Electromyographic Heterogeneity in the Human Masseter Muscle N.G. BLANKSMA, T.M.G.J. VAN EIJDEN, and W.A. WEIJS Academic Center for Dentistry Amsterdam (ACTA), Department of Functional Anatomy, Meibergdreef 15, 1105 AZ Amsterdam, The Netherlands The complex, pennate architecture of the human masseter muscle points to a functional division into more than the commonly distinguished deep and superficial parts. In this study, the possible existence of regional differences in activation was examined. EMG activity was registered in three deep and three superficial regions with the use of bipolar fine-wire electrodes. Recordings were made during different static bite tasks, in specified directions, and with a specifiedbite-force magnitude. Alinearbite-force/EMGrelationship was observed. Furthermore, it appeared that muscle regions showed a different pattern of change in activity as a function of biteforce direction. Heterogeneity was nearly absent in anteriorly-, anteriomedially-, and medially-directed bites, but became increasingly obvious in the other bite-force directions. The posterior deep region showed the most aberrant activation pattern, which was almost opposite that from the other regions. This part was fully active in posterolaterally-directed bites. The posterior superficial region showed the largest variability in activity as a function ofbiteforce direction. The results point to a functional partition of the masseter muscle in at least three parts: anterior deep, posterior deep, and superficial. A further subdivision of the superficial portion might be present, but was not as obvious as the division of the deep masseter. J Dent Res 71(1):47-52, January, 1992

Introduction. The human masseter muscle has a complex pennate architecture; it consists of several separate portions with different fiber directions (e.g., Ebert, 1938/39; Schumacher, 1961). This points to functional differences within the muscle. Despite this, the masseter has often been considered as a functionally homogeneous muscle (Munro and Griffin, 1970; Vitti and Basmajian, 1977; Van Eijden, 1990). Other workers have identified deep and superficial parts (e.g., Belser and Hannam, 1986; Wood, 1987) and, indeed, have demonstrated a different activation according to task. However, there is increasing evidence that a functional partition into more than two parts might be possible. Eriksson and Thornell (1983) have distinguished five different masseter portions, each with its own unique histochemical and morphological muscle fiber characteristics. Van Eijden and Raadsheer (1992) demonstrated heterogeneity in fiber and sarcomere lengths within the muscle. Other studies have already indicated that a motoneuron pool of a particular muscle is not always activated homogeneously. A motoneuron pool may consist ofsubpopulations ofmotoneurons that can be activated independently to perform different tasks (ter Haar Romeny et al., 1982; Hoffer et al., 1987). Likewise, a finer functional partitioning ofthe masseter muscle into more than superficial and deep parts seems a real possibility. A functional partition became obvious in the human temporalis muscle after subjects were instructedto bite isometrically in different directions (Blanksma and Van Eijden, 1990). In the present study, the aim was to examine the possible existence of regional differences in activation in the masseter muscle while standardized bite-force tasks were being executed. Received for publication April 30, 1991 Accepted for publication August 21, 1991

Materials and methods. Subjects. -The right masseter muscle was investigated in five male subjects, ranging in age from 28 to 40 years. They had a normal intermaxillary relationship and no signs offunctional disturbances or diseases of the masticatory system. One of the subjects was missing a lower left premolar. The experiment was approved by the ethical committee of the Academic Medical Centre. EMG-registration. -The EMG activity in different regions ofthe right (working side) masseter muscle was registered by means ofsix bipolar fine-wire electrodes. Each electrode consisted oftwo Tefloninsulated stainless-steel wires (diameter, 0.12 mm) with bared tips (1mm), bent into a hook (Basmajian and Stecko, 1962); the distance between the two bare ends was about 2 mm. The electrodes were inserted by means of a 0.6 x 25 mm disposable hypodermic needle. The positions of the condyle, the mandibular angle, and the anterior border of the muscle were determined by palpation. Three electrodes were inserted into the deep masseter at equal distances (17 mm deep) from the condyle, the anterior border, and each other. These electrodes were at a distance of 1 cm below the zygomatic arch (region 1 is the posteriormost, region 3 the anteriormost region). Three other electrodes were inserted at equal distances from the mandibule, the muscle's anterior border, and each other, 12 mm deep into the superficial part of the masseter. They were at a distance of 2 cm above the lower margin of the mandible (region 4 is the posteriormost, region 6 the anteriormost region). Available computer-tomography scans of these subjects, which had been used in a previous study (Weijs and Hillen, 1986), showed that insertion at depths of 12 and 17 mm always reaches the superficial and the deep parts of the masseter muscle, respectively. In no case did the needle come into contact with the bone. Bite-force registration.-A feedback procedure was used, which enabled a subject to exert bite forces in certain specified directions, with a specified force, during static contraction of his jaw muscles. Thisprocedurehasbeendescribedpreviously(VanEijdenetal., 1988). In short, a three-component piezo-electric force transducer (Kistler, dimensions 24 x 24 x 10 mm, x w x h), positioned between a pair of occlusal clutches, was used to register and visualize both the direction and magnitude of bite force. The plane of these clutches will be called the "occlusal plane". The center ofthe transducer was fixed at the center of the second right premolar; the interincisal distance was 18 ± 5 mm (mean ± SD of the subjects). The following artesian coordinate system with its origin in the tranducer was defined: x-axis, anteroposterior, parallel to the occlusal plane; yaxis, mediolateral, parallel to the occlusal plane; and z-axis, perpendicular to the occlusal plane. The visualization enabled the subject to keep the bite force constant in the desired direction. The direction ofthe resultantforce was defined relative to the z-axis, i.e., the axis perpendicular to the occlusal plane, and to the anteroposterior x-axis.

