The relationships among jaw‐muscle fiber architecture,jaw morphology,and feeding behavior in extant apes and modern humans

The jaw‐closing muscles are responsible for generating many of the forces and movements associated with feeding. Muscle physiologic cross‐sectional area (PCSA) and fiber length are two architectural parameters that heavily influence muscle function. While there have been numerous comparative studies of hominoid and hominin craniodental and mandibular morphology, little is known about hominoid jaw‐muscle fiber architecture. We present novel data on masseter and temporalis internal muscle architecture for small‐ and large‐bodied hominoids. Hominoid scaling patterns are evaluated and compared with representative New‐ (Cebus) and Old‐World (Macaca) monkeys. Variation in hominoid jaw‐muscle fiber architecture is related to both absolute size and allometry. PCSAs scale close to isometry relative to jaw length in anthropoids, but likely with positive allometry in hominoids. Thus, large‐bodied apes may be capable of generating both absolutely and relatively greater muscle forces compared with smaller‐bodied apes and monkeys. Compared with extant apes, modern humans exhibit a reduction in masseter PCSA relative to condyle‐M₁ length but retain relatively long fibers, suggesting humans may have sacrificed relative masseter muscle force during chewing without appreciably altering muscle excursion/contraction velocity. Lastly, craniometric estimates of PCSAs underestimate hominoid masseter and temporalis PCSAs by more than 50% in gorillas, and overestimate masseter PCSA by as much as 30% in humans. These findings underscore the difficulty of accurately estimating jaw‐muscle fiber architecture from craniometric measures and suggest models of fossil hominin and hominoid bite forces will be improved by incorporating architectural data in estimating jaw‐muscle forces. Am J Phys Anthropol 151:120–134, 2013. © 2013 Wiley Periodicals, Inc.     

A cineradiographic and electromyographic study of mastication in Tenrec ecaudatus

Regular chewing was studied in the specialized Malagasy insectivore Tenrec ecaudatus with the aid of precisely correlated electromyography of the main adductors, digastrics, and two hyoid muscles and cineradiography for which metallic markers were placed in the mandibles, tongue, and hyoid bone. During the power stroke the body of the mandible moves dorsally and medially. The medially directed component of movement at this time is greatly increased by simultaneous rotation of the mandible about its longitudinal axis. The highly mobile symphysis, spherical dentary condyle, loss of superficial masseter muscle and zygoma, and the simplified zalamnodont molars all appear to be related to the large amount of mandibular rotation that occurs during occlusion. The balancing side lateral pterygoid muscle (inferior head) apparently shifts the working side mandible laterally during the last part of opening and the first part of closing. The working side temporalis and the superficial masseter muscle are both responsible for the shift back to the midline. The temporalis is usually active to the same extent on the working and balancing sides during the power stroke. The level of activity (amplitude) of the temporalis and duration of the power stroke increase with harder foods. Whenever soft foods are chewed, the superficial masseter is only active on the working side; whenever foods of increasing hardness are chewed, its level of activity on the balancing side increases to approach that of the working side. Mandibular rotation is greatly reduced when hard foods are chewed.     

Masticatory motor patterns in ungulates: a quantitative assessment of jaw-muscle coordination in goats, alpacas and horses

We investigated patterns of jaw-muscle coordination during rhythmic mastication in three species of ungulates displaying the marked transverse jaw movements typical of many large mammalian herbivores. In order to quantify consistent motor patterns during chewing, electromyograms were recorded from the superficial masseter, deep masseter, posterior temporalis and medial pterygoid muscles of goats, alpacas and horses. Timing differences between muscle pairs were evaluated in the context of an evolutionary model of jaw-muscle function. In this model, the closing and food reduction phases of mastication are primarily controlled by two distinct muscle groups, triplet I (balancing-side superficial masseter and medial pterygoid and working-side posterior temporalis) and triplet II (working-side superficial masseter and medial pterygoid and balancing-side posterior temporalis), and the asynchronous activity of the working- and balancing-side deep masseters. The three species differ in the extent to which the jaw muscles are coordinated as triplet I and triplet II. Alpacas, and to a lesser extent, goats, exhibit the triplet pattern whereas horses do not. In contrast, all three species show marked asynchrony of the working-side and balancing-side deep masseters, with jaw closing initiated by the working-side muscle and the balancing-side muscle firing much later during closing. However, goats differ from alpacas and horses in the timing of the balancing-side deep masseter relative to the triplet II muscles. This study highlights interspecific differences in the coordination of jaw muscles to influence transverse jaw movements and the production of bite force in herbivorous ungulates.     

