Jaw Gapes Research Articles

The influence of masseter and temporalis sarcomere length operating ranges as determined by laser diffraction on architectural estimates of muscle force and excursion in macaques (Macaca fascicularis and Macaca mulatta)

ObjectiveDetermine sarcomere length (Ls) operating ranges of the superficial masseter and temporalis in vitro in a macaque model and examine the impact of position-dependent variation on Ls and architectural estimates of muscle function (i.e., fiber length, PCSA) before and after Ls-normalization. DesignHeads of adult Macaca fascicularis (n = 4) and M. mulatta (n = 3) were bisected postmortem. One side of the jaw was fixed in occlusion, the other in maximum gape. Ls was measured bilaterally using laser diffraction and these measurements were used to estimate sarcomere-length operating ranges. Differences in fiber length and PCSA between sides were tested for significance prior to and following Ls-normalization. ResultsSarcomere-length operating ranges were widest for the anterior superficial masseter and narrowest for the posterior temporalis. Compared with other mammals, macaque operating ranges were wider and shifted to the right of the descending limb of a representative length-tension curve. Fibers were significantly stretched by as much as 100%, and PCSAs reduced by as much as 43%, on the maximally gaped compared with occluded sides. Ls-normalization substantially reduced position-dependent variance. ConclusionsThe superficial masseter ranges between 87–143% and the temporalis between 88–130% of optimal Ls from maximum gape to occlusion, indicating maximum relative Ls for these macaque muscles exceeds the upper end range previously reported for the jaw muscles of smaller mammals. The wider macaque operating ranges may be functionally linked to the propensity for facially prognathic primates to engage in agonistic canine display behaviors that require jaw-muscle stretch to facilitate production of wide jaw gapes.

Jaw-muscle architecture and mandibular morphology influence relative maximum jaw gapes in the sexually dimorphic Macaca fascicularis

Maximum jaw gape is a performance variable related to feeding and non-feeding oral behaviors, such as canine gape displays, and is influenced by several factors including jaw-muscle fiber architecture, muscle position on the skull, and jaw morphology. Maximum gape, jaw length, and canine height are strongly correlated across catarrhine primates, but relationships between gape and other aspects of masticatory apparatus morphology are less clear. We examine the effects of jaw-adductor fiber architecture, jaw-muscle leverage, and jaw form on gape in an intraspecific sample of sexually dimorphic crab-eating macaques (Macaca fascicularis). As M. fascicularis males have relatively larger maximum gapes than females, we predict that males will have muscle and jaw morphologies that facilitate large gape, but these morphologies may come at some expense to bite force.Male crab-eating macaques have relatively longer jaw-muscle fibers, masseters with decreased leverage, and temporomandibular joint morphologies that facilitate the production of wide gapes. Because relative canine height is correlated with maximum gape in catarrhines, and males have relatively longer canines than females, these results support the hypothesis that male M. fascicularis have experienced selection to increase maximum gape. The sexes do not differ in relative masseter physiologic cross-sectional area (PCSA), but males compensate for a potential trade-off between muscle excursion versus muscle force with increased temporalis weight and PCSA. This musculoskeletal configuration is likely functionally significant for behaviors involving aggressive canine biting and displays in male M. fascicularis and provides additional evidence supporting the multifactorial nature of the catarrhine masticatory apparatus. Our results have implications for the evolution of craniofacial morphology in catarrhine primates and reinforce the importance of evaluating additional factors other than feeding behavior and diet in analyses of masticatory apparatus form, function, and evolution.

Afferent sensory mechanisms involved in jaw gape-related muscle activation in unilateral biting