Measurements.-All subjects participated in two experiments, each ofwhich was performed during a separate session; between the two sessions was a time period of about 12 weeks. The electrodes were not removed during a session. In experiment A, bite forces of 50, 150, 250, and 350 N and maximal voluntary force were exerted in five bite-force directions: vertical (z angle 00; x angle undefined), anterior (200, 00), lateral (200, 900), posterior (200, 1800), and medial (200, 2700). Each

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48

anterior direction

10

t3,2 5,6

90 80

1194

70 60tw 'u

-

10090807060

January 1992

posterior direction

I

2 3

up50

50

5040 3020-

@ 40-

10 0

I

I

0 50

150

I

9

550

medial direction

104

6

20-

5

10-

4

0 Ii I 0 50

I.

v

250 350 450 bite force (N)

30-

100

9(

I

I

150

II

1

250 350 bite force (N)

450

550

lateral direction

90 80 ,594 1 70 - 60c 50-

6,3 12

I-I

bs

0

_--I

0 50

150

250 350 bite force (N)

450

550

1

2,3 6 5

40 3020100O i 0 50

.4

II

150

II-

250 350 bite force (N)

450

550

Fig. 1-Mean EMG activity of the subjects for all muscle regions as a function ofbite-force magnitude for four bite-force directions. EMG measurements +, region two; *, region three; A, region four; X, region five; and V, region six.

at 50, 150, 250, and 350 N, and maximal voluntary force. *, region one;

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FNEIFYIN THE MASSE7ER MUSCLE 761.ol71EVo 71 No.

49

Additional,vin done with a bite-rce m4agn1direction two extra trials tude of 150 N so tha variability between the two sessions could be

measurement was repeated once for each subject. each

were

tested.

In experiment B, a constant bite-foc magnitude (150 N was exeted in nine directions: the five bite-fbfre directions as defined in experiment A plus four intermediate directions, namely, anterolateral (20', 451), posterolateral (20', 135) posteromedial (20 , 225 ), and anteromedial (20', 315'). This magnitude was chosen because all subjects could easily exert 150 N in the nine directions. The sequence of performance of the nine bites was chosen randomly. Each biteforce measurement was performed six times for each subject, and each time another rardomized order of the nine bite-force directions was determined. So that fatigue effects would be avoided in both expe iments rest periods vith lenghs adjusted to the bitefrce magnitude, were nseted between the bites, as follows two min of rest afer a bite N there min after 250 N four in after 350 N d, ad orce of 50 ,

r

fve min after a maimal voluntaryfoce

The

duratn

of a

sigle

bite never exceeded 30 s. A4iass re n EM signals T-e threeforeesignls (one eah ore component) ard the six muscle-region EMG signals were pre-amplped (from 200 to 10000 b differ ertial amplifiers arnd siultaneousl recorded on FM analogue tape (speed 19 cV). Thebandwidth for the EMG signals was from 30 to 1000 Hz. The analogue data were digitized (2400 samples channel) b a DEC 11/ x

nicomputer

system

stored

digital

Fig ARaw EMG signs ix muscle regions, during biting with Tagnitude in four directions in a single session of subject E. The oi

the

sa me

r ded with Siemens Oscillomink inkjet writer. Vertical signals calibration bars represent 150 pV Horizontal calibration ba represents 50 were

a

M.

