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CRITICAL REVIEWS IN ORAL BIOLOGY & MEDICINE |
Fiber-type Composition of the Human Jaw Muscles—(Part 1) Origin and Functional Significance of Fiber-type Diversity
J.A.M Korfage,
J.H. Koolstra,
G.E.J. Langenbach and
T.M.G.J. van Eijden*
Department of Functional Anatomy, Academic Center for Dentistry Amsterdam, Meibergdreef 15, 1105 AZ Amsterdam, The Netherlands;
Correspondence: * corresponding author, t.m.vaneijden{at}amc.uva.nl
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ABSTRACT
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This is the first of two articles on the fiber-type composition of the human jaw muscles. The present article discusses the origin of fiber-type composition and its consequences. This discussion is presented in the context of the requirements for functional performance and adaptation that are imposed upon the jaw muscles. The human masticatory system must perform a much larger variety of motor tasks than the average limb or trunk motor system. An important advantage of fiber-type diversity, as observed in the jaw muscles, is that it optimizes the required function while minimizing energy use. The capacity for adaptation is reflected by the large variability in fiber-type composition among muscle groups, individual muscles, and muscle regions. Adaptive changes are related, for example, to the amount of daily activation and/or stretch of fibers. Generally, the number of slow, fatigue-resistant fibers is relatively large in muscles and muscle regions that are subjected to considerable activity and/or stretch.
Key Words: jaw muscles • fiber type • myosin heavy-chain
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INTRODUCTION
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Jaw muscles are active during a large variety of motor tasks, like mastication, biting, speech, and swallowing. To execute this variety in tasks, they must be able to control the position of the mandible precisely, and instantaneously apply changing forces to it. The jaw muscles can meet these different requirements because of their complex architecture, in combination with a heterogeneous composition of fibers capable of producing a variety of forces at different contraction speeds. [For an extensive review of various aspects of the functional anatomy of the jaw muscles and their control, the reader is referred to several recent publications (e.g., Miller, 1991; Hannam and McMillan, 1994; Van Eijden and Turkawski, 2001; Langenbach and Van Eijden, 2001; Miles and Nordstrom, 2002).] Based on immunohistochemical features and differences in contraction velocity and fatigability, muscle fibers have been classified into several types: for example, types I, IIA, IIX, and IIB fibers (e.g., Hoh, 2002; Sciote et al., 2003). Contraction velocity increases successively from type I  type IIA type IIX type IIB, while fatigability decreases in that order (e.g., Bottinelli et al., 1996). Large differences in fiber-type composition have been observed among individuals, muscle groups (jaw-closers vs. jaw-openers), individual muscles, and muscle regions (e.g., Serratrice et al., 1976; Vignon et al., 1980; Ringqvist et al., 1982; Eriksson and Thornell, 1983; Thornell et al., 1984; Shaughnessy et al., 1989; Sciote et al., 1994; Stål et al., 1994; Korfage and Van Eijden, 1999, 2000, 2003a; Korfage et al., 2000). These muscle groups, muscles, and muscle regions are assumed to be specialized for certain functions (e.g., Hannam and McMillan, 1994; Van Eijden et al., 1997; Van Eijden and Turkawski, 2001). It seems likely that such specialization is reflected in the fiber-type composition.
Muscle fibers have the ability to adapt to environmental alterations by changing from one fiber type into another (e.g., Adams et al., 1993; Oishi et al., 1998). For instance, in humans, during exercise against a load, the amount of IIX fibers decreases in favor of slower fiber types (Hather et al., 1991; Staron et al., 1994); in contrast, disuse of a muscle induces the conversion of type I fibers into type IIA fibers (Oishi et al., 1998).
Information about the relationship among jaw-muscle fiber-type composition, jaw-muscle functioning, and adaptation is limited. The purpose of this series of two review articles, therefore, is to discuss the current knowledge of the fiber-type composition in the jaw muscles, particularly in humans. A detailed knowledge of fiber-type composition, together with a thorough discussion of the concomitant functional and anatomical properties, increases our insight into the relationship between form and function in the jaw muscles and their adaptive capacity. The present (first) article is focused on the origin and functional significance of fiber-type diversity. The second article (Korfage et al., 2005) reviews the role of hybrid fibers and factors responsible for inter-individual variation in fiber-type composition.