In unilateral biting or chewing, the working/balancing-side ratio (W/B-ratio) of masseter activities is inversely proportional to the jaw gape which was interpreted as a neuromuscular strategy to protect occlusion. This suggests that jaw separation is afferently perceived, raising the question how this perception might work. In related studies, isometric biting was exerted on rubber pieces that slightly yielded similar to compressed food in chewing. We hypothesized that minor jaw movements associated with this yielding are necessary to elicit a jaw gape-related control of relative activation in isometric biting. Surface electromyograms of masseter muscles were recorded bilaterally in 20 males during (a) unilateral chewing, (b) isometric biting on rubber pieces inducing jaw gapes of 5, 3, 2, 1, and 0.5 mm, and (c) isometric biting with teeth embedded in rigid splints causing gapes of 5 and 1 mm. With rubber, the masseter W/B-ratio increased from 100 % (5 mm) to 166 % (1 mm) (p = 0.0003) whereas with the splint it increased just slightly to 112 % (p = 0.005). With 1 mm gape, W/B-ratios in splint biting were significantly smaller than in rubber biting or in chewing (p = 0.01). We conclude that minor jaw motion preceding peak force in unilateral biting is necessary to create afferent sensory information that could elicit jaw gape-related activation of masseter muscles. Demonstrating a condition under which jaw gape-related activation can lose its occlusion protecting effect, these findings might contribute to disclose the causes of craniomandibular disorders.

Comparative analysis of masticatory apparatus features in neonatal common marmosets (Callithrix jacchus) and cotton‐top tamarins (Saguinus oedipus)

Marmosets are unique among callitrichids in habitually gouging trees with their anterior teeth to stimulate exudate flow. Previous analyses suggest that the masticatory apparatus of adult marmosets displays features facilitating relatively large jaw gapes, but decreased load‐resistance ability relative to closely‐related non‐gouging tamarins. We analyzed masticatory apparatus features of neonatal marmosets and tamarins to determine if the morphological differences observed between adults are present at birth. If marmoset infants show similar morphological divergence as adults, then the early appearance of these features suggest they are potential adaptations for tree gouging at wide gapes.We examined six stillborn common marmosets (Callithrix jacchus) and six cotton‐top tamarins (Saguinus oedipus). We microCT scanned the jaws, quantified fiber architecture of masticatory muscles and estimated symphyseal strength in simulated in vitro loading.We found few differences in mandibular cross‐sectional geometry, symphyseal strength or jaw‐muscle architecture between marmoset and tamarin neonates. Collectively, these findings suggest that at least some of the postnatal changes in the marmoset mandible and jaw‐muscle architecture that facilitate wide gapes, but reduced load‐resisting abilities compared to tamarins, arise from phenotypic plasticity related to gouging at wide gapes.Grant Funding Source: This work was funded by grants from the National Science Foundation (BCS‐0959438; BCS‐0412153).

Dietary correlates of temporomandibular joint morphology in New World primates

Previous analyses of the masticatory apparatus have demonstrated that the shape of the temporomandibular joint (TMJ) is functionally and adaptively linked to variation in feeding behavior and diet in primates. Building on previous research, this study presents an analysis of the link between diet and TMJ morphology in the context of functional and dietary differences among New World primates. To evaluate this proposed relationship, I used three-dimensional morphometric methods to quantify TMJ shape across a sample of 13 platyrrhine species. A broad interspecific analysis of this sample found strong relationships among TMJ size, TMJ shape, and diet, suggesting that both size and diet are significant factors influencing TMJ morphology in New World primates. However, it is likely that at least some of these differences are related to a division of dietary categories along clade lines. A series of hypotheses related to load resistance capabilities and range of motion in the TMJ were then tested among small groups of closely related taxa with documented dietary differences. These pairwise analyses indicate that some aspects of TMJ morphology can be used to differentiate among closely related species with different diets. However, not all of my predictions were upheld. The anteroposterior dimensions of the TMJ were most strongly consistent with hypothesized differences in ingestive/masticatory behaviors and jaw gape, whereas the predictions generated for variation in entoglenoid and articular tubercle height were not upheld. These results imply that while some features can be reliably associated with increased load resistance and facilitation of wider jaw gapes in the masticatory apparatus, other features are less strongly correlated with masticatory function.