bite-

tape

fore registration, a coituous interval of 05 s was selected automatically The selected period was the one where ftc direction of te resultat force was within 5 of the specified bite-fore diton, and the mean, squared difference between th exerted and desired ce levels was the smallest o pose 05second periods generally his difference was smaller than 5 N). In trials in which maxvial bite forces exerted, the 0a5-second period ith the largest bite force was chosen. The EMG activity of the muscl during this period was quanrtifed asthe mean value of the rectified signal. In experiment A, t two avalable VMG measurements fr each bit-force direction and magnitude were first averaged Ther, for each subec and muscle region, all values expressed as actions of ie maximal value bund during the session. These values were normlly observed when the subjects were instructed to produce naxima volruntary fore. The difference between tIe two measuremens was used as a measure of variability between the a

,

were

ea

x

medial

lateral

reon

were

bite-fore levels. In experiment B, he mean SD EMG was calculated for each subject muscle region, and bite-force direction over the six trials,

and this mea was scaled to the maximum value oundper muscle region and subject during this session The scaled values vere entered into an analysis of variance to test for influence of bite-fore

posterior Fg .34lar plot ofthe mn EMGsof he subjects Scaled EMG activity is in the radial direction (ring represents 100% activity) and the direction of the hi force is in the angWar direction. The bite-fbore magnitude is 150 N. Curves of the six muscle regions are depicted

direction and muscle region on EMG activity. As a test for variability between measurements taken in two different sessions the flowing comparisons were made: In ex

four non-vertical bite-force directions, this EMG relationship is shown in Fig 1. This way, the levels of EMG activity of the six muscle regions for contrasting bite-fore directions can be corn peniment A, for each s e muscle region, and bite redirection, done at pared. All muscle regions appeared to be active in all bite-force the mean SD was calculated over the four trials that directions investigated, including the vertical one (not shown). For a bite-force level of 150 N These values were scaled to the maximum all muscle regions, the bite-force/EMG relationship was about value found per muscle region, per subject, and averaged over the subjects. Similarly the mean values of experiment B were scaled linear. The masseter regions showed nearly uniform behavior wen the subjects, but with only the the bite-force direction was vertical, medial, or anterior; however, in again, and also averaged five bite-force directions that also studied in experiment A lateral and posterior directions, theirbehaviorwas clearly different. taken into account. The mean scaled values of experiment A and B Apparently, in these directions the muscle was activated heteroge were

over

now

were

were

compared by means of a Student t test.

neously.

For a tair comparison between muscle regions, the EMG values to be normalized. However to give an impression of signal had Results. magnitudes, the minimum and maximum EMG values for each Experiment A.fThe relationship between bite force and EMO muscle region are shown, for one subject, in Table 1. The difference between the EMG activity in the first and that in activity was investigated for different bite-force directions For the Downloaded from jdr.sagepub.com at MCMASTER UNIV LIBRARY on March 20, 2015 For personal use only. No other uses without permission.

50

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TABLE 1 SUBJECT E: RANGE IN MICROVOLTS OF THE EMGs RECORDED AT EACH MUSCLE REGION

Region

1

2

3

4

5

6

Minimum

2.45

7.51

3.10

2.18

2.18

11.98

Maximum

112.31

67.06

45.41

209.13

234.25

231.59

the second measurement was expressed as a percentage of the mean EMG ofthese two measurements. This difference was dependent on the bite-force level. As the bite-force level increased, the difference decreased (Table 2). The differences between subjects were examined by comparison of standard deviations ofthe normalized EMG values averaged over the five subjects. In Table 3, this variability is shown for the vertical direction, which can be considered to be representative ofthe other directions investigated. Experiment B.-The bite-force direction/EMG relationship was examined at a constant bite-force magnitude of 150 N. An analysis of variance of the scaled EMG activities demonstrated that the EMG activity was significantly different for different bite-force directions (p < 0.05), but not for different muscle regions (p > 0.05). However, a significant interaction between region and bite-force direction (p < 0.05) was present. Region 1 (posterior, deep) showed by far the most deviation from the rest of the muscle. An analysis of variance of the data from regions 2-5 still showed a significant interaction (p < 0.05). This implies that muscle regions did not react in the same way to a change in bite-force direction. Fig. 2 illustrates how the relative change in EMG activity was not the same for all muscle regions. Fig. 3 shows the mean scaled EMG activity over the five subjects for each muscle region and bite-force direction; it demonstrates that the masseter muscle was activated heterogeneously. This heterogeneity was nearly absent in anteriorly-, anteromedially-, and medially-directed bites, but became obvious in the other bite-force directions. Maximum regional differences were found at posterolateral bites. Region 1 (posterior, deep masseter) differed remarkably from the other regions in two ways, namely, (1) it had its highest EMG activity during posterolateral bites, and (2) it had its lowest activities in opposing bite-force directions. The activity patterns of the other deep regions (regions 2 and 3) were very similar to each other, but differed from the patterns of region 1 and the superficial regions. Their highest EMG activity was present at anteriorly- and anteromedially-directed bites, and their lowest activities were in the opposite directions. Hence, from the deep regions, the posteriormost one demonstrated the most deviating behavior. From the superficial regions, again, the posteriormost one (region 4) showed the most aberrant activity pattern, although less strikingly. All superficial regions (regions 4-6) were activated in roughly the same way during anteriorly-, anteromedially, and medially-directed bites. In the other directions, the activity increased, going from the posterior (region 4) to the anterior (region 6) portion of the muscle. The posteriormost superficial region demonstrated a greater difference in EMG activity beTABLE 2 PERCENTAGE OF VARIATION [(x1 x2)/x * 100%) OF THE TWO REPEATED MEASUREMENTS AVERAGED OVER THE BITEFORCE DIRECTIONS, MUSCLE REGIONS, AND SUBJECTS -