The instantaneous center of rotation during human jaw opening and its significance in interpreting the functional meaning of condylar translation

Mandibular condyles translate back and forth during mouth closing and opening in primates and most other mammals. To account for the functional significance of this phenomenon, several hypotheses have been proposed. The sarcomere-length hypothesis holds that condylar translation provides a mechanical advantage by minimizing sarcomere-length changes in the masseter-medial pterygoid complex throughout a wide range of jaw openings. As the hypothesis is inherently associated with the locations of the instantaneous centers of rotation (ICRs) of the mandible, a more accurate determination of this variable would help test this hypothesis. This study investigated ICRs in the sagittal plane during human symmetrical mandibular opening based on a recently developed analytical method. The results confirmed that, with inter- and intraindividual variation, the natural opening was a simultaneous rotational and translational motion. In addition, the ICR was found to lie closer to the condyle during the first 10° than during the rest of the rotation. This suggests that for the condyles the rotational component is somewhat more significant at the early phase than at the late phase of the opening stroke. For the whole range of the natural opening, the grossly approximated centers of rotation (CRs) scattered below the palpable lateral condylar poles in the superior half of the ramus. This study supports neither the ICR path determined by Grant ([1973], J. Biomech. 6:109–113) nor the conclusions reached by recording manually operated jaw movements in human cadavers (Rees [1954] Br. Dent. J. 6:125–133). Moss's suggestion ([1960] Disorders of the Temporomandibular Joint (Philadelphia: W.B. Saunders), pp. 73–88) that the center of rotation lies at the lingula is also not confirmed. Although the new data cannot reject the sarcomere-length hypothesis, they do not strongly support it either. Another hypothesis is proposed in this study as plausible. With this hypothesis, translation is regarded as an adaptation to the use of the inferior head of the lateral pterygoid as a jaw depressor in noncarnivorous mammals. Potential functional advantages of this portion of the muscle are also discussed. Am J Phys Anthropol 106:35–46, 1998. © 1998 Wiley-Liss, Inc.     

Predicted pattern of human muscle activity during clenching derived from a computer assisted model: symmetric vertical bite forces

A computer assisted three-dimensional model of the jaw, based on linear programming, is presented. The upper and lower attachments of the muscles of mastication have been measured on a single human skull and divided into thirteen independent units on each side--a total of 26 muscle elements. The direction (in three dimensions) and maximum forces that could be developed by each muscle element, the bite reaction and two joint reactions are included in the model. It is shown for symmetrical biting that a model which minimizes the sum of the muscle forces used to produce a given bite force activates muscles in a way which corresponds well with previous observations on human subjects. A model which minimizes the joint reactions behaves differently and is rejected. An analysis of the way the chosen model operates suggests that there are two types of jaw muscles, power muscles and control muscles. Power muscles (superficial masseter, medial pterygoid and some of temporalis) produce the bite force but tend to displace the condyle up or down the articular eminence. This displacement is prevented by control muscles (oblique temporalis and lateral pterygoid) which have very poor moment arms for generating usual bite forces, but are efficient for preventing condylar slide. The model incorporates the concept that muscles consist of elements which can contract independently. It predicts that those muscle elements with longer moment arms relative to the joint are the first to be activated and, as the bite force increases, a ripple of activity spreads into elements with shorter moment arms. In general, the model can be used to study the three-dimensional activity in any system of joints and muscles.     