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(1) MOTOR UNIT AND FIBER-TYPE PROPERTIES
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The functioning of the jaw muscles is highly dependent on the physiological properties of their motor units. [A motor unit is the combination of a single motoneuron and all the muscle fibers it innervates.] These properties, like their force output, fatigability, and contraction speed, vary considerably (Van Eijden and Turkawski, 2001). A motor unit’s ability to produce force is proportional to its cross-sectional area, which depends on the number and cross-sectional areas of the constituent muscle fibers. The ability to resist fatigue is dependent on the metabolic properties of the fibers. Muscle fibers of fatigue-resistant motor units contain a substantial amount of aerobic end-oxidation enzymes. In contrast, fibers of fatigable motor units are rich in glycolytic enzymes and low in enzymes of aerobic oxidative metabolism. The speed of motor unit contraction is largely dependent on the heavy-chain of the myosin protein in the muscle fibers.
Myosin Heavy-chain Isoforms and Contraction Speed
Sarcomeric myosin is a complex hexameric structure and is composed of 4 light-chain (MyLC) molecules (mol wt 16–20 kDa), named essential MyLC and regulatory MyLC, and 2 heavy-chain (MyHC) molecules (mol wt 200–220 kDa) (Fig. 1 ). The MyLC molecules play a part in the conversion of chemical energy into movement (Lowey et al., 1993). The MyHC subunit contains the ATPase activity that provides energy to generate force for muscle contraction. There are several isoforms (i.e., proteins which have the same function but are encoded by a different gene) of the MyHC molecule. In humans, these MyHC isoforms, which are encoded by a multigene family, are clustered at 2 distinct locations, 2 genes on chromosome 14 and 6 on chromosome 17 (Weiss et al., 1999). The MyHC isoform genes found in humans (Sartore et al., 1987; Butler-Browne et al., 1988; Smerdu et al., 1994; Stål et al., 1994; Weiss and Leinwand, 1996) include MyHC-cardiac  , MyHC-I (or -β), MyHC-IIA, MyHC-IIX, MyHC-IIB, MyHC-extra-ocular (expressed in the extrinsic eye and some pharyngeal muscles), and 2 developmental forms, namely, MyHC-fetal (also named MyHC-neonatal, -perinatal, or -developmental) and MyHC-embryonic. Although MyHC-cardiac is normally expressed in the atrium of the heart, and MyHC-fetal in developing muscles, they can both be expressed in some mature jaw muscles (e.g., Butler-Browne et al., 1988; Bredman et al., 1991; Monemi et al., 1996; Korfage et al., 2000). Not all MyHC genes are always translated into proteins. For example, mRNA encoding for MyHC-IIB is expressed abundantly in the human masseter, but its protein has not been found in this muscle (Horton et al., 2001). The MyHC isoforms are highly conserved among mammals. Similar isoforms were found among humans, rats, and mice.
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Figure 1. Diagram showing the level of organization within a skeletal muscle fiber, from single fiber to myofibrils, sarcomeres, actin and myosin myofilaments, and myosin molecule. The myosin molecule is composed of 4 light-chain (MyLC) molecules (2 essential and 2 regulatory) and 2 myosin heavy-chain (MyHC) subunits.
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Chromosomes 14 and 17 are not the only locations where genetic information is located for the isoforms of human MyHC. Recently, 3 new locations have been found, on chromosomes 3, 7, and 20, that decode for 3 novel MyHC isoforms (Desjardins et al., 2002). Two of these isoforms are structurally most like the slow MyHC-I, whereas the third one is closest to the MyHC-IIB isoform. This latter MyHC isoform (a product of the MYH 16 gene) is expressed in the jaw muscles of most primates (Stedman et al., 2004). However, in humans, this gene was inactivated by a frameshifting mutation, which is said to have occurred 2.4 million years ago, coinciding with the appearance of the modern human. The loss of this MyHC isoform has been suggested to lead to considerably smaller jaw muscles in humans than in other primates.