Neuromuscular control of balancing side contacts in unilateral biting and chewing

When jaw gape in unilateral biting or chewing narrows, the working/balancing side activity ratio (W/B ratio) of masseter muscles increases due to decrease of balancing side (BS) activity. This was interpreted as a neuromuscular strategy to delimit the impact of BS contacts during chewing. To test this hypothesis, we studied whether W/B ratios are associated with incidence of BS tooth contacts. In 40 healthy subjects, bilateral masseter activity was recorded during unilateral biting with different jaw gapes and during various chewing tasks. Biting was performed with absence and with deliberate avoidance or generation of BS tooth contacts. Subjects were divided into three groups according to jaw gapes of 2, 1, and 0.5mm for which BS contact was first noticed in strong biting. The smaller this gape was, the higher were the mean W/B ratios. In biting with contact avoidance, the W/B ratios in each group increased with decreasing gape. In biting with generation of BS contacts, W/B ratios were smaller than with contact avoidance. W/B ratios in chewing with minimum interocclusal distances below 0.5mm were bigger than in biting with contact generation and were mostly bigger than in biting with contact avoidance. The findings confirm that increasing the masseter W/B ratio is a neuromuscular measure suitable to avoid BS contacts and support the idea that motor control uses jaw gape-related activation to limit the impact of BS contacts. Clarification of this protection mechanism might contribute to uncover the etiology of functional disorders and occlusal malfunctions.

Heterochrony of cranial features associated with wide jaw gapes in common marmosets (Callithrix jacchus)

Marmosets are unique among platyrrhines for habitually gouging trees with their anterior teeth to stimulate exudate flow. We previously demonstrated that marmosets exhibit cranial features that facilitate biting at wide jaw gapes during gouging, as compared to skulls of non‐gouging tamarins. Here we examine the role of heterochronic shifts during the ontogeny of cranial features facilitating wide gapes.Three cranial dimensions associated with wide gapes were measured, as well as three dimensions related to load resistance in ontogenetic series from neonates to adults of marmosets (Callithrix jacchus, N=129) and tamarins (Saguinus fuscicollis, N=135). All specimens were captive individuals housed at Oak Ridge Associated Universities' Colony with known ages at death.Marmosets exhibit a complex pattern of heterochronic shifts in cranial features linked to wide gape throughout ontogeny relative to tamarins. The relatively elongated anteroposterior glenoid, condyle and mandible of marmosets consistently appear peramorphic during ontogeny. Corporal and symphyseal dimensions associated with load resistance consistently appear paedomorphic in marmosets.Results support a hypothesis that the shape differences facilitating wide jaw gapes are the result of multiple heterochronic shifts in ontogenetic trajectories between gouging marmosets and non‐gouging tamarins.Supported by NSF (BCS‐0412153, BCS‐0094666).Grant Funding Source: Supported by NSF (BCS‐0412153, BCS‐0094666)

Indications for jaw gape‐related control of relative muscle activation in sequent chewing strokes

Jaw muscle activity ratios in unilateral isometric biting differ from ratios of unilateral chewing but approach the latter if the jaw gape in biting is made as small as the minimum interocclusal distance (MID) of chewing. Especially, the masseter working/balancing side ratio (W/B-ratio) becomes as asymmetric as in chewing, because of reduction in balancing side (BS) masseter activity. This behaviour of ratios might reflect a 'chewing-specific' motor strategy induced when isometric biting is performed with a 'chewing-like' gape. If this hypothesis applies, activity ratios should be associated with MIDs of sequent chewing strokes in a similar manner as with incremented jaw gapes in isometric biting. To test this prediction, bilateral surface electromyograms of masseter and anterior temporalis muscles and incisor movements were recorded during unilateral chewing in 52 subjects. W/B-ratios of masseter and temporalis activities and temporalis/masseter-ratios on both sides were calculated. The ratios were related to MIDs of consecutive chewing cycles. Three of the four ratios were associated with masticatory MID in the same manner as with jaw gape in isometric biting. In particular with decreasing MID, the masseter W/B-ratio increased from 1.5 to 2.2 (P < 0.01). This increase in asymmetry was attributed to a stronger decrease in masseter activity on the BS than on the working side. We conclude that relative jaw muscle activation is associated with interocclusal distance in a similar way in isometric biting and in chewing. This analogy supports the idea of a common jaw gape-related neuromuscular strategy facilitated by afferent signalling of interocclusal distance.

