William L. Hylander

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)

Mandibular corpus strain in primates: Further evidence for a functional link between symphyseal fusion and jaw‐adductor muscle force

Previous work indicates that compared to adult thick-tailed galagos, adult long-tailed macaques have much more bone strain on the balancing-side mandibular corpus during unilateral isometric molar biting (Hylander [1979a] J. Morphol. 159:253-296). Recently we have confirmed in these same two species the presence of similar differences in bone-strain patterns during forceful mastication. Moreover, we have also recorded mandibular bone strain patterns in adult owl monkeys, which are slightly smaller than the galago subjects. The owl monkey data indicate the presence of a strain pattern very similar to that recorded for macaques, and quite unlike that recorded for galagos. We interpret these bone-strain pattern differences to be importantly related to differences in balancing-side jaw-adductor muscle force recruitment patterns. That is, compared to galagos, macaques and owl monkeys recruit relatively more balancing-side jaw-adductor muscle force during forceful mastication. Unlike an earlier study (Hylander [1979b] J. Morphol. 160:223-240), we are unable to estimate the actual amount of working-side muscle force relative to balancing-side muscle force (i.e., the W/B muscle force ratio) in these species because we have no reliable estimate of magnitude, direction, and precise location of the bite force during mastication. A comparison of the mastication data with the earlier data recorded during isometric molar biting, however, supports the hypothesis that the two anthropoids have a small W/B jaw-adductor muscle force ratio in comparison to thick-tailed galagos. These data also support the hypothesis that increased recruitment of balancing-side jaw-adductor muscle force in anthropoids is functionally linked to the evolution of symphyseal fusion or strengthening. Moreover, these data refute the hypothesis that the recruitment pattern differences between macaques and thick-tailed galagos are due to allometric factors. Finally, although the evolution of symphyseal fusion in primates may be linked to increased stress associated with increased balancing-side muscle force, it is currently unclear as to whether the increased force is predominately vertically directed, transversely directed, or is a near equal combination of these two force components (cf. Ravosa and Hylander [1994] In Fleagle and Kay [eds.]: Anthropoid Origins. New York: Plenum, pp. 447-468).

Elastic properties and masticatory bone stress in the macaque mandible.

One important limitation of mechanical analyses with strain gages is the difficulty in directly estimating patterns of stress or loading in skeletal elements from strain measurements. Because of the inherent anisotropy in cortical bone, orientation of principal strains and stresses do not necessarily coincide, and it has been demonstrated theoretically that such differences may be as great as 45 degrees (Cowin and Hart, 1990). Likewise, relative proportions of stress and strain magnitudes may differ. This investigation measured the elastic properties of a region of cortical bone on both the buccal and lingual surfaces of the lower border of the macaque mandible. The elastic property data was then combined with macaque mandibular strain data from published and a new in vivo strain gage experiment to determine directions and magnitudes of maximum and minimum principal stresses. The goal was to compare the stresses and strains and assess the differences in orientation and relative magnitude between them. The main question was whether these differences might lead to different interpretations of mandibular function. Elastic and shear moduli, and Poissons ratios were measured using an ultrasonic technique from buccal and lingual cortical surfaces in 12 macaque mandibles. Mandibular strain gage data were taken from a published set of experiments (Hylander, 1979), and from a new experiment in which rosette strain gauges were fixed to the buccal and lingual cortices of the mandibular corpus of an adult female Macaca fascicularis, after which bone strain was recorded during mastication. Averaged elastic properties were combined with strain data to calculate an estimate of stresses in the mandibular corpus. The elastic properties were similar to those of the human mandibular cortex. Near its lower border, the macaque mandible was most stiff in a longitudinal direction, less stiff in an inferosuperior direction, and least stiff in a direction normal to the bones surface. The lingual aspect of the mandible was slightly stiffer than the buccal aspect. Magnitudes of stresses calculated from average strains ranged from a compressive stress of -16.00 GPa to a tensile stress of 8.84 GPa. The orientation of the principal stresses depended on whether the strain gage site was on the working or balancing side. On the balancing side of the mandibles, maximum principal stresses were oriented nearly perpendicular to the lower border of the mandible. On the working side of the mandibles, the orientation of the maximum principal stresses was more variable than on the balancing side, indicating a larger range of possible mechanisms of loading. Near the lower border of the mandible, differences between the orientation of stresses and strains were 12 degrees or less. Compared to ratios between maximum and minimum strains, ratios between maximum and minimum stresses were more divergent from a ratio of 1.0. Results did not provide any major reinterpretations of mandibular function in macaques, but rather confirmed and extended existing work. The differences between stresses and strains on the balancing side of the mandible generally supported the view that during the power stroke the mandible was bent and slightly twisted both during mastication and transducer biting. The calculated stresses served to de-emphasize the relative importance of torsion. On the working side, the greater range of variability in the stress analysis compared to the strain analysis suggested that a more detailed examination of loadings and stress patterns in each individual experiment would be useful to interpret the results. Torsion was evident on the working side; but in a number of experiments, further information was needed to interpret other superimposed regional loading patterns, which may have included parasagittal bending and reverse parasagittal bending.