The different isoforms of MyHC are functionally unique and cannot be substituted for one another (Allen et al., 2000). The main difference between the MyHC isoforms is their rate of converting ATP into energy, which determines the speed of actin-myosin detachment. There is a good correlation between the MyHC isoforms and the maximum contraction velocity of fibers (Bottinelli et al., 1996). This velocity increases successively, from fibers that contain solely MyHC-I to those containing MyHC-IIA, MyHC-IIX, and MyHC-IIB. Using the slack-test technique (Edman, 1979), which determines unloaded shortening velocity (V0), investigators demonstrated that V0 is consistently about 10 times lower in MyHC-I fibers than in MyHC-IIX fibers; V0 for MyHC-IIB is approximately 20% higher than V0 for MyHC-IIX (Bottinelli et al., 1994). V0 of MyHC-IIA fibers is intermediate between MyHC-I and -IIX fibers, and V0 of hybrid fibers (see below) is intermediate between the relevant pure fiber types (Larsson and Moss, 1993; Bottinelli et al., 1996; Widrick et al., 1996). The contraction velocity of fibers co-expressing MyHC-cardiac is said to lie between the velocities of MyHC-I and MyHC-IIA fibers (Kwa et al., 1995; Sciote and Kentish, 1996); the contraction velocity of fibers expressing MyHC-fetal has not yet been determined unambiguously but seems to be low (D’Antona et al., 2003). Furthermore, it should be noted that the consumption rate of ATP is higher in fibers expressing the fast MyHC isoforms, and these fibers consume more energy than fibers expressing MyHC-I (He et al., 2000).
Muscle fibers do not always express just one MyHC isoform. Therefore, they can be divided into ‘pure’ fiber types, which express only one MyHC, and ‘hybrid’ fiber types, which express more than one MyHC isoform.
Classification of Motor Units and Muscle Fibers
Differences in contraction velocity and fatigability made it possible to classify motor units physiologically into different types, namely, S (slow-contracting, fatigue-resistant), FR (fast-contracting, fatigue-resistant), Fint (fast-contracting, intermediate fatigable), and FF (fast-contracting, fatigable) (Burke et al., 1971; Fournier and Sieck, 1988). The contractile speed is defined by the so-called ‘twitch contraction time’, i.e., the time necessary to build up force when a motor unit is elicited once. Slow units have a longer twitch contraction time than fast units. Fatigue is usually defined as a decline in force during tetanic stimulation. If the tetanic force of a motor unit declines relatively little, if at all, then the motor unit is called fatigue-resistant. If there is a relatively large decline, then the motor unit is called fatigable.
Most information on the physiological properties of motor units comes from animal experiments involving stimulation of single motoneurons of limb muscles by the insertion of an electrode into the motor nucleus. Therefore, the values obtained from these studies can be different from those in human jaw muscles. This kind of experiment cannot be performed in humans, because of the difficulty in accessing the motoneurons. Therefore, generally, motor unit and fiber properties are extrapolated from histochemical staining of muscle fiber samples. The ability to resist fatigue is related to the amounts of some metabolic enzymes, such as succinate dehydrogenase and citrate synthase. Enzyme histochemistry, therefore, makes it possible to identify and characterize individual slow- and fast-contracting muscle fibers based on these metabolic enzymes. Muscle fibers can then be classified into slow, oxidative (SO) fibers, which are recruited for slow, repetitive postural or chronic activity, and fast-contracting fibers, which are either oxidative and glycolytic (FOG), or glycolytic only (FG) (Barnard et al., 1971; Burke et al., 1971; Peter et al., 1972); this latter group of fibers is recruited for fast-phasic contractions.
Based on the distinct instabilities of the myofibrillar ATPase activity of the muscle fibers in alkaline (Guth and Samaha, 1970) and acidic media (Brooke and Kaiser, 1970), fibers were initially classified into type I (slow) and type II (fast) fibers. Further manipulation of the pH of the acidic media led to a subdivision of the type II fibers into fiber types IIA and IIB. By using a double pre-incubation, each at a different pH, investigators found that it was also possible to identify type IIX fibers (Santana Pereira et al., 1995). Some muscle fibers could not easily be classified by ATPase histochemistry into one of the aforementioned types, thereby resulting in subgroups, like IIC and IM (Ringqvist, 1971, 1973; Rowlerson et al., 1981; Eriksson et al., 1982). These fibers were found in muscles that were regenerating or in muscles that were subjected to exercise, but they were also found in large numbers in the jaw-closing muscles.
In the last few decades, a technique has been developed for the identification of proteins that could serve as a marker for the classification of muscle fibers (Fig. 2). Hybridoma cell lines can be used to raise antibodies against different MyHC isoforms. A strong correlation exists between contraction speed and MyHC isoform content at a single-fiber level (Bottinelli et al., 1999). It should be noted that, except for MyHC, MyLC and other muscle-specific proteins (e.g., sarcoplasmic reticulum Ca2+ ATPase, troponin subunits, -actinin) have fiber-type-specific isoforms that can modulate the contractile properties (these are not discussed in this article).
