Arch oral Biol. Vol. 36, No. 6, pp. 435-441, 1991 Printed in Great Britain. All rights reserved
0003-9969/91 83.00 + 0.00
Copyright 0 1991Pergamon Press plc
MOTOR-UNIT TERRITORY IN THE HUMAN MASSETER MUSCLE A. S. MCMILLANI and A. G. HANNAM’ ‘Department of Clinical Dental Sciences and 2Department of Oral Biology, Faculty of Dentistry, The University of British Columbia, Vancouver, B.C., Canada V6T 127 (Accepted 9 January 1991)
Sammary-Motor-unit territories in human masseter are reportedly focal and related to putative subvolumes of muscle. However, in the absence of a reliable method of locating needle-electrode recording sites within the muscle in three dimensions and due to inherent weaknesses in electromyographic recording techniques, the limits of motor-unit territory in the masseter may have been underestimated. Single motor-unit responses were recorded as time-locked events from 32 paired-needle recording sites throughout the masseter muscles of three subjects. Recording sites were located stereotactically with an optical system, magnetic resonance imaging, and a common reference, then displayed graphically in three dimensions. The mean linear separation of the paired recording sites was 8.8 f 3.4 mm. The putative territories had a preferred orientation in the antero-posterior axis. Motor-unit territories were larger than described previously and appeared to be related to anatomical compartments. The restriction of these territories to discrete regions of the muscle provides an anatomical substrate for selective regional motor control of the human masseter muscle. Key words: motor-unit, electromyography,
masseter muscle, stereotaxy.
INTRODUCIION
There is ample evidence that the fibres of many motor units are scattered throughout substantial areas of the limb and trunk muscles, for example 20% of the muscle volume in the case of the rat soleus muscle and 14% in the cat medial gastrocnemius muscle (e.g. Burke, 1981; Burke and Tsaitis, 1973; Edstrom and Kugelberg, 1968; Stalberg et al., 1976). There are, however, some limb and jaw muscles that appear outwardly to be single structures whereas internally they incorporate a number of putative subvolumes (English and Letbetter, 1982; Herring, Wineski and Anapol, 1989; Letbetter, 1974; Richmond, MacGillis and Scott, 1985). In these cases, motor-unit territories seem to be confined within functional or anatomical ‘compartments’, or both. These findings have raised speculation about the nature of motor control in a compartmentalized muscle because the presence of localized motor-unit territories could conceivably permit differential motor control of separate regions of the muscle (Belser and Hannam, 1986; Herring et al., 1989; Herring, Grimm and Grimm, 1979; English, 1985; Stalberg and Eriksson, 1987). Evidence in support of the focal distribution of motor units may be inferred from descriptions of differential activity in distinct regions of anatomically complex muscles such as the jaw elevator muscles during the performance of routine functional tasks (Herring et al., 1979, 1989; Herring and Wineski, 1986; Weijs and Dantuma, 1981). Although motor-unit territories have been investigated quite extensively in animal muscles (reviewed by Buchthal and Schmalbruch, 1980; Burke, 1981) there is a dearth of information on them in human muscles, and the jaw muscles in particular. The
distribution of motor-units within the human masseter muscle is reputed to be focal, approx. 3-5 mm dia, more akin to the territories of animal jaw muscles than those found in human limb and trunk muscles, and the distribution is considered to be related to internal muscle compartments (Buchthal and Schmalbruch, 1980; Herring et al., 1979, 1989; Stalberg and Eriksson, 1987). It is, however, likely that motor-unit territories in human masseter have been underestimated because of inherent weaknesses in the indirect experimental techniques used previously (McMillan and Hannam, 1989a, b). We suggested recently that uniaxial cross-sectional scanning may be an inappropriate method by which to determine motor-unit territory in a multipinnate muscle such as the human masseter because the complex interdigitation of the constituent muscle fibres may preclude sampling from all fibres of the single motor unit. We proposed a more appropriate experimental approach in which single motorunit activity is sampled in several regions of the masseter muscle simultaneously, provided the recording sites can be located stereotactically in three dimensions of space (McMillan and Hannam, 1989a). A sensitive method of stereotactically locating needle electrode recording sites within the human masseter muscle has been developed (McMillan and Hannam, 1989a). The availability of this technique prompted us to map motor-unit territory in the masseter using multiple electrodes in known regions of the muscle. We considered that a more complete understanding of this motor-unit distribution would provide insight into the functional compartmentalization of this complex muscle, and that of jaw elevator muscles in general. 435
436
A. S. MCMILLAN MATERIALS
AND METHODS
Single motor -unit recordings Mapping technique. Single motor-unit electromyographic experiments were carried out on two male and one female subjects aged 31-36 yr. Each subject had a complete natural dentition and no history of jaw dysfunction. The subjects were selected because of their skill in activation of single motor-units, which is an advantage in this type of experiment. The experiment was approved by the Human Experimentation Committee at the University of British Columbia, and each subject gave informed consent. Two Teflon-covered monopolar needle electrodes (MF-37, TECA, Pleasantville, NY) were inserted into the right masseter muscle, and their position was stabilized with a light metal platform. Reference electrodes were attached to the skin over the muscle. At the beginning of each recording session, the needles were normally situated approx. 15-20 mm apart (as measured on the skin surface). Single motor-unit activity was amplified (Model AL 2010, Axon Instruments Inc., Burlingame, CA) and bandpass-filtered (l-10 kHz). Units were activated by strategies that allowed continuous firing at a low frequency (approx. 10-12 Hz) with the aid of auditory and visual feedback. When a clearly defined compound action potential was obtained from a group of single motor-unit fibres located at one of the needle tips it was used to trigger a digital oscilloscope sweep (Model 2221, Tektronix Canada Inc., Vancouver, B.C.). Any synchronous activity recorded from the second needle was displayed on the second channel of the oscilloscope as a time-locked event, and therefore was considered to originate from the same single motor-unit. If no synchronous activity was recorded, the second needle was repositioned progressively closer to the triggering site until a synchronous compound action potential was recorded. At each location the needle electrodes were moved in and out of the muscle along the conventional trajectory used in uniaxial cross-sectional scanning until compound action potentials of maximum amplitude were obtained at both recording sites. The single motor-unit responses from the two recording sites were sampled and averaged, then plotted (Model HClOOO, Tektronix Canada Inc., Vancouver, B.C.). In order to probe different parts of the muscle adequately, each muscle was divided into eight arbitrary regions. The muscle was first divided into major superficial and deep parts, which in turn were subdivided into quadrants. Paired single motor-unit recordings were obtained in each of these regions for a total of 32 units. Recording selectivity of the electromyographic technique. The increase in selectivity of electromyographic
recordings achieved by highpass-filtering has been described previously (Gath and Stalberg, 1976; Stalberg and Trontelj, 1979), and is a useful technique when selective preservation of high-frequency components of a signal is desired. The higher spatial resolution achieved by this method is advantageous in territorial mapping of single motor-units when multiple needles are used simultaneously because it minimizes the possibility of recording from the same group of fibres.
and A. G.