Strain in the galago facial skull.

Little experimental work has been directed at understanding the distribution of stresses along the facial skull during routine masticatory behaviors. Such information is important for understanding the functional significance of the mammalian circumorbital region. In this study, bone strain was recorded along the dorsal interorbit, postorbital bar, and mandibular corpus in Otolemur garnettii and O. crassicaudatus (greater galagos) during molar chewing and biting. We determined principal‐strain magnitudes and directions, compared peak shear‐strain magnitudes between various regions of the face, and compared galago strain patterns with similar experimental data for anthropoids. This suite of analyses were used to test the facial torsion model (Greaves [1985] J Zool (Lond) 207:125–136; [1991] Zool J Linn Soc 101:121–129; [1995] Functional morphology in vertebrate paleontology. Cambridge: Cambridge University Press, p 99–115). A comparison of galago circumorbital and mandibular peak strains during powerful mastication indicates that circumorbital strains are very low in magnitude. This demonstrates that, as in anthropoids, the strepsirhine circumorbital region is highly overbuilt for countering routine masticatory loads. The fact that circumorbital peak‐strain magnitudes are uniformly low in both primate suborders undermines any model that emphasizes the importance of masticatory stresses as a determinant of circumorbital form, function, and evolution. Preliminary data also suggest that the difference between mandibular and circumorbital strains is greater in larger‐bodied primates. This pattern is interpreted to mean that sufficient cortical bone must exist in the circumorbital region to prevent structural failure due to nonmasticatory traumatic forces. During unilateral mastication, the direction of ϵ1 at the galago dorsal interorbit indicates the presence of facial torsion combined with bending in the frontal plane. Postorbital bar principal‐strain directions during mastication are oriented, on average, very close to 45° relative to the skulls long axis, much as predicted by the facial torsion model. When chewing shifts from one side of the face to the other, there is a characteristic reversal or flip‐flop in principal‐strain directions for both the interorbit and postorbital bar. Although anthropoids also exhibit an interorbital reversal pattern, peak‐strain directions for this clade are opposite those for galagos. The presence of such variation may be due to suborder differences in relative balancing‐side jaw‐muscle force recruitment. Most importantly, although the strain‐direction data for the galago circumorbital region offer support for the occurrence of facial torsion, the low magnitude of these strains suggests that this loading pattern may not be an important determinant of circumorbital morphology. J. Morphol. 245:51–66, 2000

An in vivo strain-gauge analysis of the squamosal-dentary joint reaction force during mastication and incisal biting in Macaca mulatta and Macaca fascicularis

Abstract Rectangular rosette or single-element strain gauges were bonded to surgically-exposed mandibular cortical bone in the region immediately below the temporo-mandibular ligament in adult and sub-adult macaques. After recovery from the general anaesthetic, bone strain was recorded during incision and mastication of apples. The bone strain data demonstrate that the joint is loaded to varying degrees depending on the position of the bite point. Bone strain values were larger on the contralateral side than on the ipsilateral during mastication, demonstrating that the net compressive reaction force along the contralateral joint probably exceeds the net compressive reaction force along the ipsilateral one during these periods. The largest bone strain values were recorded during apple incision, demonstrating that the joint is also loaded during incisal biting.