A different approach is to separate the muscle proteins by the use of high-glycerol-containing gels (Laemmli, 1970; Talmadge and Roy, 1993). With this technique, also known as SDS-PAGE, it is possible to separate the different MyHC isoforms (Fig. 3). Further, laser densitometry makes it possible to calculate the relative concentrations of the different isoforms in whole muscles or muscle portions, and in single hybrid fibers (Giulian et al., 1983; Korfage and Van Eijden, 2003a,b).
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Figure 3. Example of a cross-section of a fiber bundle from the anterior belly of the digastric muscle (A-D) and the electrophoresis results (E,F). (B-D) Magnifications of the indicated area in A after incubation with antibodies against MyHC-I (B), MyHC-IIA (C), and MyHC-IIA+IIX (D). Bar = 100 µm. (E) MyHC composition of this bundle as determined by gel electrophoresis. Only the MyHCs are shown. The plot obtained from laser densitometry (F) shows the integrated optical density of this particular fiber bundle.
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Classification based on the MyHC isoform expression, as detected by immunohistochemistry, is largely similar to the classification based on ATPase histochemistry. However, some problems are encountered in use of the ATPase technique. First, there are ambiguities related to, for example, the identification of gray fibers, the lack of reproducibility in different laboratories, and the nomenclature used. Second, ATPase-classified type IIB fibers are composed of 2 different MyHC isoforms. In mammals, these latter isoforms have been subdivided into MyHC-IIB and MyHC-IIX fibers (Schiaffino et al., 1989; DeNardi et al., 1993). Since this MyHC-IIX isoform is homologous with the human ATPase-classified type IIB fibers, it is thus more appropriate for these type IIB fibers to be denoted as MyHC-IIX fibers (Santana Pereira and Moorman, 1994). Third, with ATPase histochemistry, it is not possible to classify the whole spectrum of hybrid fibers that might occur in muscles. Finally, with ATPase histochemistry, it is not possible to distinguish fibers that express MyHC-fetal and/or MyHC-cardiac .
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(2) ADAPTATIONAL CAPACITY OF MUSCLE FIBERS
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As mentioned above, muscle fibers have the capacity to adapt to a new functional demand. The occurrence of adaptive changes has been related to a change in the amount and pattern of muscle activation and/or stretch. An increase in type I fibers has been reported after a long period of activation (Delp and Pette, 1994; Windisch et al., 1998) or electrical stimulation (Pette and Vrbová, 1992). Furthermore, a relationship has been demonstrated between the daily amount of muscle activation (the so-called ‘daily duty time’), and the proportion of type I fibers (Monster et al., 1978; Kernell et al., 1998). In contrast, a muscle will convert slower fibers into faster fibers during a period of reduced activity—for instance, during bedrest, space flight (Edgerton et al., 1995), or when a muscle is immobilized in a shortened position. Except for the amount of activation, the pattern of motoneuron activity has also been considered as an important factor for the regulation of fiber types (e.g., Hennig and Lømo, 1985; Gorassini et al., 1999, 2000; English and Widmer, 2003). It has been shown that motoneurons innervating fast fibers fire more rapidly and in shorter bursts than motoneurons innervating slow fibers. These properties are correlated with differences in the intrinsic properties of the motoneuron (Bakels and Kernell, 1993). It has been suggested that repeated, rapid high-amplitude Ca2+ transients in the sarcoplasma (Kubis et al., 2003), which occur during activation, play a role in the fast- to slow-fiber conversion. They will trigger the calcineurin signaling pathway that up-regulates slow-fiber-specific gene promoters (Chin et al., 1998).
However, activation is not the only influence. In experiments in which a muscle was fixed in a stretched position by a plaster cast (Yang et al., 1997), there was still a conversion from fast to slow fibers; this conversion was even stronger when the muscle was also subjected to electrical stimulation. During stretch, an increase in muscle IGF-I (Insulin Growth Factor-1) mRNA has been observed (Czerwinski et al., 1994; Goldspink et al., 1995). This particular IGF-I is a splice variant of the IGF-I gene found in the liver. The autocrine variant of IGF-I was cloned and named MGF (Mechano Growth Factor) (Yang et al., 1996; Goldspink, 1999). This protein increases the myoblast proliferation required for hypertrophy or repair (Yang and Goldspink, 2002). MGF was not detectable in dystrophic mdx muscles, even during stretch and stretch combined with electrical stimulation. Therefore, it was thought that the dystrophin cytoskeletal complex might be involved in the mechano-transduction mechanism. When this complex is defective, MGF and systemic growth factors are not produced, resulting in the ensuing cell death and in a progressive loss of muscle mass. In contrast, when the cDNA of MGF is introduced into murine muscle fibers, an increase in mass is achieved (Goldspink, 2003). It must be noted that the calcineurin and MGF models can account for the regulation of only slow fibers, and that fast MyHC expression is not really considered by these models. For a more extensive review of various aspects of muscle plasticity, we refer the reader to several recent publications (e.g., Roy et al., 1991; Hamilton and Booth, 2000; Baldwin and Haddad, 2001). In the companion article (Korfage et al., 2005), the authors discuss, in more detail, the effects of hormones on the adaptational capacity of muscle fibers.