HANNAM
As a precursor to the mapping experiments, the selectivity of the monopolar electrode achieved by filtering the low-frequency components from the amplified signal was investigated in four masseter motor units of two normal male subjects aged 34 yr. A small adhesive scale, graduated in mms, was attached to the Teflon coating of the needle. The needle was inserted percutaneously at right angles to the skin surface and supported by a metal framework, so that the scale on the grid could be visualized relative to the metal framework. The amplifier bandpass-filters were adjusted to eliminate signal frequency components beyond the range l-10 kHz throughout the recording session. The needle was moved within the muscle until a compound action potential from a single motor-unit was observed on a digital oscilloscope screen during the performance of a gentle tooth-clenching task. While the single motor-unit fired continuously, the needle was moved manually along its medio-lateral trajectory until a compound action potential of maximum amplitude was obtained, i.e. the needle tip was closest to the single motor-unit. It was considered too cumbersome to use a micromanipulator to move the needle in the muscle cross-section (Stalberg and Eriksson, 1987), because the needle was repeatedly inserted and retracted in order to locate a compound action potential of maximum amplitude. The compound action potential was used to trigger the oscilloscope sweep, and an averaged potential for the single unit was recorded and plotted. The needle was moved along a medio-lateral trajectory, first deep, then superficial to the primary recording site, in mm increments. These were verified by means of the graduated scale on the needle which was referenced to the supporting metal framework. Averaged compound action potentials from the single motor-unit were obtained at positions +2, + 1, - 1, -2 mm relative to the primary recording site (Fig. 1). The amplitude of each compound action potential from a single motor-unit was measured at the primary recording site and at the different needle positions. There was a significant reduction in this amplitude as the needle was moved further from the site of the single motor-unit fibre group within the muscle, viz. a 5585% decrease in the signal amplitude at a distance of 2 mm. Voltage ratios (dB) were calculated at each needle position relative to the primary recording site. The mean voltage ratios of the single motor units at needle positions +2, + 1, - 1, -2 mm relative to the primary recording sites were 8.6 f 3.0, 3.1 f 1.0, 3.4 + 0.4 and 9.9 f 3.6dB, respectively. Based on these findings, the volume of pick-up of the monopolar electrode was estimated to be approx. +2 mm, when an amplifier bandwidth of l-10 kHz was used. This is comparable with the value for monopolar needles reported by Stalberg (1980). An amplifier bandwidth of l-10 kHz was therefore employed in the present territorial mapping experiments. Stereotactic location of electrode recording sites
At the end of each paired-needle recording session, a customized reference grid (which incorporated four copper sulphate-filled glass tubes aligned to form a
Motor-unit territory in the masseter
437 5ms
1
, -2
0.2mV
, -1
0
+l
+2(mm)
Fig. 1. Changes in a single masseter motor-unit electromyographic signal according to the position of the electrode recording tip. Changes in waveform shape of an averaged (n = 16),single motor unit, compound action potential as the needle tip is moved f 2 mm along a media-lateral axis from the location of the signal of maximum amplitude. square) was placed between the teeth of the subject (see Fig. 2). The four point angles of the grid (which defined a reference plane), and two known points on each needle were digitized three-dimensionally in situ, by means of a Reflex Metrograph (HF Ross, Salisbury, Wilts., England), and the data were stored digitally for off-line analysis. Because the length of each needle was known, the position of the needle tips relative to the Metrograph-based reference plane could be calculated.
Before the first recording session, the pertinent oro-facial structures of each of the three subjects were imaged by magnetic resonance, with the reference grid in situ. This was carried out with a Picker Vista MRl 100 system, using a 0.15T magnet. Spin-echo sequences with a fixed repetition time (TR:833 ms) and echo time (TE:60 ms) were used to obtain a series of 16 contiguous, 5 mm sections in the axial plane (Fig. 2). The copper sulphate incorporated in the glass tubes of the reference grid appeared as ovoid
Fig. 2. Relationship of the reference grid to oro-facial landmarks and the magnetic resonance plane of section. The reference grid comprises four glass tubes in the form of a square, with four point angles. The position of the grid relative to the right masseter muscle and a needle electrode within the muscle is shown on the right. On the left, the relationship of 16 contiguous axial magnetic-resonance sections to the right masseter muscle, the right articular condyle, the teeth and the grid are depicted. AOB X,&-s
A. S. MCMILLAN and A. G. HANNAM
438
markers (ellipses) in contiguous magnetic resonance sections. From each axial section, the outlines of the right masseter muscle, the right articular condyle, the right maxillary canine tooth, and the centroid of each copper sulphate marker were digitized by means of a digitizer and computer (Models HP9874 and HP350, Hewlett Packard Canada, Vancouver, B.C.). The digitized sections were configured into a three-dimensional matrix and displayed graphically. Regression lines were formed through the centroids of the ellipses from each axial section, and from these, the squareshape of the grid was reconstructed. This allowed a magnetic resonance-generated plane of reference to be calculated for each subject. The reference plane from the metrograph data recorded after each electromyographic session was then made coplanar with the magnetic resonance-generated plane for that subject. All relevant reference points were subsequently superimposed to permit the location of the paired needle tips to be displayed within the reconstructed masseter muscle. This method for stereotactically locating needle electrode recording sites within the human masseter muscle has been described in detail elsewhere (McMillan and Hannam, 1989a). The paired recording sites for each subject were displayed within a graphic reconstruction of the right masseter muscle viewed in three planes. As the threedimensional coordinates of these needle tip locations were known, the linear distance between each pair could be calculated. The distances between each pair of recording sites were also calculated separately along anteroposterior, superior-inferior and medio-lateral axes. From these, mean orthogonal distances were computed for the 32 paired recording locations. Statistical comparisons between the mean distances along each axis were performed using paired t-tests. RESULTS Single motor-units were activated by tasks such as light intercuspal clenching and jaw retrusion during which the units could be fired freely without muscle discomfort. When a clearly defined compound action potential was obtained from a single unit located at one of the needle tips, the unit could be fired slowly and continuously at low levels of effort (S-10% of maximum). Unit activation strategies that allowed slow, regular firing appeared to vary throughout the muscle. In almost all instances, the second electrode, which was initially located approx. 15-22 mm from the first, had to be reinserted within the muscle at a position nearer to the triggering electrode, In many instances the second needle had to be repositioned 2-3 times progressively closer to the triggering site before timelocked compound action potentials could be recorded at both needle tips. Synchronous compound action potentials were always obtainable from the unit investigated at each experimental session (Fig. 3). The distribution by region of the 32 triggering sites is depicted in Fig. 4. The mean linear distance measured three-dimensionally between the 32 paired recording sites from which synchronous single-unit activity could be obtained was 8.8 f 3.4 mm, and ranged from 5 to