Morphological and videofluorographic study of the hyoid apparatus and its function in the rabbit (Oryctolagus cuniculus)

The anatomy of the hyoid apparatus and positional changes of the hyoid bone during mastication and deglutition are described in the New Zealand White rabbit (Oryctolagus cuniculus). A testable model is constructed to predict the range of movement during function of the hyoid, a bone entirely suspended by soft tissue. Frame-by-frame analysis of a videofluorographic tape confirms the accuracy of the prediction through observation of hyoid bone excursion during oral behavior. During chewing, translation of the hyoid bone is diminutive and irregular, lacking a clearly discernible path of excursion. However, some movements of the hyoid occur with regularity. During fast opening, anterodorsal movement of the hyoid is interrupted with an abrupt posteroventral depression when the bolus is moved posteriorly toward the cheek teeth by the tongue. This clockwise rotation (when viewed from the right side) of the hyoid accompanies jaw opening and is reversed (posteroventral movement) for the jaw closing sequence. Lateral movements of the hyoid may be slightly coupled to mandibular rotation in the horizontal plane. The findings suggest that the hyoid bone maintains a relatively static position during the dynamics of chewing. The primary function would be to provide a stable base for the movements of the tongue. Another possible function would be to control the position of the larynx within the pharyngeal cavity. Some characteristic features of the rabbit hyoid apparatus may be consequential to relatively erect posture and a saltatory mode of locomotion.     

Electromyography and mechanics of mastication in the albino rat.

The masticatory apparatus in the albino rat was studied by means of electromyography and subsequent estimation of muscular forces. The activity patterns of the trigeminal and suprahyoid musculature and the mandibular movements were recorded simultaneously during feeding. The relative forces of the individual muscles in the different stages of chewing cycles and biting were estimated on the basis of their physiological cross sections and their activity levels, as measured from integrated electromyograms. Workinglines and moment arms of these muscles were determined for different jaw positions. In the anteriorly directed masticatory grinding stroke the resultants of the muscle forces at each side are identical; they direct anteriorly, dorsally and slightly lingually and pass along the lateral side of the second molar. Almost the entire muscular resultant force is transmitted to the molars while the temporo-mandibular joint remains unloaded. A small transverse force, produced by the tense symphyseal cruciate ligaments balances the couple of muscle resultant and molar reaction force in the transverse plane. After each grinding stroke the mandible is repositioned for the next stroke by the overlapping actions of three muscle groups: the pterygoids and suprahyoids produce depression and forward shift, the suprahyoids and temporal backward shift and elevation of the mandible while the subsequent co-operation of the temporal and masseter causes final closure of the mouth and starting of the forward grinding movement. All muscles act in a bilaterally symmetrical fashion. The pterygoids contract more strongly, the masseter more weakly during biting than during chewing. The wide gape shifts the resultant of the muscle forces more vertically and moreposteriorly. The joint then becomes strongly loaded because the reaction forces are applied far anteriorly on the incisors. The charateristic angle between the almost horizontal biting force and the surface of the food pellet indicates that the lower incisors produce a chisel-like action. Tooth structure reflects chewing and biting forces. The transverse molar lamellae lie about parallel to the chewing forces whereas perpendicular loading of the occlusal surfaces is achieved by their inclination in the transverse plane. The incisors are loaded approximately parallel to their longitudinal axis, placement that avoids bending forces during biting. It is suggested that a predominantly protrusive musculature favors the effective force transmission to the lower incisors, required for gnawing. By grinding food across transversely oriented molar ridges the protrusive components of the muscles would be utilized best. From the relative weights of the masticatory muscles in their topographical relations with joints, molars and incisors it may be concluded that the masticatory apparatus is a construction adapted to optimal transmission of force from muscles to teeth.     