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(3) DISTRIBUTION OF FIBER TYPES IN HUMAN JAW MUSCLES
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There are several studies on the various aspects of fiber-type composition of the human jaw muscles (e.g., Johnson et al., 1973; Ringqvist, 1973, 1974; Serratrice et al., 1976; Vignon et al., 1980; Eriksson et al., 1981, 1982; Ringqvist et al., 1982; Eriksson and Thornell, 1983; Thornell et al., 1984; Shaughnessy et al., 1989; Sciote et al., 1994; Stål et al., 1994; Korfage and Van Eijden, 1999, 2000, 2003a; Korfage et al., 2000). Many differences have been found in the fiber-type composition between and within the jaw muscles. In the following, we will summarize these differences and discuss possible explanations for them.
Intermuscular Differences in Fiber-type Composition
The fiber-type composition of the jaw-closing muscles (including the lateral pterygoid) differs from that of the jaw-opening muscles. A comparison of these muscle groups showed that about 70% of all fibers (pure + hybrid) in the jaw-closers expressed MyHC-I, while this isoform was expressed in about 40–45% of all fibers in the jaw-openers (Korfage et al., 2001). The jaw-closers contained fewer fibers that expressed MyHC-IIA (about 30%) than did the jaw-openers (about 50%). Moreover, the jaw-closers contained 40% hybrid fibers, while the jaw-openers contained only 10% hybrid fibers. Many of these hybrid fibers co-expressed MyHC-fetal (about 10% of the hybrid fibers) and/or MyHC-cardiac (about 30% of the hybrid fibers), which are normally not present in limb and trunk muscles. Thus, the jaw-closing muscles seem more adapted to perform slow, tonic movements and to produce a smooth, gradable force. The jaw-opening muscles, in contrast, seem to be more adapted to produce faster, phasic movements.
The differences in fiber-type composition between the jaw-closer and jaw-opener muscle groups suggest a difference in the amount of daily activity. The higher proportion of slow fibers in the jaw-closing muscles indicates that they could have a higher ‘daily duty time’ than the jaw-openers—for instance, in maintaining the mandible in its resting postural position against gravity (Kitagawa et al., 2002). In extreme cases, like bruxism, the duration of activation might be longer than in normal individuals, which, in turn, might increase the formation of MyHC-I even further. Therefore, it can be expected that these patients will have a higher proportion of type I fibers. To date, there are no studies in which the daily activity of the muscle groups has been compared. Presently, our research group is studying the relationship between daily activity and fiber-type composition using the jaw muscles of the rabbit as an experimental model (Langenbach et al., 2002, 2004; Van Wessel et al., 2005). Preliminary results show that the digastric muscle of the rabbit has a higher ‘daily duty time’, and a larger proportion of MyHC type I fibers, than does the masseter. Studies in which the activity of the jaw muscles are monitored for 24 hrs could confirm this relationship in humans.
The differences in fiber-type composition between jaw-closers and jaw-openers could also be related to the amount of stretch, which could be larger in jaw-closing muscles than in jaw-opening muscles. The jaw-closing muscles consist of shorter fibers than the jaw-opening muscles (Van Eijden et al., 1997) and, therefore, might experience more stretch than the jaw-opening muscle fibers. We speculate that this stretch would cause an up-regulation of the MGF, and thus a conversion from fast- to slow-type fibers. However, it is not known if this up-regulation of MGF indeed occurs.