(a)
-~_n
I
0.4mV
(b)
-‘)
__-__P-
5ms
Fig. 3. Time-locked, averaged (n = 16), single motor-unit, compound action potentials recorded by the triggering electrode ‘a’, and by the second electrode ‘b’. 20mm. A distribution histogram for these data is shown in Fig. 5. The mean distances measured along anteroposterior, superior-inferior and medio-lateral axes for the 32 paired recording sites were 6.1 f 4.0 mm (range 0.3-19.0 mm), 3.8 f 2.5 mm (0.1-l 1.5 mm) and 3.2 + 2.3 mm (0.1-10.0 mm), respectively. The unit terntories, therefore, appeared to have a preferred axis of orientation, because the distances between the 32 pairs of recording sites measured along an anteroposterior axis were approximately double those measured along a superior-inferior or medio-lateral axis (p < 0.01). The motor-unit territories thus appeared to be ovoid or ‘cigar-shaped’, and arranged in layers throughout the muscle irrespective of their locations. DBCUSSION
Our recording method was based on the technique of electrophysiological cross-sectional scanning of motor units in human muscles (Stalberg and Eriksson, 1987; Schwartz et al., 1976; Stalberg and Antoni, 1980), but with a number of modifications. Stalberg and Antoni (1980) originally described the use of a single-fibre electrode to record a single-fibre action potential, which acted as a trigger. A second concentric needle was used to probe for motor-unit activity, synchronous with the single-fibre action potential in the cross-section of the muscle, without confirmation of the spatial relationship of the needlerecording locations within the muscle as a whole. In the present study, however, we used two monopolar needles with one acting as the triggering electrode. The paired needles were used to probe for synchronous motor-unit activity in the masseter muscle cross-section, and along three orthogonal axes, to reduce the likelihood of underestimating the territory
Motor-unit territory in the masscter
b
Fig. 4. (a) Distribution by region of 32 single motor-unit triggering sites in the right mass&r muscle. Each number represents the total number of units sampled in that region. (b), (c) and (d) represent a three dimensional slice reconstruction of the right masseter muscle (M), the right articular condyle (C), right maxillary canine (Ca), viewed in three planes. The location of the two needle electrodes tips, {a) and (b), within the masseter muscle are depicted. In this instance the linear distance between the paired recording sites was 11 mm.
lo23
-
8 k Y
5
‘32 8 8 8
‘I I
JL
5.5 4.5
7.5 6.5
9.5 0.5
ll.5 xx5
135 125
15.5 14.5
I
I
17.5 m5 16.5 la5
LIISTANCE BETWEEN PARED RECCllXW3
(mm)
Fig. 5. Distribution histogram of the distance between 32 paired recording sites in the right mass&r muscle.
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A. S. MCMILLAN and A. G. HANNAM
of motor units by unidirectional cross-sectional probing through this multipinnate muscle. In addition, because the needle recording tips could be located stereotactically in three dimensions of space, the location of these sites could be displayed within a three-dimensional reconstruction of the masseter muscle. Previously, this has not been possible in studies of masseter motor-unit territory (Stalberg and Eriksson, 1987). There was a potential systematic error inherent in our experimental method which resulted, in part, from the need to limit the number of needle penetrations at any one experiment in order to maintain patient compliance. At each recording session the second electrode was initially located approx. 20 mm from the triggering site (as measured on the skin surface). However, if no synchronous electromyographic activity was recorded in the muscle cross-section at that particularly site, the needle was moved progressively closer to the triggering site. If no activity was recorded after 2-3 probes the needle was then moved to a position 5-7 mm from the triggering electrode, where a synchronous compound action potential could usually be recorded. Thus, in some instances, it was possible that the limits of the motor-unit territory were underestimated along the axis defined by the line joining the two recording tips. The distances between paired recording sites were markedly greater than the mean diameter of 3.7 + 0.6 mm for single motor-units reported for the inferior part of the masseter by Stalberg and Eriksson (1987) and the territories may be even larger because the radius of pick-up of our needle electrode was estimated to be 2 mm. Focal motor-unit territories in the pig masseter muscle described by Herring et al. (1989) are also apparently significantly smaller. The distances that we found between paired recording sites in the medio-lateral direction were none the less similar to the territories defined by Stalberg and Eriksson (1987), who used transverse cross-sectional scanning. Although the diameters of most single motor units described by Stalberg and Eriksson (1987) were less than 5 mm, 5 out of 32 recordings had diameters which ranged from 5.0-12.5 mm, and three of these appeared to traverse a large part of the muscle cross-section. Likewise, a small number of our paired data (6 out of 32) ranged from 5-10 mm measured in the mediolateral direction. This finding is at variance with observations in the human limb and most animal muscles where motor-unit fibres are distributed over only part of the muscle cross-section (e.g. Buchthal and Schmalbruch, 1980; Stalberg and Antoni, 1980; Stalberg et al., 1976). It does, however, concur with Stalberg and Eriksson’s (1987) finding that a small number of masseter units may have quite large territories. Motor-unit territories in the masseter muscle, although larger than previously reported, do not, in most instances, appear to extend widely throughout the muscle, and may in fact be restricted to specific regions. The results also suggest that there is a preferred axis of orientation in the anteroposterior direction between pairs of recording sites. This is consistent with the notion of cigar-shaped motor-unit territories arranged in layers throughout the muscle, rather than the circular or spherical territories proposed by Stalberg and Eriksson (1987).