Mastication and the postorbital ligament: dynamic strain in soft tissues

Although the FEED database focuses on muscle activity patterns, it is equally suitable for other physiological recording and especially for synthesizing different types of information. The present contribution addresses the interaction between muscle activity and ligamentary stretch during mastication. The postorbital ligament is the thickened edge of a septum dividing the orbital contents from the temporal fossa and is continuous with the temporal fascia. As a tensile element, this fascial complex could support the zygomatic arch against the pull of the masseter muscle. An ossified postorbital bar has evolved repeatedly in mammals, enabling resistance to compression and shear in addition to tension. Although such ossification clearly reinforces the skull against muscle pull, the most accepted explanation is that it helps isolate the orbital contents from contractions of the temporalis muscle. However, it has never been demonstrated that the contraction of jaw muscles deforms the unossified ligament. We examined linear deformation of the postorbital ligament in minipigs, Sus scrofa, along with electromyography of the jaw muscles and an assessment of changes in pressure and shape in the temporalis. During chewing, the ligament elongated (average 0.9%, maximum 2.8%) in synchrony with the contraction of the elevator muscles of the jaw. Although the temporalis bulged outward and created substantial pressure against the braincase, the superficial fibers usually retracted caudally, away from the postorbital ligament. In anesthetized animals, stimulating either the temporalis or the masseter muscle in isolation usually elongated the ligament (average 0.4-0.7%). These results confirm that contraction of the masticatory muscles can potentially distort the orbital contents and further suggest that the postorbital ligament does function as a tension member resisting the pull of the masseter on the zygomatic arch.     

Symphyseal fusion and jaw-adductor muscle force: an EMG study

The purpose of this study is to test various hypotheses about balancing-side jaw muscle recruitment patterns during mastication, with a major focus on testing the hypothesis that symphyseal fusion in anthropoids is due mainly to vertically- and/or transversely-directed jaw muscle forces. Furthermore, as the balancing-side deep masseter has been shown to play an important role in wishboning of the macaque mandibular symphysis, we test the hypothesis that primates possessing a highly mobile mandibular symphysis do not exhibit the balancing-side deep masseter firing pattern that causes wishboning of the anthropoid mandible. Finally, we also test the hypothesis that balancing-side muscle recruitment patterns are importantly related to allometric constraints associated with the evolution of increasing body size. Electromyographic (EMG) activity of the left and right superficial and deep masseters were recorded and analyzed in baboons, macaques, owl monkeys, and thick-tailed galagos. The masseter was chosen for analysis because in the frontal projection its superficial portion exerts force primarily in the vertical (dorsoventral) direction, whereas its deep portion has a relatively larger component of force in the transverse direction. The symphyseal fusion-muscle recruitment hypothesis predicts that unlike anthropoids, galagos develop bite force with relatively little contribution from their balancing-side jaw muscles. Thus, compared to galagos, anthropoids recruit a larger percentage of force from their balancing-side muscles. If true, this means that during forceful mastication, galagos should have working-side/balancing-side (W/B) EMG ratios that are relatively large, whereas anthropoids should have W/B ratios that are relatively small. The EMG data indicate that galagos do indeed have the largest average W/B ratios for both the superficial and deep masseters (2.2 and 4.4, respectively). Among the anthropoids, the average W/B ratios for the superficial and deep masseters are 1.9 and 1.0 for baboons, 1.4 and 1.0 for macaques, and both values are 1.4 for owl monkeys. Of these ratios, however, the only significant difference between thick-tailed galagos and anthropoids are those associated with the deep masseter. Furthermore, the analysis of masseter firing patterns indicates that whereas baboons, macaques and owl monkeys exhibit the deep masseter firing pattern associated with wishboning of the macaque mandibular symphysis, galagos do not exhibit this firing pattern. The allometric constraint-muscle recruitment hypothesis predicts that larger primates must recruit relatively larger amounts of balancing-side muscle force so as to develop equivalent amounts of bite force. Operationally this means that during forceful mastication, the W/B EMG ratios for the superficial and deep masseters should be negatively correlated with body size. Our analysis clearly refutes this hypothesis. As already noted, the average W/B ratios for both the superficial and deep masseter are largest in thick-tailed galagos, and not, as predicted by the allometric constraint hypothesis, in owl monkeys, an anthropoid whose body size is smaller than that of thick-tailed galagos. Our analysis also indicates that owl monkeys have W/B ratios that are small and more similar to those of the much larger-sized baboons and macaques. Thus, both the analysis of the W/B EMG ratios and the muscle firing pattern data support the hypothesis that symphyseal fusion and transversely-directed muscle force in anthropoids are functionally linked. This in turn supports the hypothesis that the evolution of symphyseal fusion in anthropoids is an adaptation to strengthen the symphysis so as to counter increased wishboning stress during forceful unilateral mastication. (ABSTRACT TRUNCATED)     