The fiber-type compositions of muscles within a particular muscle group also differ. We found that the fiber-type composition varied significantly between different jaw-closers (Korfage et al., 2000). The most deviant pattern was observed for the temporalis muscle. This muscle contained more MyHC type I and type IIA fibers and fewer hybrid fibers than the masseter and the medial pterygoid muscles; compared with the other jaw-closers, the fibers in the temporalis had the largest cross-sectional areas. These differences suggest that the temporalis is slower than the other jaw-closers and that, because of its thicker fibers, it may experience more resistance. Generally, the jaw-openers do not differ much from each other in fiber-type composition or fiber cross-sectional area (Korfage et al., 2000). Only the bellies of the digastric are significantly different from each other, i.e., the anterior belly has considerably more MyHC type IIX fibers than the posterior belly, which has more MyHC type IIA fibers. This difference suggests that the bellies have the potential to act independently.
Differences in activation and/or stretch might also explain the different fiber-type compositions of muscles within a particular muscle group. Because of differences in ‘neural drive’, the muscles in a particular muscle group could differ in ‘daily duty times’, and because of differences in architecture and/or positions in the leverage system of the jaw, they can experience different amounts of stretch than could another muscle from the same group.
Heterogeneity in Fiber-type Composition within a Muscle
There also exists an intramuscular heterogeneity in fiber-type composition, particularly in the jaw-closing muscles. Such a heterogeneity could have a genetic basis. Generally, deep and anterior muscle portions contain more type I fibers than do superficial and posterior muscle portions (Johnson et al., 1973; Eriksson and Thornell, 1983; Korfage et al., 2000). But even within the main portions of the muscles, there is a finer regional difference in fiber-type distribution [(temporalis) Korfage and Van Eijden, 1999; (pterygoids) Korfage and Van Eijden, 2000]. In the temporalis, for example, the relative amount of MyHC type I fibers increases gradually as one proceeds in an anterior direction. This gradual change is in line with the fine regional differences in activation that have been reported for various motor tasks (Blanksma and Van Eijden, 1990, 1995; Blanksma et al., 1997).
In addition to genetic factors, activation- and stretch-related fiber-type adaptation might contribute to the heterogeneity within a muscle. For example, with respect to the temporalis, the longer moment arm of the anterior muscle portions makes these portions more advantageous for jaw-closing than do the posterior muscle portions (Van Eijden et al., 1996, 1997). In addition, because of their vertical direction of pull, the anterior muscle portions can be effectively used in more motor tasks than can the posterior muscle portions. Thus, from a mechanical point of view, it can be expected that the anterior portions are activated more frequently than the posterior portions. Indeed, this was observed in the EMG activity, as registered with fine-wire electrodes (Blanksma et al., 1997). A similar situation is found in the anterior muscle portion of the masseter. This muscle portion has a longer moment arm than does the posterior muscle portion. Thus, it seems more efficient to activate fibers in the anterior masseter to produce bite forces. Therefore, we speculate that the anterior portions of the temporalis and masseter are more frequently activated, which might lead to a higher proportion of MyHC type I fibers in these muscle portions.
In addition, architectural factors, such as the length of the muscle fibers and their position relative to the average rotation axis of the jaw, might contribute to the amount of stretch-related fiber-type adaptation. When the jaw is opened, muscle portions with a longer moment arm, like the anterior portions of the temporalis and masseter, undergo larger sarcomere excursions, and will thus be subjected to more stretch, than muscle portions with a shorter moment arm (Van Eijden and Raadsheer, 1992; Van Eijden et al., 1996). We speculate that this might result in an up-regulation of the MGF protein, which, in turn, might induce the fibers to express MyHC-I (Yang et al., 1997). Future experiments with antibodies staining MGF could resolve whether there is indeed a relation between the regional expression of MGF and that of MyHC type I within the jaw muscles.
Such heterogeneity in fiber-type expression cannot be observed in most of the jaw-opening muscles (Korfage et al., 2000). In general, the cross-sectional areas of these muscles and their attachment sites are relatively small. This makes it unlikely that different muscle portions of a particular muscle can execute different mechanical functions. It can thus be concluded that the jaw-opening muscles are, in general, functionally simpler than the jaw-closing muscles, with respect to activation, architecture, and fiber-type composition. However, there are also some studies indicating that these muscles do not function as a single entity. Work on the rabbit digastric, for example, points to a functional partitioning of this muscle (Tsuruyama et al., 2002).
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(4) WHY DO THE JAW MUSCLES HAVE DIFFERENT FIBER TYPES?
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Functional Significance of Fiber-type Diversity
The human jaw muscles participate in a large variety of motor tasks, including biting and mastication of food of different textures and sizes, swallowing, speech, singing, and yawning. These activities require a diversity of forces which must be maintained under various contraction velocities. To be able to perform the vast array of different tasks, the system must contain many different muscles.