Schumacher (1961) described the separation of successive layers of muscle fibres by connective tissue septa from the superficial to the deep part of the muscle. Within these layers, aggregations were greater in the anteroposterior direction than along other axes. The preferred orientation of the single motor-unit territories of the masseter appears consistent with the anatomical compartments described previously by Schumacher (1961, 1982). We are, however, cautious in drawing general conclusions from the data because of the small number of subjects used in our study. Our method of estimating motor-unit territory in the masseter relies on the absence of motor-unit synchronization within the muscle. In normal muscles, motor units are presumed to recruit asynchronously (Loeb et al., 1987), and during the ensucontraction ing voluntary each unit fires independently (Milner-Brown, Stein and Lee, 1975). In human muscles, synchronization has been described in subjects with neuromuscular disorders (Milner-Brown et al., 1974). Synchronization has also been observed within the muscles of normal subjects who regularly exert large, brief forces (e.g. weightlifters and manual labourers), and it is observed more commonly when the duration of muscle contraction increases and particularly with muscle fatigue (Milner-Brown et al., 1975; Person and Kudina, 1968). In the human masseter muscle, Yemm (1977) was unable to detect any tendency towards synchronization of motor units using the rectified electromyographic technique described by Milner-Brown, Stein and Yemm (1973). Likewise Goldberg and DerBer (1977) and Nordstrom, Miles and Veale (1989), who used cross-correlation histograms, reported no tendency towards synchrony of masseter motor-units. In the present study, masseter motor-units fired for only short periods of time and at low force thresholds, therefore any tendency towards synchronous firing within the muscle, although possible, was unlikely. The restriction of motor-units to certain regions of the masseter muscle provides a potential substrate for differential motor control of discrete regions of the muscle, as has been proposed previously (Stalberg and Eriksson, 1987), and reported in pig and rabbit masseter muscles (Herring et al., 1989; 1979; Weijs and Dantuma, 1981). Thus, differential contraction of single motor-units in separate parts of the muscle would then permit multidirectional contraction of internal connective-tissue septa, and thereby provide a functional basis for the heterogeneous behaviour of the human masseter muscle suggested by Belser and Hannam (1986) and Eriksson, Stalberg and Antoni (1984). The wide distribution of a small number of motorunit territories in the muscle cross-section does, however, suggest that putative muscle compartments may not be based solely on the internal anatomical features of the muscle. Human masseter muscle compartments may not, in fact, have strictly defined boundaries, and some unit territories may traverse more than one compartment, as proposed by Stalberg and Eriksson (1987). Previous studies by Herring et al. (1989) in pig masseter muscle suggest that there may not be clear-cut anatomical compartments but rather, less distinct functional subdivisions. The
Motor-unit territory in the masseter extent to which this ‘functional compartmentalization’ applies to the human masseter is presently uncertain. Certainly the concept of ‘regional specialization’ has been proposed for the human masseter muscle by Stalberg and Eriksson (1987), but is equivocal without further insight into the specific behaviour patterns of single motor-units in different, known regions of the muscle. Acknowledgements-The work was supported by the Medical Research Council of Canada. The assistance of Mr Bruce Sinclair is also gratefully acknowledged.
REFERENCES
Belser U. and Hannam A. G. (1986) The contribution of the deep fibres of the masseter muscle to selected toothclenching tasks. J. prosthet. Dent. 56, 629636. Buchthal F. and Schmalbruch H. (1980) Motor units of mammalian muscle. Physiol. Rev. 60, 9&142. Burke R. E. (1981) Motor units: anatomy, physiology and functional organization. In Handbook of Physiology. Section 1: The Nervous System, Vol. Il. Motor control, Part 1, pp. 345-422. Burke R. E. and Tsairis P. (1973) Anatomy and innervation ratios in motor units of cat gastrocnemius. J. Physiol. 234, 723-748.
Edstrom L. and Kugelberg E. (1968) Histochemical composition, distribution of fibres and fatiguability of single motor units. J. Neurol. Neurosurg. Psychiat. 31,424-433. English A. W. (1985) Limbs vs jaws: can they be compared? Am. Zool. 25, 351-363.
English A. W. and Letbetter W. D. (1982) A histochemical analysis of identified compartments in cat lateral gastrocnemius. Expl Brain Res. 56, 361-368. Eriksson P.-O., Stalberg E. and Antoni L. (1984) Flexibility in motor-unit firing pattern in the human temporal and masseter muscles related to type of activation and location. Archs oral Biol. 29, 7071712. Gath I. and Stalbere- E. (1976) ~ , Techniaues for imnrovine . _ the selectivity of electromyographic recordings. IEEE Trans. Biomed. Engng NME-23, 467472. Goldberg L. J. and Derfler B. (1977) Relationship among recruitment order, spike amplitude, and twitch tension of single motor units in human masseter muscle. J. Neurophysiol. 40, 879-890.
Herring S. W. and Wineski L. E. (1986) Development of the masseter muscle and oral behaviour ion the pig. J. exp. Zool. 237, 191-207. Herring S. W., Grimm A. F. and Grimm B. R. (1979) Functional heterogeneity in a multipinnate muscle. Am. J. Anat. 154, 563-576. Herring S. W., Wineski L. E. and Anapol F. C. (1989) Neural organization of the masseter muscle of the pig. J. camp. Neurol. 280, 563-576.
Letbetter W. D. (1974) Influence of intramuscular nerve branching on motor unit organization in medial gastrocnemius muscle. Anat. Rec. 178, 402.
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Loeb G. E., Pratt C. A., Chanaud C. M. and Richmond F. J. R. (1987) Distribution and innervation of short-interdigitating muscle fibres in parallel&bred muscles of cat hindhmbs. 2. Morph. 191, 1115. McMillan A. S. and Hannam A. G. (1989a) > , Location of needle electrode recording sites in the human masscter muscle by magnetic resonance imaging. J. Neurosci. Methods 30, 85-89.