Mastication in springhares,Pedetes capensis: A cineradiographic study

Analysis of lateral and dorsoventral radiographic films shows that ingestion, transport, and mastication in Pedetes capensis (Rodentia) are cyclic and their movement patterns are essentially similar for the three food types offered. During the ingestion cycle, closing of the mouth is accompanied by a backward translation of the condyles, so that movement is predominantly orthal. During the opening stage, the extent of the anterior condylar translation is smaller. As a result the mandibular incisors move ventrally and posteriorly. During the ingestion cycles, food is transported to the back of the tongue, with the transverse rugae and the folds of the upper lip playing important roles. Springhares show a bilateral masticatory pattern; food is chewed on both sides simultaneously. During chewing, the condyles lie in their most forward position at maximum opening of the mouth. The mouth is closed by rotation of the lower jaw around the temporomandibular joint coupled with posterior condylar translation. At the beginning of the slow-closing stage, the upward rotation of the mandible slows and the jaw slowly shifts forward. During the grinding stage, the mandible is shifted forward with both toothrows in occlusion. During the opening stage, the jaw returns to its starting position. Comparison of kinematic and anatomical data on rodent mastication suggests that some dental characteristics form the most important factors regulating the masticatory pattern and consequently allow reasonably reliable prediction of rodent masticatory patterns.     

Contour analysis of masticatory jaw movements and muscle activity in Macaca mulatta

Frontal plane mandibular movements during mastication and the associated electromyographic (EMG) activity for left and right superficial masseter, posterior temporalis, anterior temporalis, and anterior belly of the digastric (ABD) were studied for two adult male Macaca mulatta by the new technique of “contour” analysis. Contour analysis allowed graphic and quantitative portrayal of multiple chew cycle patterns of mandibular movement and EMG activity during active mastication. A series of computer programs (ATS, ATSED, ATSXYZ) facilitated the collection, editing and definition, and finally processing of these masticatory data into contour plots. These preliminary data indicated the essential symmetry of mandibular movement patterns, high chew cycle variability inferior to occlusion, multiple centers of intense EMG activity for balancing-side superficial masseter, and no difference between working-side anterior and posterior temporalis EMG patterns. Maximum EMG amplitude was found in the area of buccal phase power stroke (BPS). Maximum EMG amplitude for ABD was located medial and inferior to occlusion; all other muscle maximum amplitudes were buccal and inferior to occlusion. The location of maximum EMG amplitudes for superficial masseter and ABD were closer to occlusion (more superior) during mastication of carrot than were maximum amplitudes during biscuit mastication. The absence of any detectable shift of EMG maximum amplitude location between biscuit and carrot for posterior and anterior temporalis suggested, along with the continuous EMG activity of working-side posterior temporalis, a secondary role for the temporalis (compensation for superficial masseter activity) during active mastication.     

Comparative analysis of masseter fiber architecture in tree-gouging (Callithrix jacchus) and nongouging (Saguinus oedipus) callitrichids

Common marmosets (Callithrix jacchus) and cotton-top tamarins (Saguinus oedipus) (Callitrichidae, Primates) share a broadly similar diet of fruits, insects, and tree exudates. Common marmosets, however, differ from tamarins by actively gouging trees with their anterior teeth to elicit tree exudate flow. During tree gouging, marmosets produce relatively large jaw gapes, but do not necessarily produce relatively large bite forces at the anterior teeth. We compared the fiber architecture of the masseter muscle in tree-gouging Callithrix jacchus (n = 10) to nongouging Saguinus oedipus (n = 8) to determine whether the marmoset masseter facilitates producing these large gapes during tree gouging. We predict that the marmoset masseter has relatively longer fibers and, hence, greater potential muscle excursion (i.e., a greater range of motion through increased muscle stretch). Conversely, because of the expected trade-off between excursion and force production in muscle architecture, we predict that the cotton-top tamarin masseter has more pinnate fibers and increased physiological cross-sectional area (PCSA) as compared to common marmosets. Likewise, the S. oedipus masseter is predicted to have a greater proportion of tendon relative to muscle fiber as compared to the common marmoset masseter. Common marmosets have absolutely and relatively longer masseter fibers than cotton-top tamarins. Given that fiber length is directly proportional to muscle excursion and by extension contraction velocity, this result suggests that marmosets have masseters designed for relatively greater stretching and, hence, larger gapes. Conversely, the cotton-top tamarin masseter has a greater angle of pinnation (but not significantly so), larger PCSA, and higher proportion of tendon. The significantly larger PCSA in the tamarin masseter suggests that their masseter has relatively greater force production capabilities as compared to marmosets. Collectively, these results suggest that the fiber architecture of the common marmoset masseter is part of a suite of features of the masticatory apparatus that facilitates the production of relatively large gapes during tree gouging.     