The mechanical or metabolic function of secondary osteonal bone in the monkey Macaca fascicularis

Secondary osteonal bone is believed by many to serve a mechanical function, altering the properties and/or orientation of bone in response to fluctuating mechanical demands or in the prevention and/or repair of fatigue microdamage. Based on this belief, secondary osteons should be concentrated mainly in regions experiencing high peak-strain conditions. Others contend that secondary osteonal bone functions primarily in meeting the bodys calcium needs, and should be expected to form principally in low peak-strain regions so as to avoid compromising the mechanical strength of the bone. These two hypotheses were tested by examining the distribution of secondary osteonal bone in both relatively high- and low-strain regions of the macaque face. Previous strain-gauge studies have demonstrated a steep strain gradient in the macaque face, with relatively high peak strains in the anterior portion of the zygomatic arch and in the mandibular corpus. Relatively low peak strains have been found in the posterior portion of the zygomatic arch and supraorbital bar. Results presented here show that in the mature macaques, there is no consistent relation between newly forming secondary osteons (i.e. those labelled with fluorescent dyes) and peak strain levels. From these data it is concluded that, in the non-perturbed adult, either mechanical and metabolic factors contribute equally to the observed pattern or that metabolically driven remodelling is initiated without regard to strain levels. In immature macaques, however, the relation between peak strain levels and secondary osteon density is positive, with a significantly higher density of labelled osteons in the high strain regions. From these data it is concluded that, in immature individuals, mechanical factors are predominantly responsible for the initiation of secondary osteonal remodelling.

Jaw movements and patterns of mandibular bone strain during mastication in the monkey Macaca fascicularis.

Small amalgam fillings were placed in maxillary and mandibular second molar and canine teeth for cine-radiographic analysis. The rosette strain gauges were bonded bilaterally to mandibular cortical bone below the second or third molars. The monkeys were placed in a restraining chair that did not restrict normal head, neck or jaw movements; they were fed various foods and the bone-strain data recorded. Simultaneous jaw movements were recorded with cine-radiographic apparatus synchronized with the bone-strain recordings. During vigorous mastication, the transition between fast close and the power stroke was correlated with a sharp increase in masticatory force. In most instances, the jaws were maximally-loaded prior to maximum intercuspation, i.e. during the buccal phase (phase I) of occlusion. The macaques swallowed frequently throughout a chewing sequence and these swallows were intercalated into the chewing cycle toward the end of the power stroke. Such swallows had little effect on the magnitude or direction of peak principal strains during the power stroke. Bone-strain data suggested that unloading patterns during the power stroke of mastication were largely a function of the relaxation time of the jaw adductors. The period from 100 per cent peak strain to 50 per cent peak strain during unloading closely approximated to the half-relaxation time of the whole adductor jaw muscles.

The relationship between masseter force and masseter electromyogram during mastication in the monkey Macaca fascicularis