McMillan A. S. and Hannam A. G. (1989b) Motor unit territory in the human masseter muscle. J. dent. Res. 68, 951.
Milner-Brown H. S., Stein R. B. and Yemm R. (1973) The isometric properties of human motor units during voluntary isometric contractions. J. Physiol. 228, 285-306. Milner-Brown H. S., Stein R. B. and Lee R. G. (1974) The contractile and electrical properties of human motor units in neuropathies and motor neurone disease. J. Neurol. Neurosurg. Psych&.
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Milner-Brown H. S., Stein R. B. and Lee R. G. (1975) Synchronization of human motor units: possible roles of exercise and supraspinal reflexes. Electroenceph. clin. Neurophysiol. 38, 245254.
Norstrom M. A., Miles T. S. and Veale J. L. (1989) Effect of motor unit firing pattern on twitches obtained by spike-triggered averaging. Muscle Nerve 12, 556567. Person R. S. and Kudina L. P. (1968) . , Cross-correlation of electromyograms showing interference patterns. Electroenceph. clin. Neurophysiol. 25, 58-68. _
Richmond F. J. R.. MacGillis D. R. R. and Scott D. A. (1985) Muscle fibre compartmentalization in cat splenius muscle. J. Neurophysiol. 53, 868-885. Schumacher G.-H. (1961) Funktionelle morphologie der kaumuskulatur. Veb Gustav F&hen, Jena. Schumacher G.-H. (1982) V. Comparative functional anatomy of jaw muscles. In Jaw Position and Jaw Movement (Eds Kubota K., Nakamura Y. and Schumacher G.-H.), pp. 76-93. Veb, Volk & Geschundheit, Berlin. Schwartz M. S., Stalberg E., Schiller H. H. and Thiele B. (1976) The reinnervated motor unit in man. J. Ncurol. Sci. 27, 303-312.
Stalberg E. (1980) Macro EMG, a new recording technique. J. Neurol. Psychiat. 43, 475-482.
Stalberg E. and Trontelj J. V. (1979) Single Pibre Electromyography. Miravelle Press, Old Woking, U.K. Stalberg E. and Antoni L. (1980) Electrophysiological cross section of the motor unit. J. Neurol. Neurosurg. Psychiat. 43, 469-474.
Stalberg E. and Eriksson P.-O. (1987) A scanning electromyographic study of the topography of human masseter sinale motor units. Archs oral Biol. 32. 793-797. Stalberg E, Schwartz M. S., Thiele B. and Schiller H. H. (1976) The normal motor unit in man. A single fibre EMG multielectrode investieation. J. Neurol. Sci. 27. 191-201. Weijs W. A. and Dantuma R. (1981) Functional anatomy of the masticatory apparatus in the rabbit (Orycrolagus cuniculus L.). Neth. J. Zool. 31, 99-147. Yemm R. (1977) The orderly recruitment of motor units of the masseter and temporal muscles during voluntary isometric contraction in man. J. Physiol. 265, 1633174.
0003-9969/91 83.00 + 0.00
Copyright 0 1991Pergamon Press plc
MOTOR-UNIT TERRITORY IN THE HUMAN MASSETER MUSCLE A. S. MCMILLANI and A. G. HANNAM’ ‘Department of Clinical Dental Sciences and 2Department of Oral Biology, Faculty of Dentistry, The University of British Columbia, Vancouver, B.C., Canada V6T 127 (Accepted 9 January 1991)
Sammary-Motor-unit territories in human masseter are reportedly focal and related to putative subvolumes of muscle. However, in the absence of a reliable method of locating needle-electrode recording sites within the muscle in three dimensions and due to inherent weaknesses in electromyographic recording techniques, the limits of motor-unit territory in the masseter may have been underestimated. Single motor-unit responses were recorded as time-locked events from 32 paired-needle recording sites throughout the masseter muscles of three subjects. Recording sites were located stereotactically with an optical system, magnetic resonance imaging, and a common reference, then displayed graphically in three dimensions. The mean linear separation of the paired recording sites was 8.8 f 3.4 mm. The putative territories had a preferred orientation in the antero-posterior axis. Motor-unit territories were larger than described previously and appeared to be related to anatomical compartments. The restriction of these territories to discrete regions of the muscle provides an anatomical substrate for selective regional motor control of the human masseter muscle. Key words: motor-unit, electromyography,
masseter muscle, stereotaxy.
INTRODUCIION
There is ample evidence that the fibres of many motor units are scattered throughout substantial areas of the limb and trunk muscles, for example 20% of the muscle volume in the case of the rat soleus muscle and 14% in the cat medial gastrocnemius muscle (e.g. Burke, 1981; Burke and Tsaitis, 1973; Edstrom and Kugelberg, 1968; Stalberg et al., 1976). There are, however, some limb and jaw muscles that appear outwardly to be single structures whereas internally they incorporate a number of putative subvolumes (English and Letbetter, 1982; Herring, Wineski and Anapol, 1989; Letbetter, 1974; Richmond, MacGillis and Scott, 1985). In these cases, motor-unit territories seem to be confined within functional or anatomical ‘compartments’, or both. These findings have raised speculation about the nature of motor control in a compartmentalized muscle because the presence of localized motor-unit territories could conceivably permit differential motor control of separate regions of the muscle (Belser and Hannam, 1986; Herring et al., 1989; Herring, Grimm and Grimm, 1979; English, 1985; Stalberg and Eriksson, 1987). Evidence in support of the focal distribution of motor units may be inferred from descriptions of differential activity in distinct regions of anatomically complex muscles such as the jaw elevator muscles during the performance of routine functional tasks (Herring et al., 1979, 1989; Herring and Wineski, 1986; Weijs and Dantuma, 1981). Although motor-unit territories have been investigated quite extensively in animal muscles (reviewed by Buchthal and Schmalbruch, 1980; Burke, 1981) there is a dearth of information on them in human muscles, and the jaw muscles in particular. The
distribution of motor-units within the human masseter muscle is reputed to be focal, approx. 3-5 mm dia, more akin to the territories of animal jaw muscles than those found in human limb and trunk muscles, and the distribution is considered to be related to internal muscle compartments (Buchthal and Schmalbruch, 1980; Herring et al., 1979, 1989; Stalberg and Eriksson, 1987). It is, however, likely that motor-unit territories in human masseter have been underestimated because of inherent weaknesses in the indirect experimental techniques used previously (McMillan and Hannam, 1989a, b). We suggested recently that uniaxial cross-sectional scanning may be an inappropriate method by which to determine motor-unit territory in a multipinnate muscle such as the human masseter because the complex interdigitation of the constituent muscle fibres may preclude sampling from all fibres of the single motor unit. We proposed a more appropriate experimental approach in which single motorunit activity is sampled in several regions of the masseter muscle simultaneously, provided the recording sites can be located stereotactically in three dimensions of space (McMillan and Hannam, 1989a). A sensitive method of stereotactically locating needle electrode recording sites within the human masseter muscle has been developed (McMillan and Hannam, 1989a). The availability of this technique prompted us to map motor-unit territory in the masseter using multiple electrodes in known regions of the muscle. We considered that a more complete understanding of this motor-unit distribution would provide insight into the functional compartmentalization of this complex muscle, and that of jaw elevator muscles in general. 435