Jaw-muscle fiber architecture in tufted capuchins favors generating relatively large muscle forces without compromising jaw gape

Tufted capuchins ( sensu lato) are renowned for their dietary flexibility and capacity to exploit hard and tough objects. Cebus apella differs from other capuchins in displaying a suite of craniodental features that have been functionally and adaptively linked to their feeding behavior, particularly the generation and dissipation of relatively large jaw forces. We compared fiber architecture of the masseter and temporalis muscles between C. apella ( n = 12) and two “untufted” capuchins ( C. capucinus, n = 3; C. albifrons, n = 5). These three species share broadly similar diets, but tufted capuchins occasionally exploit mechanically challenging tissues. We tested the hypothesis that tufted capuchins exhibit architectural properties of their jaw muscles that facilitate relatively large forces including relatively greater physiologic cross-sectional areas (PCSA), more pinnate fibers, and lower ratios of mass to tetanic tension (Mass/P 0). Results show some evidence supporting these predictions, as C. apella has relatively greater superficial masseter and temporalis PCSAs, significantly so only for the temporalis following Bonferroni adjustment. Capuchins did not differ in pinnation angle or Mass/P 0. As an architectural trade-off between maximizing muscle force and muscle excursion/contraction velocity, we also tested the hypothesis that C. apella exhibits relatively shorter muscle fibers. Contrary to our prediction, there are no significant differences in relative fiber lengths between tufted and untufted capuchins. Therefore, we attribute the relatively greater PCSAs in tufted capuchins primarily to their larger muscle masses. These findings suggest that relatively large jaw-muscle PCSAs can be added to the suite of masticatory features that have been functionally linked to the exploitation of a more resistant diet by C. apella. By enlarging jaw-muscle mass to increase PCSA, rather than reducing fiber lengths and increasing pinnation, tufted capuchins appear to have increased jaw-muscle and bite forces without markedly compromising muscle excursion and contraction velocity. One performance advantage of this morphology is that it promotes relatively large bite forces at wide jaw gapes, which may be useful for processing large food items along the posterior dentition. We further hypothesize that this morphological pattern may have the ecological benefit of facilitating the dietary diversity seen in tufted capuchins. Lastly, the observed feeding on large objects, coupled with a jaw-muscle architecture that facilitates this behavior, raises concerns about utilizing C. apella as an extant behavioral model for hominins that might have specialized on small objects in their diets.

The functional correlates of jaw‐muscle fiber architecture in tree‐gouging and nongouging callitrichid monkeys

Common (Callithrix jacchus) and pygmy (Cebuella pygmaea) marmosets and cotton-top tamarins (Saguinus oedipus) share broadly similar diets of fruits, insects, and tree exudates. Marmosets, however, differ from tamarins in actively gouging trees with their anterior dentition to elicit tree exudates flow. Tree gouging in common marmosets involves the generation of relatively wide jaw gapes, but not necessarily relatively large bite forces. We compared fiber architecture of the masseter and temporalis muscles in C. jacchus (N = 18), C. pygmaea (N = 5), and S. oedipus (N = 13). We tested the hypothesis that tree-gouging marmosets would exhibit relatively longer fibers and other architectural variables that facilitate muscle stretch. As an architectural trade-off between maximizing muscle excursion/contraction velocity and muscle force, we also tested the hypothesis that marmosets would exhibit relatively less pinnate fibers, smaller physiologic cross-sectional areas (PCSA), and lower priority indices (I) for force. As predicted, marmosets display relatively longer-fibered muscles, a higher ratio of fiber length to muscle mass, and a relatively greater potential excursion of the distal tendon attachments, all of which favor muscle stretch. Marmosets further display relatively smaller PCSAs and other features that reflect a reduced capacity for force generation. The longer fibers and attendant higher contraction velocities likely facilitate the production of relatively wide jaw gapes and the capacity to generate more power from their jaw muscles during gouging. The observed functional trade-off between muscle excursion/contraction velocity and muscle force suggests that primate jaw-muscle architecture reflects evolutionary changes related to jaw movements as one of a number of functional demands imposed on the masticatory apparatus.