The growth of the skull and jaw muscles and its functional consequences in the New Zealand rabbit (Oryctolagus cuniculus)

Between weaning and adulthood, the length and height of the facial skull of the New Zealand rabbit (Oryctolagus cuniculus) double, whereas much less growth occurs in the width of the face and in the neurocranium. There is a five-fold increase in mass of the masticatory muscles, caused mainly by growth in cross-sectional area. The share of the superficial masseter in the total mass increases at the cost of the jaw openers. There are changes in the direction of the working lines of a few muscles. A 3-dimensional mechanical model was used to predict bite forces at different mandibular positions. It shows that young rabbits are able to generate large bite forces at a wider range of mandibular positions than adults and that the forces are directed more vertically. In young and adult animals, the masticatory muscles differ from each other with respect to the degree of gape at which optimum sarcomere length is reached. Consequently, bite force can be maintained over a range of gapes, larger than predicted on basis of individual length-tension curves. Despite the considerable changes in skull shape and concurrent changes in the jaw muscles, the direction of the resultant force of the closing muscles and its mechanical advantage remain stable during growth. Observed phenomena suggest that during development the possibilities for generation of large bite forces are increased at the cost of a restriction of the range of jaw excursion.     

A preliminary analysis of correlations between chewing motor patterns and mandibular morphology across mammals

The establishment of a publicly-accessible repository of physiological data on feeding in mammals, the Feeding Experiments End-user Database (FEED), along with improvements in reconstruction of mammalian phylogeny, significantly improves our ability to address long-standing questions about the evolution of mammalian feeding. In this study, we use comparative phylogenetic methods to examine correlations between jaw robusticity and both the relative recruitment and the relative time of peak activity for the superficial masseter, deep masseter, and temporalis muscles across 19 mammalian species from six orders. We find little evidence for a relationship between jaw robusticity and electromyographic (EMG) activity for either the superficial masseter or temporalis muscles across mammals. We hypothesize that future analyses may identify significant associations between these physiological and morphological variables within subgroups of mammals that share similar diets, feeding behaviors, and/or phylogenetic histories. Alternatively, the relative peak recruitment and timing of the balancing-side (i.e., non-chewing-side) deep masseter muscle (BDM) is significantly negatively correlated with the relative area of the mandibular symphysis across our mammalian sample. This relationship exists despite BDM activity being associated with different loading regimes in the symphyses of primates compared to ungulates, suggesting a basic association between magnitude of symphyseal loads and symphyseal area among these mammals. Because our sample primarily represents mammals that use significant transverse movements during chewing, future research should address whether the correlations between BDM activity and symphyseal morphology characterize all mammals or should be restricted to this "transverse chewing" group. Finally, the significant correlations observed in this study suggest that physiological parameters are an integrated and evolving component of feeding across mammals.     

An electromyographic analysis of the biting mechanism of the lemon shark,Negaprion Brevirostris: Functional and evolutionary implications

The kinetics of the head and function of select jaw muscles were studied during biting behavior in the lemon shark, Negaprion brevirostris. High speed cinematography and electromyography of seven cranial muscles were recorded during bites elicited by a probe to the oral cavity. In weak bites mandible depression was followed by mandible elevation and jaw closure without cranial elevation. In strong bites cranial elevation always preceded lower jaw depression, lower jaw elevation, and cranial depression. The average duration of the strong bites was rapid (176 msec), considering the size of the animal relative to other fishes. Different electromyographic patterns distinguished the two forms of bite, primarily in activity of the epaxial muscles, which effect cranial elevation. A composite reconstruction of the activity of seven cranial muscles during biting revealed that epaxial muscle activity and consequently cranial elevation preceded all other muscle activity. Mandible depression was primarily effected by contraction of the common coracoarcual and coracomandibularis, with assistance by the coracohyoideus. Simultaneous activity of the levator hyomandibulae is believed to increase the width of the orobranchial chamber. The adductor mandibulae dorsal was the primary jaw adductor assisted by the adductor mandibulae ventral. This biomechanically conservative mechanism for jaw opening in aquatic vertebrates is conserved, with the exception of the coracomandibularis, which is homologous to prehyoid muscles of salamanders.     