Bite-force magnitude

50 N

150 N

250 N

350 N

Percentage of variation

41.7%

34.8%

33.0%

27.1%

tween bite-force directions than did the anteriormost region. This

that region 1 (posterior, deep masseter) and region 4 (posterior, superficial masseter) demonstrated the most contrasting behavior. The repeatability ofthe measurements within experiment B was calculated by expression ofthe SD as a percentage ofthe mean EMG activity. The standard error was not systematically different for different subjects, bite-force directions, and muscle regions; the pooled SD was 21.2%. The high SD could be due to either variations in the bite-force level and direction actually produced, or variations in neural control, and/or to movements of electrodes between recordings in the same session. The inter-session variability of measurements was also tested. A Student t test comparing the mean values over all subjects in the two sessions showed that there were no statistically significant differences between the two sessions (p > 0.05). However, when the scaled values per subject were compared, some major differences were observed. In one subject, a large inter-session variation was observed for four muscle regions in all bite-force directions. The other subjects demonstrated their inter-session differences mainly in one, but not the same, muscle region. This implies that changing electrodes in our experiments did introduce an additional source of error, which was probably due to variations in electrode placement. The difference between the percentage of variation found in experiment A at 150 N and the percentage found in experiment B can be explained by the different method used. In experiment A, the absolute difference, rather than the SD, of the two measurements was given, because only two trials were done, and the difference was expressed as a percentage of the mean. This percentage must be multiplied by 1/242 to be a measure ofthe standard deviation. The adjusted percentage of experiment A (23.3%) almost equaled the percentage found in experiment B (21.2%). means

Discussion. A functional partition of the masseter muscle into more than a superficial and a deep part has been demonstrated in this study. The posteriormost deep region (region 1) demonstrated an almost opposite activity pattern from the other parts. The other deep regions (regions 2 and 3) showed a similar pattern, deviating from the superficial parts. Furthermore, in the superficial portion, a difference between the posteriormost and anteriormost regions has been observed. This points to a partition ofthe muscle into at least three functionally different parts: posterior deep, anterior deep, and superficial. A further division of the superficial part might be present, but was less conspicuous than the subdivision of the deep part. Anatomical studies have already distinguished more than two separate portions (Schumacher, 1961; Baron and Debussy, 1979), but never came to an uniform division ofthe muscle. Eriksson and Thomnell (1983) studied the histochemical and morphological musclefiber characteristics and divided the masseter muscle into five separate parts. EMG studies have demonstrated a functional difference between deep and superficial parts. Our study confirms the results of Greenfield and Wyke (1956), who used surface electrodes and found a greater activity in the superior posterior region when voluntary jaw retrusion tasks were performed on the ipsilateral

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Vol. 71 No. 1

HETEROGENEITY IN THE MASSETER MUSCLE

51

TABLE 3 EMG ACTIVITY [MEAN + SD (n = 5) OF THE NORMALIZED VALUES] OF THE SIX MUSCLE REGIONS FOR BITES IN THE VERTICAL DIRECTION WITH DIFFERENT BITE-FORCE MAGNITUDES (MEAN MAXIMUM FORCE, 608 N) 1

2

3

4

5

6

50N

0.07 ± 0.06

0.09 ± 0.07

0.11 ± 0.09

0.09 ± 0.10

0.11 ± 0.07

0.10 ± 0.09

150 N

0.17 ± 0.08

0.22 ± 0.14

0.31± 0.15

0.22 ± 0.16

0. 26± 0.10

0.29 ± 0.14

250N

0.29 ± 0.11

0.36 ± 0.18

0.46 ± 0.11

0.36 ± 0.19

0.42 ± 0.10

0.45 ± 0.12

350 N

0.43 ± 0.13

0.45 ± 0.16

0. 60± 0.13

0.47 ± 0.22

0. 57 ± 0.15

0.58 ± 0.14

Max.