Motor control of jaw muscles in chewing and in isometric biting with graded narrowing of jaw gape

When a certain bite force is applied during unilateral chewing, the combination of jaw elevator muscle activities is different than when a comparable force is applied in unilateral isometric biting, e.g. on a force transducer. Masticatory peak force is generated in a nearly isometric phase of the chewing cycle, with a jaw gape of about 1 mm. In contrast, peak force in isometric biting on force measuring equipment usually induces jaw gapes of 6 mm or even more. Therefore, we tested the hypothesis that the jaw gape influences relative activation of elevator muscles in unilateral isometric biting. We further examined whether such influence could explain the different activity combinations of chewing and isometric biting. In thirty asymptomatic males, masseter and temporalis activities were recorded during intermittent isometric biting with jaw gapes of 6, 5, 3, 2 and 1 mm and during unilateral chewing. Activity combinations were described by working/balancing ratios and by temporalis/masseter ratios. With decreasing jaw gape the working/balancing ratio of the posterior temporalis decreased (P < 0.002) while that of the masseter increased (P < 0.001). Likewise, the temporalis/masseter ratio on the balancing side increased (P < 0.001). With decreasing jaw gape, activity ratios of isometric biting approached ratios of chewing. We conclude that: (i) relative jaw muscle activation in isometric biting depends on the jaw gape, (ii) relative muscle activation in chewing resembles relative activation of isometric biting with a small 'chewing-like' gape. This suggests that characteristic activity combinations in chewing are mainly a result of the approximately isometric contraction during the slow closing phase of the chewing cycle.

Influence of jaw gape on EMG of jaw muscles and jaw-stretch reflexes

The influence of jaw gapes on jaw-stretch reflexes and jaw muscles activity was studied in order to test the sensitivity of human muscle spindle afferents in various jaw muscles. Twelve healthy men (mean age ± S.E.M.: 25.0 ± 1.2 yr) participated in the study. Short-latency excitatory reflex responses were evoked by a custom-made stretch device with the subjects biting on a jaw-bar with their front teeth. Surface electromyographic (sEMG) recordings from right masseter (MAR), and right temporalis (TAR), intramuscular EMG (imEMG) recordings from right lateral pterygoid (LPR) and right anterior digastric (ADR) muscles were made. The reflex at different jaw gapes of 6, 10, 14, 18, 22, 26, 30, 34, and 38 mm were examined in random order with standard stretch conditions of 1 mm displacement and 10 ms ramp time. Twenty sweeps of the reflex were recorded at each level with at least 5 s interval between each sweep with online monitoring of the visual feed back at 15% of maximum voluntary contraction (MVC) of each jaw gape from MAR. The results showed that the peak-to-peak amplitude of the jaw-stretch reflex in MAR was significantly higher at 14 mm compared to 30, 34, and 38 mm ( P < 0.038), whereas the reflex amplitude in TAR increased with jaw gape until a maximum at 34 mm. There was no significant effect of jaw gape in LPR muscles ( P = 0.825) and no obvious stretch reflex was observed in ADR. When the amplitude was normalised to the pre-stimulus EMG at each jaw gape, the highest normalised amplitude was observed at 14 mm jaw gape in MAR, however there was no significant effect of jaw gape on the normalised amplitude in TAR and LPR. In addition, masseter EMG at MVC significantly decreased with the increase of the gapes, i.e. biting at 6, 14, and 18 mm gapes had a significantly higher MVC compared to 26, 30, 34, and 38 mm (ANOVA: P < 0.013). It is concluded that the jaw gapes influence the sensitivity of the human muscle spindle afferents in jaw-closing muscles with a distinct peak, which is within normal jaw gapes during function.

Comparative functional analysis of skull morphology of tree-gouging primates.