Generally, muscles cannot be optimized simultaneously for each task. For example, a muscle that can contract at high speed cannot operate during a prolonged period, and vice versa. This requires a combination of fibers characterized by different physiological properties. For example, this combination may be composed, at the one extreme, of the slowest, most fatigue-resistant fibers and, at the other extreme, of the fastest, most fatigable fibers. The differences in fiber performance are the result of both qualitative modifications (e.g., myosin, troponin, and Ca2+ pump isoforms with different kinetic rates) and quantitative modifications (e.g., densities of sarcoplasmic reticulum and mitochondria) within the muscle fibers.
We speculate that the observed variety of MyHC isoforms in the jaw muscles could reflect the requirements of the masticatory system regarding the contraction velocities of the various muscle portions. As explained above, the contraction velocity of fibers depends on their MyHC contents. When high speeds of contraction are required, these speeds can be produced only by the fibers that contain the fastest MyHCs. Furthermore, fast fibers are capable of producing more isometric force and more power (force times velocity) than are slow fibers. Because of the force-velocity relationship, this difference will also be present at a similar speed of contraction.
An important advantage of the diversity in MyHCs is that these isoforms greatly help to optimize contractile function while minimizing energy use. The energetic cost of contractions is dependent on 2 components, i.e., the ATP used by Ca2+ pumps, and the ATP used by the cross-bridges. In humans, fast fibers have an ATP utilization approximately 4 times higher than that of slow fibers (Stienen et al., 1996). The tension cost, i.e., the ratio between expended energy and generated tension, is about 3 times lower for type I fibers than for type IIX fibers (Stienen et al., 1996). Slow fibers transfer energy more efficiently than do fast fibers (He et al., 2000), although they are less powerful. Hence, fast fibers are less suitable for efficiently powering movements that occur at low frequencies.
The fact that not one muscle fiber type can perform all activities effectively explains why the jaw muscles contain many fiber types. When a muscle is composed of one particular fiber type, it is optimized to perform one type of activity. However, this will reduce its ability to perform another type of activity. To achieve a wider repertoire of movement velocities, and to sustain different durations of activation, jaw muscles must use different fiber types. The more variation in fiber-type composition of a muscle, the larger is its potential role in different motor tasks.
Recruitment of Different Fiber Types
The presence of a variety of different muscle fibers optimized to perform different tasks would suggest a complex, organized nervous system where muscle fibers of different compositions are connected to different motoneurons. Fortunately, such a complex system is not necessary. Generally, a motoneuron is connected to several fibers of a similar type, to form a motor unit. Because the excitation threshold of a motor unit generally differs with its fiber types, only a relatively simple system is necessary.
In general, the recruitment of motor units follows the so-called ‘size principle’ (Henneman et al., 1965; Hennig and Lømo, 1985), i.e., they are recruited in order of increasing size, whether that is based on motoneuron soma size, axon caliber, or axonal conduction velocity. According to this principle, they are recruited sequentially and in a strict, hierarchical order (and de-recruited in the reverse sequence). The smallest, and slow, fatigue-resistant, motor units are recruited first. They produce small forces. With increasing force demands, the larger, faster, and more fatigable units join in. The largest, fastest, and most fatigable motor units are rarely used and are recruited only during maximal effort for brief periods of time. It is this hierarchy of motor unit recruitment order that governs the neural control of different fiber types within the same muscle, or muscle portions (Pette, 1990; Pette and Staron, 2000). Important implications of the orderly recruitment of motor units are that the slower fiber types are more frequently used than the faster ones, and that a finer modulation of force is possible at lower than at higher task intensities (Fig. 4). This finer modulation is due to the fact that small motor units produce less force than do large motor units, and that there are more small than large motor units (Kernell, 1992).
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Figure 4. Cumulative muscle force vs. number of recruited motor units. Based on Kernell (1992). The recruitment of motor units follows the size principle. According to this principle, the smallest (slow, fatigue-resistant) motor units are recruited first; these units produce relatively small forces. Therefore, for a small muscle force to be produced, a relatively large number of motor units is recruited. For muscle force to be increased, the larger (faster, less fatigable) units are recruited; these units produce larger forces, and thus, a relatively small number of motor units is recruited. As a consequence of the size principle, a finer modulation of muscle force is possible at lower than at higher muscle forces.