0.93 ± 0.09

0.93 ± 0.06

0. 95 ± 0.06

0.84 ± 0.18

0.94 ± 0.12

0.94 ± 0.09

side. Belser and Hannam (1986) compared the superficial and posterior deep masseters. They showed that measurements with intramuscular fine-wire electrodes did not significantly differ from measurements made with bipolar surface electrodes (p > 0.01), and therefore used surface electrodes, which are non-invasive. They found the same result for the posterior deep part at retrusive and ipsilateral positions. They also demonstrated that the superficial masseter was more active in an incisal bite position, and that both parts were equally active when the bite was performed contralaterally. These findings correspond with our results, but, as mentioned above, we have indications for a finer partition of the masseter muscle. Furthermore, when the results are compared, it should be noticed that in our experiments it was possible to define the bite-force magnitude and direction exactly, but that only static bites in one jaw position were carried out. Our experiments were performed with a rather large amount of vertical separation between the occlusal planes, and it is unclear whether the same pattern of compartmental organization would be observed for a more closed position of the mandible. Furthermore, only relatively high forces have been studied, and different results might be found in a study ofthe lower (from 0 to 50-N) range. In this range, the variation might be very large, since it was shown that a decreasing bite-force level goes together with an increasing percentage of variation. A possible explanation for this finding might be that when bite-force magnitude increases, the number of different neural strategies possible for the task to be performed decreases. The observed heterogeneity points to a partitioning of the excitatory command to the motoneuron pool of the muscle, a conclusion which is in agreement with results of studies of motor unit recruitment. For example, Hoffer et al. (1987) demonstrated a similar task-dependent specialization of motor units in the cat. Herring et al. (1989) showed, in the pig masseter, a highly compartmentalized neural organization in which motor unit territories were confined to muscle fascicles. This certainly makes possible a very fine functional subdivision of this muscle. Furthermore, a functional heterogeneity has been observed in the human temporal muscle (Blanksma and Van Eijden, 1990); we demonstrated that, in an anteroposterior direction along the muscle belly, there was an increasing ability of the central nervous system to activate motor units selectively. In this study, such a pattern was observed only in the superficial part, where differences in activity for different bite tasks were generally the smallest in the anteriormost region, and largest in the posteriormost one. An aberrant activity pattern of the posterior deep part of the masseter has earlier been described for the pig (Herring and Wineski, 1986) and for the rabbit (Weijs and Dantuma, 1981; Weijs et al., 1989). It is interesting to note that in the rabbit the motoneurons of this portion of the muscle are localized separately from those of the rest ofthe muscle and are mixed with those of the temporalis muscle in the trigeminal motor nucleus (Mizuno et al.,

1980). The observed activation pattern in man is indeed reminiscent of that of the temporalis muscle (Blanksma and Van Eijden, 1990). The unique behavioral pattern of this part can probably be

explained by its considerable difference in fiber direction compared with the rest of the masseter. With respect to the Frankfort horizontal plane, the fibers of the posterior deep part run almost vertically downward, in contrast to the remainder of the muscle, whose fibers are directed roughly downward and posteriorly. Olthof (1986, unpublished results) found, in a cadaver study, a difference of 170 between the mean fiber angulation ofthe deep and that ofthe superficial part. An important function of such a complex architecture is that selective activation of certain fiber groups makes the muscle produce forces in different directions. This makes possible the performance of various tasks. Eriksson and Thornell (1983) did not find a striking difference between fiber composition in posterior deep and that in other parts. However, they demonstrated in all parts, except for the posterior superficial one, a predominance of type I fibers. This suggests that the posterior superficial region (region 4) is less suited to the performance of continuous activity than are the other regions. If it is assumed that muscle regions which show great activity in only a few directions will also generally be active for shorter periods, their results correspond with ours. For all muscle regions, the bite-force/EMG relationship was almost linear. This suggests that an increase offorce is achieved by a parallel increase of the EMG of all muscle regions. Such linear behavior has been described earlier for regions within the temporal muscle (Blanksma and Van Eijden, 1990), but also for different masticatory muscles sampled by surface electrodes (Van Eijden et al., 1990). Hence, these results mean that for a given bite-force direction, the system chooses a single pattern of muscle activation.

Acknowledgments. We are grateful to P. Brugman for his technical assistance, to C. Hersbach for the artwork, and to H. Rolleman-ter Heurne for assistance in the preparation of the manuscript. REFERENCES

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