the genioglossus is the principal agonist in the tongue-protrusion task and that other muscles which are active serve a more accessory role. Thus, it is likely that tongue-MI neurones are involved in driving the tongue musculature but it is also possible that they or other neurones (e.g. in the face-MI) might drive other orofacial muscles and thereby bring about the appropriate changes in their activity. Biting task Although the biting task was characterised by increased EMG activity in the masseter and zygomaticus major muscles, there were differences between the two animals in the use of the genioglossus, digastric and left platysma. These differences might have resulted from each monkey using a different motor strategy to successfully perform the task, or from anatomical differences in muscle form and attachment points that have been described previously in monkeys (Grant, 1973) and man (Ingervall and Thilander, 1974). Variations in muscle patterns have also been reported between different individuals performing an orofacial motor task (Doty and Bosma, 1956; Moller, 1966; Dubner et al., 1978; Gay and Piecuch, 1986; Moore et al., 1988) or a limb motor task (Georgopoulos, Kalaska and Massey, 1981; Brooks et al., 1983). Our finding of increased activity of the masseter during the trained biting task are in accord with previous findings that this muscle is primarily concerned with jaw closing and with the application of force during mastication and biting in man (Ahlgren, 1966; Gibbs et al., 1981; Schieppati et al., 1989) and monkeys (Lund and Lamarre, 1974; Hoffman and Luschei, 1980; Byrd and Garthwaite, 1981; Luschei and Goldberg, 1981; Hylander and Johnson, 1985, 1989). That the masseter EMG activity may increase as bite force is increased is also consistent with others’ findings in man (Devlin and Wastell, 1985; Haraldson et al., 1985) and monkeys (Luschei, Garthwaite and Armstrong, 1971; Hoffman and Luschei, 1980; Luschei and Goldberg, 1981) of increased EMG activity of the masseter and temporalis muscles as bite force increases. The increase in EMG activity may be due to recruitment of additional motor units from the masseter and increased firing rates of previously recruited motor units (Goldberg and Derfler, 1977; Clark, Luschei and Hoffman, 1978; Lund et al., 1979). In addition, some neurones in the jaw area of the motor cortex (jawMI) (Hoffman and Luschei, 1980; Murray and Sessle, 1992a) increase their activities in advance of increased EMG activity in the masseter during the biting as

activities

963

distinct from the tongue-protrusion task. These neurones were suggested to be concerned specifically with the control of fine jaw-closing movements. Our data of muscle activity patterns associated with the trained biting tasks are consistent with these recent studies but we also found that other muscles (zygomatic and platysma) as well as the masseter may be active during the biting task. Our finding that the masseter activity did not significantly lag behind the force onset is consistent with that of Luschei et al. (1971) who found no significant lag in the masseter and temporalis activities, which increased at the onset of increased force during a biting task in monkeys. However, a lag between EMG activity and force rise has also been reported for the limb muscles (Inman et al., 1952; Buchanan et al., 1986). In addition, in monkeys (Macaca mulatta) trained to exert steady forces up to 72.5 N on to a force transducer in response to a visual cue, Hoffman and Luschei (1980) found that EMG activity in the masseter and temporalis started lo-30 and 40-90 ms, respectively, before the onset of force rise. The difference between our findings in Macaca fascicularis and those of Hoffman and Luschei might be attributed to a number of factors, such as species difference and variations in the experimental design. It is also likely that the temporalis and the medial pterygoids, which we did not record, would increase their activities during the biting task and may indeed lead the masseter; there is published evidence to suggest that this is the case (see Luschei and Goldberg, 1981). To the best of our knowledge this study is the first to report the activity of the platysma and zygomaticus major muscles during biting in a well-controlled task. The platysma is active in the last phase of voluntary jaw-opening in man (De Sousa, 1964; Widmalm et al., 1985) and is a possible synergist of other jaw-opening muscles (Quincy and Warfel, 1967; Widmalm et al., 1985). It is unlikely that its activity as recorded in our study might be due to recordings from the masseter, because the placements of all the acute and chronic EMG electrodes were confirmed by several approaches (see Methods). Our observation of activity of the zygomaticus major during the biting task is consistent with a previous report in man by O’Dwyer et al. (1981). The platysma and zygomaticus major influence facial expression by pulling the corner of the mouth down and sideways (DuBrul, 1988) and it is quite possible that these two muscles were active in our study because of the manner in which the animal performed the task or because the muscles were contributing to an increase in force. We favour the former explanation in view of our direct visual observations of how each animal performed; when the animal was biting on the transducer, it pulled its cheek and the corner of the mouth upward and laterally away from the transducer. Previous anatomical studies by Narin (1975) and DuBrul (1988) have indicated that this movement would involve the zygomaticus major. It is further unlikely that the platysma or zygomaticus muscles support the masseter or other jaw-closing muscles to generate force during biting, because at higher bite forces, they showed no change in EMG activity whereas an increase occurred in masseter activity. Thus, of the

964

E. M. Mot

muscles recorded, the masseter is the primary agonist in the biting task whereas the other muscles that are active appear

may be considered accessory and to contribute to force recruitment.

do

not

Acknowledgements-We gratefully acknowledge the technical assistance of K. MacLeod and S. Carter, the photographic and art services of R. Batter, S. Burany, and M.-A. Williams, and the secretarial assistance of D. Tsang and F. Yuen. The study was supported by Medical Research Council of Canada Grant MT-4918 to B.J.S.

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