436
A. S. MCMILLAN MATERIALS
AND METHODS
Single motor -unit recordings Mapping technique. Single motor-unit electromyographic experiments were carried out on two male and one female subjects aged 31-36 yr. Each subject had a complete natural dentition and no history of jaw dysfunction. The subjects were selected because of their skill in activation of single motor-units, which is an advantage in this type of experiment. The experiment was approved by the Human Experimentation Committee at the University of British Columbia, and each subject gave informed consent. Two Teflon-covered monopolar needle electrodes (MF-37, TECA, Pleasantville, NY) were inserted into the right masseter muscle, and their position was stabilized with a light metal platform. Reference electrodes were attached to the skin over the muscle. At the beginning of each recording session, the needles were normally situated approx. 15-20 mm apart (as measured on the skin surface). Single motor-unit activity was amplified (Model AL 2010, Axon Instruments Inc., Burlingame, CA) and bandpass-filtered (l-10 kHz). Units were activated by strategies that allowed continuous firing at a low frequency (approx. 10-12 Hz) with the aid of auditory and visual feedback. When a clearly defined compound action potential was obtained from a group of single motor-unit fibres located at one of the needle tips it was used to trigger a digital oscilloscope sweep (Model 2221, Tektronix Canada Inc., Vancouver, B.C.). Any synchronous activity recorded from the second needle was displayed on the second channel of the oscilloscope as a time-locked event, and therefore was considered to originate from the same single motor-unit. If no synchronous activity was recorded, the second needle was repositioned progressively closer to the triggering site until a synchronous compound action potential was recorded. At each location the needle electrodes were moved in and out of the muscle along the conventional trajectory used in uniaxial cross-sectional scanning until compound action potentials of maximum amplitude were obtained at both recording sites. The single motor-unit responses from the two recording sites were sampled and averaged, then plotted (Model HClOOO, Tektronix Canada Inc., Vancouver, B.C.). In order to probe different parts of the muscle adequately, each muscle was divided into eight arbitrary regions. The muscle was first divided into major superficial and deep parts, which in turn were subdivided into quadrants. Paired single motor-unit recordings were obtained in each of these regions for a total of 32 units. Recording selectivity of the electromyographic technique. The increase in selectivity of electromyographic
recordings achieved by highpass-filtering has been described previously (Gath and Stalberg, 1976; Stalberg and Trontelj, 1979), and is a useful technique when selective preservation of high-frequency components of a signal is desired. The higher spatial resolution achieved by this method is advantageous in territorial mapping of single motor-units when multiple needles are used simultaneously because it minimizes the possibility of recording from the same group of fibres.
and A. G.
HANNAM
As a precursor to the mapping experiments, the selectivity of the monopolar electrode achieved by filtering the low-frequency components from the amplified signal was investigated in four masseter motor units of two normal male subjects aged 34 yr. A small adhesive scale, graduated in mms, was attached to the Teflon coating of the needle. The needle was inserted percutaneously at right angles to the skin surface and supported by a metal framework, so that the scale on the grid could be visualized relative to the metal framework. The amplifier bandpass-filters were adjusted to eliminate signal frequency components beyond the range l-10 kHz throughout the recording session. The needle was moved within the muscle until a compound action potential from a single motor-unit was observed on a digital oscilloscope screen during the performance of a gentle tooth-clenching task. While the single motor-unit fired continuously, the needle was moved manually along its medio-lateral trajectory until a compound action potential of maximum amplitude was obtained, i.e. the needle tip was closest to the single motor-unit. It was considered too cumbersome to use a micromanipulator to move the needle in the muscle cross-section (Stalberg and Eriksson, 1987), because the needle was repeatedly inserted and retracted in order to locate a compound action potential of maximum amplitude. The compound action potential was used to trigger the oscilloscope sweep, and an averaged potential for the single unit was recorded and plotted. The needle was moved along a medio-lateral trajectory, first deep, then superficial to the primary recording site, in mm increments. These were verified by means of the graduated scale on the needle which was referenced to the supporting metal framework. Averaged compound action potentials from the single motor-unit were obtained at positions +2, + 1, - 1, -2 mm relative to the primary recording site (Fig. 1). The amplitude of each compound action potential from a single motor-unit was measured at the primary recording site and at the different needle positions. There was a significant reduction in this amplitude as the needle was moved further from the site of the single motor-unit fibre group within the muscle, viz. a 5585% decrease in the signal amplitude at a distance of 2 mm. Voltage ratios (dB) were calculated at each needle position relative to the primary recording site. The mean voltage ratios of the single motor units at needle positions +2, + 1, - 1, -2 mm relative to the primary recording sites were 8.6 f 3.0, 3.1 f 1.0, 3.4 + 0.4 and 9.9 f 3.6dB, respectively. Based on these findings, the volume of pick-up of the monopolar electrode was estimated to be approx. +2 mm, when an amplifier bandwidth of l-10 kHz was used. This is comparable with the value for monopolar needles reported by Stalberg (1980). An amplifier bandwidth of l-10 kHz was therefore employed in the present territorial mapping experiments. Stereotactic location of electrode recording sites
At the end of each paired-needle recording session, a customized reference grid (which incorporated four copper sulphate-filled glass tubes aligned to form a
Motor-unit territory in the masseter
437 5ms
1
, -2
0.2mV
, -1
0
+l
+2(mm)
Fig. 1. Changes in a single masseter motor-unit electromyographic signal according to the position of the electrode recording tip. Changes in waveform shape of an averaged (n = 16),single motor unit, compound action potential as the needle tip is moved f 2 mm along a media-lateral axis from the location of the signal of maximum amplitude. square) was placed between the teeth of the subject (see Fig. 2). The four point angles of the grid (which defined a reference plane), and two known points on each needle were digitized three-dimensionally in situ, by means of a Reflex Metrograph (HF Ross, Salisbury, Wilts., England), and the data were stored digitally for off-line analysis. Because the length of each needle was known, the position of the needle tips relative to the Metrograph-based reference plane could be calculated.