Masseter electromyography during chewing in ring-tailed lemurs (Lemur catta)

We examined masseter recruitment and firing patterns during chewing in four adult ring-tailed lemurs (Lemur catta), using electromyography (EMG). During chewing of tougher foods, the working-side superficial masseter tends to show, on average, 1.7 times more scaled EMG activity than the balancing-side superficial masseter. The working-side deep masseter exhibits, on average, 2.4 times the scaled EMG activity of the balancing-side deep masseter. The relatively larger activity in the working-side muscles suggests that ring-tailed lemurs recruit relatively less force from their balancing-side muscles during chewing. The superficial masseter working-to-balancing-side (W/B) ratio for lemurs overlaps with W/B ratios from anthropoid primates. In contrast, the lemur W/B ratio for the deep masseter is more similar to that of greater galagos, while both are significantly larger than W/B ratios of anthropoids. Because ring-tailed lemurs have unfused and hence presumably weaker symphyses, these data are consistent with the symphyseal fusion-muscle recruitment hypothesis stating that symphyseal fusion in anthropoids provides increased strength for resisting forces created by the balancing-side jaw muscles during chewing. Among the masseter muscles of ring-tailed lemurs, the working-side deep masseter peaks first on average, followed in succession by the balancing-side deep masseter, balancing-side superficial masseter, and finally the working-side superficial masseter. Ring-tailed lemurs are similar to greater galagos in that their balancing-side deep masseter peaks well before their working-side superficial masseter. We see the opposite pattern in anthropoids, where the balancing-side deep masseter peaks, on average, after the working-side superficial masseter. This late activity of the balancing-side deep masseter in anthropoids is linked to lateral-transverse bending, or wishboning, of their mandibular symphyses. Subsequently, the stresses incurred during wishboning are hypothesized to be a proximate reason for strengthening, and hence fusion, of the anthropoid symphysis. Thus, the absence of this muscle-firing pattern in ring-tailed lemurs with their weaker, unfused symphyses provides further correlational support for the symphyseal fusion late-acting balancing-side deep masseter hypothesis linking wishboning and symphyseal strengthening in anthropoids. The early peak activity of the working-side deep masseter in ring-tailed lemurs is unlike galagos and most similar to the pattern seen in macaques and baboons. We hypothesize that this early activity of the working-side deep masseter moves the lower jaw both laterally toward the working side and vertically upward, to position it for the upcoming power stroke. From an evolutionary perspective, the differences in peak firing times for the working-side deep masseter between ring-tailed lemurs and greater galagos indicate that deep masseter firing patterns are not conserved among strepsirrhines.     

Complexity of ruminant masticatory evolution

The evolution of robust jaws, hypsodont teeth, and large chewing muscles among grazing ruminants is a quintessential example of putative morphological adaptation. However, the degree of correlated evolution (i.e., to what extent the grazer feeding apparatus represents an evolutionary module), especially of soft and hard tissues, remains poorly understood. Recent generation of large datasets and phylogenetic information has made testing hypotheses of correlated evolution possible. We, therefore, test for correlated evolution among various traits of the ruminant masticatory apparatus including tooth crown height, jaw robustness, chewing muscle size, and characters of the molar occlusal surfaces, using phylogenetic and nonphylogenetic comparative methods as well as phylogenetic evolutionary model selection. We find that the large masseter muscles of grazing ruminants evolved with the inclusion of grass in the diet, an increase in the proportion of occlusal enamel bands oriented parallel to the chewing stroke, and possibly hypsodonty. We suggest that the masseter evolved under two evolutionary regimes: i) selection for higher masticatory forces during chewing and ii) flattening of the tooth profile, which resulted in reduced tooth guidance and, thus, a requirement for more chewing muscle activity during each chewing stroke, in agreement with previous research. The linear jaw metrics (depth of the mandibular angle, mandibular angle width, and length of the superficial masseteric scar) all show correlated evolution with hypsodonty and the proportion of enamel bands oriented parallel to the chewing stroke. We suggest that changes in the shape of the mandible represent the combined effects of selection for a reorientation of the chewing stroke, so as to emphasize horizontal translation of the teeth, and accommodation of high‐crowned teeth. Our analyses show that the ruminant feeding apparatus is an evolutionary mosaic with its various components showing both correlated and independent evolution. J. Morphol. 275:1093–1102, 2014. © 2014 Wiley Periodicals, Inc.     