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The applicability of the size principle has not only been established for limb muscles, but has also been reported for various jaw-closing muscles [(human masseter and temporalis) Yemm, 1977; (human masseter) Desmedt and Godaux, 1979; Scutter and Türker, 1998; (monkey temporalis) Clark et al., 1978; (monkey masseter, temporalis and medial pterygoid) Lund et al., 1979]. It should be noted, however, that there are several studies suggesting that the jaw muscles contain many motor units which are not homogeneous with respect to fiber type (Kwa et al., 1995; Van Eijden and Turkawski, 2001). This makes the interpretation of fiber-type recruitment difficult. Muscle force is regulated not only by ‘recruitment gradation’ but also by ‘rate coding’, i.e., by variation in the rate of motor unit activation. Both strategies are used, although their relative contributions differ.
Related Recruitment of Jaw-muscle Fibers
A question that still needs to be answered is how jaw-muscle fibers with different properties are used during different tasks with widely varying demands. Similar to the situation in limb and trunk muscles (e.g., Gorassini et al., 2000; Wakeling et al., 2002), the different motor tasks of the jaw muscles are likely to be powered by different muscle fiber types. To produce a low speed for the mandible, or to produce sustained tension—for example, to resist gravity—the slow, fatigue-resistant fibers can be expected to be responsible for the majority of force production. Most of the force produced during mastication can also be expected to be the result of the activity of slow fatigue-resistant fibers, with a contribution from the faster fatigue-resistant ones. As mastication speed or force increases, additional fast, fatigue-resistant fibers will be recruited, with a small contribution of the fastest, more fatigable fibers. High muscle speed and/or power is presumably required for tasks such as speech or biting, resulting in the fastest fibers becoming a more important contributor to the speed or power produced by the muscles.
This view about the task-related recruitment of different jaw-muscle fiber types is rather speculative, however, and is based on sparse experimental data (McMillan and Hannam, 1992). If we are to understand the tremendous diversity of fibers and their recruitment, we should not study the properties of the jaw muscles without examining the entire jaw system, because one cannot appreciate why, for instance, the distribution of fiber types is as it is without examining the other components (joints, muscle moments, masses, kinematics of movement, motor tasks) to which it is adapted. There are, however, several obstacles to the integration of jaw-muscle fiber-type properties with mandibular movement and force production. First, there are more than 20 muscles or muscle portions that contribute to mandibular movement and force production. Because of this redundancy, the relative contributions of these muscles in performing a motor task are not a priori established (Van Eijden et al., 1990; Koolstra and Van Eijden, 2001). Therefore, it is difficult to identify and predict which particular muscle or muscle portion participates in a particular task, and to draw conclusions regarding mandibular movement and force production from the fiber-type composition of a single muscle. Second, thus far, there is a lack of studies in which the proportion of each fiber population, within a muscle, has been estimated to be active and at different tasks. Since slow muscle fibers are intermingled with various types of fast muscle fibers, it is very difficult to identify, experimentally, which fiber types are active during particular motor activities. Electromyographic electrodes will pick up signals from fibers of all types, making it nearly impossible to discriminate which fiber types are powering a particular movement or force. The only robust technique that has been used in mammals is to record the activation directly from the motoneurons, and to identify their fiber types at the conclusion of the experiment. However, this technique, which has been successfully done only in cats (Hoffer et al., 1987), is extremely difficult.
In conclusion, the fact that not one muscle fiber type can perform all activities effectively explains why the jaw muscles contain a diversity of fiber types. This diversity enables them to perform a large variety of motor tasks. The muscle fibers have the capacity to adapt to new functional demands, to optimize their contractile function. In the next article (Korfage et al., 2005), the role of hybrid fibers and inter-individual variations in fiber-type composition is discussed.
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ACKNOWLEDGMENTS
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This research was supported by the Interuniversity Research School of Dentistry, through the Academic Center of Dentistry Amsterdam. We are grateful to Peter Brugman for technical assistance.
Received for publication May 7, 2004.
Accepted for publication February 9, 2005.
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Journal of Dental Research, Vol. 84, No. 9,
774-783 (2005)
DOI: 10.1177/154405910508400901
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294 - 311.
[Abstract]
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S. Elworthy, M. Hargrave, R. Knight, K. Mebus, and P. W. Ingham
Expression of multiple slow myosin heavy chain genes reveals a diversity of zebrafish slow twitch muscle fibres with differing requirements for Hedgehog and Prdm1 activity
Development,
June 15, 2008;
135(12):
2115 - 2126.
[Abstract]
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ABSTRACT
INTRODUCTION