Before the first recording session, the pertinent oro-facial structures of each of the three subjects were imaged by magnetic resonance, with the reference grid in situ. This was carried out with a Picker Vista MRl 100 system, using a 0.15T magnet. Spin-echo sequences with a fixed repetition time (TR:833 ms) and echo time (TE:60 ms) were used to obtain a series of 16 contiguous, 5 mm sections in the axial plane (Fig. 2). The copper sulphate incorporated in the glass tubes of the reference grid appeared as ovoid
Fig. 2. Relationship of the reference grid to oro-facial landmarks and the magnetic resonance plane of section. The reference grid comprises four glass tubes in the form of a square, with four point angles. The position of the grid relative to the right masseter muscle and a needle electrode within the muscle is shown on the right. On the left, the relationship of 16 contiguous axial magnetic-resonance sections to the right masseter muscle, the right articular condyle, the teeth and the grid are depicted. AOB X,&-s
A. S. MCMILLAN and A. G. HANNAM
438
markers (ellipses) in contiguous magnetic resonance sections. From each axial section, the outlines of the right masseter muscle, the right articular condyle, the right maxillary canine tooth, and the centroid of each copper sulphate marker were digitized by means of a digitizer and computer (Models HP9874 and HP350, Hewlett Packard Canada, Vancouver, B.C.). The digitized sections were configured into a three-dimensional matrix and displayed graphically. Regression lines were formed through the centroids of the ellipses from each axial section, and from these, the squareshape of the grid was reconstructed. This allowed a magnetic resonance-generated plane of reference to be calculated for each subject. The reference plane from the metrograph data recorded after each electromyographic session was then made coplanar with the magnetic resonance-generated plane for that subject. All relevant reference points were subsequently superimposed to permit the location of the paired needle tips to be displayed within the reconstructed masseter muscle. This method for stereotactically locating needle electrode recording sites within the human masseter muscle has been described in detail elsewhere (McMillan and Hannam, 1989a). The paired recording sites for each subject were displayed within a graphic reconstruction of the right masseter muscle viewed in three planes. As the threedimensional coordinates of these needle tip locations were known, the linear distance between each pair could be calculated. The distances between each pair of recording sites were also calculated separately along anteroposterior, superior-inferior and medio-lateral axes. From these, mean orthogonal distances were computed for the 32 paired recording locations. Statistical comparisons between the mean distances along each axis were performed using paired t-tests. RESULTS Single motor-units were activated by tasks such as light intercuspal clenching and jaw retrusion during which the units could be fired freely without muscle discomfort. When a clearly defined compound action potential was obtained from a single unit located at one of the needle tips, the unit could be fired slowly and continuously at low levels of effort (S-10% of maximum). Unit activation strategies that allowed slow, regular firing appeared to vary throughout the muscle. In almost all instances, the second electrode, which was initially located approx. 15-22 mm from the first, had to be reinserted within the muscle at a position nearer to the triggering electrode, In many instances the second needle had to be repositioned 2-3 times progressively closer to the triggering site before timelocked compound action potentials could be recorded at both needle tips. Synchronous compound action potentials were always obtainable from the unit investigated at each experimental session (Fig. 3). The distribution by region of the 32 triggering sites is depicted in Fig. 4. The mean linear distance measured three-dimensionally between the 32 paired recording sites from which synchronous single-unit activity could be obtained was 8.8 f 3.4 mm, and ranged from 5 to
(a)
-~_n
I
0.4mV
(b)
-‘)
__-__P-
5ms
Fig. 3. Time-locked, averaged (n = 16), single motor-unit, compound action potentials recorded by the triggering electrode ‘a’, and by the second electrode ‘b’. 20mm. A distribution histogram for these data is shown in Fig. 5. The mean distances measured along anteroposterior, superior-inferior and medio-lateral axes for the 32 paired recording sites were 6.1 f 4.0 mm (range 0.3-19.0 mm), 3.8 f 2.5 mm (0.1-l 1.5 mm) and 3.2 + 2.3 mm (0.1-10.0 mm), respectively. The unit terntories, therefore, appeared to have a preferred axis of orientation, because the distances between the 32 pairs of recording sites measured along an anteroposterior axis were approximately double those measured along a superior-inferior or medio-lateral axis (p < 0.01). The motor-unit territories thus appeared to be ovoid or ‘cigar-shaped’, and arranged in layers throughout the muscle irrespective of their locations. DBCUSSION
Our recording method was based on the technique of electrophysiological cross-sectional scanning of motor units in human muscles (Stalberg and Eriksson, 1987; Schwartz et al., 1976; Stalberg and Antoni, 1980), but with a number of modifications. Stalberg and Antoni (1980) originally described the use of a single-fibre electrode to record a single-fibre action potential, which acted as a trigger. A second concentric needle was used to probe for motor-unit activity, synchronous with the single-fibre action potential in the cross-section of the muscle, without confirmation of the spatial relationship of the needlerecording locations within the muscle as a whole. In the present study, however, we used two monopolar needles with one acting as the triggering electrode. The paired needles were used to probe for synchronous motor-unit activity in the masseter muscle cross-section, and along three orthogonal axes, to reduce the likelihood of underestimating the territory
Motor-unit territory in the masscter
b
Fig. 4. (a) Distribution by region of 32 single motor-unit triggering sites in the right mass&r muscle. Each number represents the total number of units sampled in that region. (b), (c) and (d) represent a three dimensional slice reconstruction of the right masseter muscle (M), the right articular condyle (C), right maxillary canine (Ca), viewed in three planes. The location of the two needle electrodes tips, {a) and (b), within the masseter muscle are depicted. In this instance the linear distance between the paired recording sites was 11 mm.
lo23
-
8 k Y
5
‘32 8 8 8
‘I I
JL
5.5 4.5
7.5 6.5
9.5 0.5
ll.5 xx5
135 125
15.5 14.5
I
I
17.5 m5 16.5 la5
LIISTANCE BETWEEN PARED RECCllXW3
(mm)
Fig. 5. Distribution histogram of the distance between 32 paired recording sites in the right mass&r muscle.