Many primates habitually feed on tree exudates such as gums and saps. Among these exudate feeders, Cebuella pygmaea, Callithrix spp., Phaner furcifer, and most likely Euoticus elegantulus elicit exudate flow by biting into trees with their anterior dentition. We define this behavior as gouging. Beyond the recent publication by Dumont ([1997] Am J Phys Anthropol 102:187-202), there have been few attempts to address whether any aspect of skull form in gouging primates relates to this specialized feeding behavior. However, many researchers have proposed that tree gouging results in larger bite force, larger internal skull loads, and larger jaw gapes in comparison to other chewing and biting behaviors. If true, then we might expect primate gougers to exhibit skull modifications that provide increased abilities to produce bite forces at the incisors, withstand loads in the skull, and/or generate large gapes for gouging. We develop 13 morphological predictions based on the expectation that gouging involves relatively large jaw forces and/or jaw gapes. We compare skull shapes for P. furcifer to five cheirogaleid taxa, E. elegantulus to six galagid species, and C. jacchus to two tamarin species, so as to assess whether gouging primates exhibit these predicted morphological shapes. Our results show little morphological evidence for increased force-production or load-resistance abilities in the skulls of these gouging primates. Conversely, these gougers tend to have skull shapes that are advantageous for creating large gapes. For example, all three gouging species have significantly lower condylar heights relative to the toothrow at a given mandibular length in comparison with closely related, nongouging taxa. Lowering the height of the condyle relative to the mandibular toothrow should reduce the stretching of the masseters and medial pterygoids during jaw opening, as well as position the mandibular incisors more anteriorly at wide jaw gapes. In other words, the lower incisors will follow a more vertical trajectory during both jaw opening and closing. We predict, based on these findings, that tree-gouging primates do not generate unusually large forces, but that they do use relatively large gapes during gouging. Of course, in vivo data on jaw forces and jaw gapes are required to reliably assess skull functions during gouging.

Mechanical properties of single motor units in the rabbit masseter muscle as a function of jaw position

Positions and contractile properties of rabbit masseter motor units were investigated at different jaw gapes. Twitch responses were measured at gapes ranging from dental occlusion (0 degree) to maximum opening (21 degrees), in steps of 3 degrees. The twitches were elicited by stimulating motoneurons extracellularly in the trigeminal motor nucleus. The units appeared to produce a large variety of force vectors. On average motor units in the deep parts of the masseter produced considerably less twitch force (average: 25-30 mN) than those in the superficial parts (average: 45-50 mN) and anteriorly located motor units were slower than posteriorly located units. With an increase of jaw angle, twitches became slower, reflected by an increase (30%) of the twitch contraction time. Most motor units had a parabolic-like active jaw angle-force relationship. A large variation in the shape of the curves was found. The average optimum jaw angle was reached at 12 degrees jaw opening. In general, force output was relatively low (20-60% of maximum force) at occlusion and relatively high (60-100% of maximum force) at maximal jaw opening. Anteriorly and posteriorly located motor units differed significantly in their angle-force curves. Anteriorly located motor units produced less relative force at occlusion, showed a steeper increase of force with an increase of jaw angle, reached maximum force at larger jaw angles and produced larger forces at maximum jaw opening. The larger force changes in the more anterior units are probably related to their longer distance from the axis of jaw rotation. The large variability of motor unit properties and angle-force curves suggests that a fine gradation of both force magnitude and direction is possible within the masseter and that the angle-force curve of the whole muscle or of whole muscle parts is broader than that of individual motor units. This broadening may be considered as a mechanism to sustain active muscle force throughout a large movement range.

The Effect of Particle Size Reduction on the Jaw Gape in Human Mastication

Eight subjects participated in chewing experiments to examine how the jaw gape in consecutive chewing cycles depends on the dimensions and the volume of the food bolus. Different volumes of chewing-gum and a silicone rubber (Optosil) were used. The initial particle size of Optosil was also varied. With the aid of a sieving procedure, the size distribution of Optosil particles was determined after different numbers of chewing cycles. The maximum size of a chewing-gum bolus along three orthogonal axes was determined after a random number of chewing cycles for all the volumes of chewing-gum offered. The jaw gape was measured by means of an optical motion analysis system and calibrated at the level of the first molars. The maximum jaw gape and the gape at the first fall in mandibular velocity after the onset of jaw-closing were determined for different chewing cycles from the position signal and its time derivative. For each volume of chewing gum offered to the subject, the average of the maximum gapes attained in the subsequent cycles of jaw movement was related to the characteristic height of a bolus of that volume; maximum velocity of closing appeared to occur while the antagonistic teeth were already penetrating the gum bolus. The increase in the maximum jaw gape, the gape at the velocity maximum, and the height of the gum bolus, as a function of the volume of chewing-gum, could be well-described by a power function of the volume. The exponent of the power function for both jaw gapes was only slightly smaller than the exponent obtained for the bolus height.(ABSTRACT TRUNCATED AT 250 WORDS)