In five adult monkeys, electromyograms (EMGs) were recorded from bipolar surface electrodes positioned over the superficial masseter and from bipolar fine-wire electrodes within both the superficial and deep masseter. Relative masseter force was estimated by measuring surface bone strain from the lateral aspect of the zygomatic arch using rosette strain gauges. Multiple step-wise regression procedures demonstrated that peak values of the averaged masseter EMG could often explain a considerable amount of the variation of peak relative masseter force during mastication, i.e. r2 values ranged from 0.23 to 0.96 for the various single-electrode models and R2 values ranged from 0.78 to 0.96 for the various multiple-electrode models. The r2 values for relative masseter force and EMG data from the surface electrodes ranged from 0.69 to 0.96, and, on average, EMG data from surface electrodes provided somewhat more information about overall relative muscle force than data from fine-wire electrodes. The R2 values for a two-electrode model, consisting of data from surface electrodes over the superficial masseter and fine-wire electrodes in the posterior portion of the deep masseter, ranged from 0.78 to 0.95. The latency between the averaged surface EMG and relative muscle force was determined and the data indicated that the surface EMG usually preceded muscle force. This latency tended to decrease gradually throughout the entire power stroke of mastication. At peak values, the surface EMG preceded muscle force by about 22 ms. Towards the end of the power stroke, i.e. the 25% of peak values during unloading, muscle force may actually precede the average EMG.

Temporalis and masseter muscle function during incision in macaques and humans

Most previously published electromyographic (EMG) studies have indicated that the temporalis muscles in humans become almost electrically quiet during incisai biting. These data have led various workers to conclude that these muscles may contribute little to the incisai bite force. The feeding behavior and comparative anatomy of the incisors and temporalis muscles of certain catarrhine primates, however, suggest that the temporalis muscle is an important and powerful contributor to the bite force during incision. One purpose of this study is to analyze the EMG activity of the masseter and temporalis muscles in both humans and macaques with the intention of focusing on the conflict between published EMG data on humans and inferences of muscle function based on the comparative anatomy and behavior of catarrhine primates. The EMG data collected from humans in the present study indicate that, in five of seven subjects, the masseter,anterior temporalis, and posterior temporalis muscles are very active during apple incision (i.e., relative to EMG activity levels during apple and almond mastication). In the other two human subjects the EMG levels of these muscles are lower during incision than during mastication, but in no instance are these muscles ever close to becoming electrically quiet. The EMG data on macaques indicate that, in all six subjects, the masseter, anterior temporalis, and posterior temporalis muscles are very active during incision. These data are in general agreement with inferences on muscle function that have been drawn from the comparative anatomy and behavior of primates, but they do not agree with previous experimental data. The reason for this disagreement is probably due to differences in the experimental procedure. In previous studies subjects simply bit isometrically on their incisors and the resulting EMG pattern was compared to the pattern associated with powerful clenching in centric occlusion. In the present study the subjects incised into actual food objects, and the resulting EMG pattern was compared to the pattern associated with mastication of various foods. It is not surprising that these two procedures result in markedly different EMG patterns, which in turn result in markedly different interpretations of jaw-muscle function. In an attempt to explain the evolution of the postorbital septum in anthropoids, it has been suggested that the anterior temporalis is more active than the masseter during incision (Cachel, 1979). The human and macaque EMG data do not support this hypothesis; during incision, the two muscles show no consistent differences in humans and the masseter appears to be in fact more active than the anterior temporalis in macaques.

In-vivo bone strain as an indicator of masticatory bite force in Macaca fascicularis

The hypothesis that mandibular bone-strain patterns are a good indicator of molar bite-force patterns in M. fascicularis during mastication was tested by determining the relationship between mandibular bone-strain patterns and bite-force patterns during isometric biting. Bone-strain patterns were determined using rosette strain gauges bonded to mandibular cortical bone below the roots of the M2 during isometric binding on a transducer along the M1-M2 region. The effects of rosette position on bone-strain patterns during mastication was determined by comparing bone-strain patterns recorded from two different rosettes; one bonded below the roots of the M2 and the other below the roots of the M3. The data from the two experimental sets support the hypothesis that bone-strain patterns along the working side of the mandible are a good indicator of bite-force patterns during the power stroke. The relationship between bone-strain patterns and bite-force patterns was not perfect and the two principal strains were not of equal value. In general, principal compression was a better indicator of bite force than principal tension.