Jaw muscle functional anatomy in northern grasshopper mouse, Onychomys leucogaster, a carnivorous murid

The jaw muscle anatomy of the northern grasshopper mouse, Onychomys leucogaster, was observed and the mechanical basis of the insectivorous/carnivorous adaptations were examined. Compared with Peromyscus maniculatus, a granivorous relative of Onychomys, there is a reduction of some aponeuroses within the masseter deep layer. This characteristic indicates that shearing meat or crushing arthropod exoskeletons requires less occlusal pressure than does grinding plant material. In Onychomys both the anterior and posterior portions of the masseter deep layer are more anterodorsally inclined, so that the line of action of the masseter lies further from the jaw joint than in Peromyscus. A strong incisal bite for killing vertebrates such as other rodents can be produced by a jaw mechanism with the high lever advantage of this muscle, which compensates for the decline in muscle mass. Our quantitative analysis suggests that the disappearance of an aponeurosis along the zygomatic plate in Onychomys decreases the stretch of the corresponding muscle, i.e., the anterior fibers of the masseter deep layer, accompanying jaw opening, and increases the maximum gape necessary for hunting large prey.     

Muscle force recruitment and biomechanical modeling: an analysis of masseter muscle function during mastication in Macaca fascicularis.

The main purpose of this study is to test the hypothesis that as subjects chew with increasing levels of force, the ratio of the working- to balancing-side jaw-muscle force (W/B) decreases and begins to approach 1.0. We did this by analyzing relative masseter force in Macaca fascicularis using both strain gage and surface electromyographic (EMG) techniques. In addition, we also analyzed: 1) the relationship between jaw position using cineradiographic techniques and relative masseter force, 2) the timing differences between relative masseter force from the working and balancing sides, and 3) the loading and unloading characteristics of the masseter muscle. Our findings indicate that when macaques increase the amount of overall masticatory force during chewing, the W/B ratio for masseter force frequently (but not always) decreases and begins to approach 1.0. Therefore, our working hypothesis is not completely supported because the W/B ratio does not decrease with increasing levels of force in all subjects. The data also demonstrate timing differences in masseter force. During apple-skin mastication, the average peak masseter force on the working side occurs immediately at or slightly after the initial occurrence of maximum intercuspation, whereas the average peak masseter force on the balancing side occurs well before maximum intercuspation. On average, we found that peak force from the balancing-side masseter precedes the working-side masseter by about 26 msec. The greater the asynchrony between working- and balancing-side masseter force, the greater the difference in the relative magnitude of these forces. For example, in the subject with the greatest asynchrony, the balancing-side masseter had already fallen to about one-half of peak force when the working-side masseter reached peak force. Our data also indicate that the loading and unloading characteristics of the masseter differ between the working and balancing sides. Loading (from 50 to 100% of peak force) and unloading (from 100 to 50% of peak force) for the balancing-side masseter tends to be rather symmetrical. In contrast, the working-side masseter takes much longer to load from 50 to 100% of peak force than it does to unload from 100 to 50% of peak force. Finally, it takes on average about 35 msec for the working-side zygoma and 42 msec for the balancing-side zygoma to unload from 100 to 50% of peak force during apple-skin mastication, indicating that the unloading characteristics of the macaque masseter during mastication closely approximates its relaxation characteristics (as determined by muscle stimulation).