440
A. S. MCMILLAN and A. G. HANNAM
of motor units by unidirectional cross-sectional probing through this multipinnate muscle. In addition, because the needle recording tips could be located stereotactically in three dimensions of space, the location of these sites could be displayed within a three-dimensional reconstruction of the masseter muscle. Previously, this has not been possible in studies of masseter motor-unit territory (Stalberg and Eriksson, 1987). There was a potential systematic error inherent in our experimental method which resulted, in part, from the need to limit the number of needle penetrations at any one experiment in order to maintain patient compliance. At each recording session the second electrode was initially located approx. 20 mm from the triggering site (as measured on the skin surface). However, if no synchronous electromyographic activity was recorded in the muscle cross-section at that particularly site, the needle was moved progressively closer to the triggering site. If no activity was recorded after 2-3 probes the needle was then moved to a position 5-7 mm from the triggering electrode, where a synchronous compound action potential could usually be recorded. Thus, in some instances, it was possible that the limits of the motor-unit territory were underestimated along the axis defined by the line joining the two recording tips. The distances between paired recording sites were markedly greater than the mean diameter of 3.7 + 0.6 mm for single motor-units reported for the inferior part of the masseter by Stalberg and Eriksson (1987) and the territories may be even larger because the radius of pick-up of our needle electrode was estimated to be 2 mm. Focal motor-unit territories in the pig masseter muscle described by Herring et al. (1989) are also apparently significantly smaller. The distances that we found between paired recording sites in the medio-lateral direction were none the less similar to the territories defined by Stalberg and Eriksson (1987), who used transverse cross-sectional scanning. Although the diameters of most single motor units described by Stalberg and Eriksson (1987) were less than 5 mm, 5 out of 32 recordings had diameters which ranged from 5.0-12.5 mm, and three of these appeared to traverse a large part of the muscle cross-section. Likewise, a small number of our paired data (6 out of 32) ranged from 5-10 mm measured in the mediolateral direction. This finding is at variance with observations in the human limb and most animal muscles where motor-unit fibres are distributed over only part of the muscle cross-section (e.g. Buchthal and Schmalbruch, 1980; Stalberg and Antoni, 1980; Stalberg et al., 1976). It does, however, concur with Stalberg and Eriksson’s (1987) finding that a small number of masseter units may have quite large territories. Motor-unit territories in the masseter muscle, although larger than previously reported, do not, in most instances, appear to extend widely throughout the muscle, and may in fact be restricted to specific regions. The results also suggest that there is a preferred axis of orientation in the anteroposterior direction between pairs of recording sites. This is consistent with the notion of cigar-shaped motor-unit territories arranged in layers throughout the muscle, rather than the circular or spherical territories proposed by Stalberg and Eriksson (1987).
Schumacher (1961) described the separation of successive layers of muscle fibres by connective tissue septa from the superficial to the deep part of the muscle. Within these layers, aggregations were greater in the anteroposterior direction than along other axes. The preferred orientation of the single motor-unit territories of the masseter appears consistent with the anatomical compartments described previously by Schumacher (1961, 1982). We are, however, cautious in drawing general conclusions from the data because of the small number of subjects used in our study. Our method of estimating motor-unit territory in the masseter relies on the absence of motor-unit synchronization within the muscle. In normal muscles, motor units are presumed to recruit asynchronously (Loeb et al., 1987), and during the ensucontraction ing voluntary each unit fires independently (Milner-Brown, Stein and Lee, 1975). In human muscles, synchronization has been described in subjects with neuromuscular disorders (Milner-Brown et al., 1974). Synchronization has also been observed within the muscles of normal subjects who regularly exert large, brief forces (e.g. weightlifters and manual labourers), and it is observed more commonly when the duration of muscle contraction increases and particularly with muscle fatigue (Milner-Brown et al., 1975; Person and Kudina, 1968). In the human masseter muscle, Yemm (1977) was unable to detect any tendency towards synchronization of motor units using the rectified electromyographic technique described by Milner-Brown, Stein and Yemm (1973). Likewise Goldberg and DerBer (1977) and Nordstrom, Miles and Veale (1989), who used cross-correlation histograms, reported no tendency towards synchrony of masseter motor-units. In the present study, masseter motor-units fired for only short periods of time and at low force thresholds, therefore any tendency towards synchronous firing within the muscle, although possible, was unlikely. The restriction of motor-units to certain regions of the masseter muscle provides a potential substrate for differential motor control of discrete regions of the muscle, as has been proposed previously (Stalberg and Eriksson, 1987), and reported in pig and rabbit masseter muscles (Herring et al., 1989; 1979; Weijs and Dantuma, 1981). Thus, differential contraction of single motor-units in separate parts of the muscle would then permit multidirectional contraction of internal connective-tissue septa, and thereby provide a functional basis for the heterogeneous behaviour of the human masseter muscle suggested by Belser and Hannam (1986) and Eriksson, Stalberg and Antoni (1984). The wide distribution of a small number of motorunit territories in the muscle cross-section does, however, suggest that putative muscle compartments may not be based solely on the internal anatomical features of the muscle. Human masseter muscle compartments may not, in fact, have strictly defined boundaries, and some unit territories may traverse more than one compartment, as proposed by Stalberg and Eriksson (1987). Previous studies by Herring et al. (1989) in pig masseter muscle suggest that there may not be clear-cut anatomical compartments but rather, less distinct functional subdivisions. The
Motor-unit territory in the masseter extent to which this ‘functional compartmentalization’ applies to the human masseter is presently uncertain. Certainly the concept of ‘regional specialization’ has been proposed for the human masseter muscle by Stalberg and Eriksson (1987), but is equivocal without further insight into the specific behaviour patterns of single motor-units in different, known regions of the muscle. Acknowledgements-The work was supported by the Medical Research Council of Canada. The assistance of Mr Bruce Sinclair is also gratefully acknowledged.
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