In vivo function of the craniofacial haft: the interorbital "pillar"

The craniofacial haft resists forces generated in the face during feeding, but the importance of these forces for the form of the craniofacial haft remains to be determined. In vivo bone strain data were recorded from the medial orbital wall in an owl monkey (Aotus), rhesus macaques (Macaca mulatta), and a galago (Otolemur) during feeding. These data were used to determine whether: the interorbital region can be modeled as a simple beam under bending or shear; the face is twisting on the brain case during unilateral biting or mastication; the interorbital "pillar" is being axially compressed during incisor loading and both axially compressed and laterally bent during mastication; and the interorbital "pillar" transmits axial compressive forces from the toothrow to the braincase. The strain data reveal that the interorbital region cannot be modeled as a anteroposteriorly oriented beam bent superiorly in the sagittal plane during incision or mastication. The strain orientations recorded in the majority of experiments are concordant with those predicted for a short beam under shear, although the anthropoids displayed evidence of multiple loading regimes in the medial orbital wall. Strain orientation data corroborate the hypothesis that the strepsirrhine face is twisted during mastication. The hypothesis that the interorbital region is a member in a rigid frame subjected to axial compression during mastication receives some support. The hypothesis that the interorbital region is a member in a rigid frame subjected to lateral bending during mastication is supported by the epsilon1/absolute value epsilon2 ratio data but not by the strain orientation data. The timing of peak shear strains in the medial orbital wall of anthropoids does not bear a consistent relationship to the timing of peak shear strain in the mandibular corpus, suggesting that bite force is not the only external force influencing the medial orbital wall. Strain orientation data suggest the existence of two distinct loading regimes, possibly associated with masseter or medial pterygoid contraction. Regardless of the loading regime, all taxa showed low strain magnitudes in the medial orbital wall relative to the anterior root of the zygoma and the mandibular corpus. The strain gradients documented here and elsewhere suggest that, in anthropoids at least, local effects of external forces are more important than a single global loading regime. The low strain magnitudes in the medial orbital wall and in other thin bony plates around the orbit suggest that these structures are not optimally designed for resisting feeding forces. It is hypothesized that their function is to provide rigid support and protection for soft-tissue structures such as the nasal epithelium, the brain, meninges, and the eye and its adnexa. In contrast with the face of Otolemur, which appears to be subjected to a single predominant loading regime, anthropoids may experience different loading regimes in different parts of the face. This implies that the anthropoid and strepsirrhine facial skulls might be optimized for different functions.     

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 epsilon(1) 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 degrees relative to the skull's 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.     

Mandibular function in Galago crassicaudatus and Macaca fascicularis: an in vivo approach to stress analysis of the mandible.

Single-element and/or rosette strain gages were bonded to mandibular cortical bone in Galago crassicaudatus and Macaca fascicularis. Five galago and eleven macaque bone strain experiments were performed and analyzed. In vivo bone strain was recorded from the lateral surface of the mandibular corpus below the postcanine tooth row during transducer biting and during mastication and ingestion of food objects. In macaques and galagos, the mandibular corpus on the balancing side is primarily bent in the sagittal plane during mastication and is both twisted about its long axis and bent in the sagittal plane during transducer biting. On the working side, it is primarily twisted about its long axis and directly sheared perpendicular to its long axis, and portions of it are bent in the sagittal plane during mastication and molar transducer biting. In macaques, the mandibular corpus on each side is primarily bent in the sagittal plane and twisted during incisal transducer biting and ingestion of food objects, and it is transversely bent and slightly twisted during jaw opening. Since galagos usually refused to bite the transducer or food objects with their incisors, an adequate characterization of mandibular stress patterns during these behaviors was not possible. In galagos the mandibular corpus experiences very little transverse bending stress during jaw opening, perhaps in part due to its unfused mandibular symphysis. Marked differences in the patterns of mandibular bone strain were present between galagos and macaques during the masticatory power stroke and during transducer biting. Galagos consistently had much more strain on the working side of the mandibular corpus than on the balancing side. These experiments support the hypothesis that galagos, in contrast to macaques, employ a larger amount of working-side muscle force relative to the balancing-side muscle force during unilateral biting and mastication, and that the fused mandibular symphysis is an adaption to use a maximal amount of balancing-side muscle force during unilateral biting and mastication. These experiments also demonstrate the effects that rosette position, bite force magnitudes, and types of food eaten have on recorded mandibular strain patterns.     

Cranial morphology of Aegyptopithecus and Tarsius and the question of the tarsier-anthropoidean clade

New crania of the Oligocene anthropoidean Aegyptopithecus provide a test of the hypothesized tarsier-anthropoidean clade. Three cranial characters shared by Tarsius and some modern anthropoideans (apical interorbital septum, postorbital septum, "perbullar" carotid pathway) were examined. 1) An apical interorbital septum is absent in Aegyptopithecus. A septum does occur in Galago senegalensis (Lorisidae) and Microcebus murinus (Cheirogaleidae), so the presence of a septum is not strong evidence favoring a tarsiiform-anthropoidean clade. 2) In Aegyptopithecus and other anthropoideans, the postorbital septum is formed mainly by a periorbital flange of the zygomatic that extends medially from the lateral orbital margin onto or near the braincase. The postorbital plate of Tarsius is formed by frontal and alisphenoid flanges that extend laterally from the braincase to the zygomatic's frontal process, which is not broader than the postorbital bars of other prosimians. Periorbital flanges evolved in Tarsius for support or protection of the enormous eyes, as suggested by the occurrence of maxillary and frontal flanges that cup portions of the eye but do not separate it from temporal muscles. 3) The internal carotid artery of Aegyptopithecus enters the bulla posteriorly and crosses the anteroventral part of the promontorium. The tympanic cavity was probably separated from the anteromedial cavity by a septum stretching from the carotid channel to the ventrolateral bullar wall. In Tarsius, the carotid pathway is prepromontorial, and a septum stretches from the carotid channel to the posteromedial bullar wall. Quantitative analyses indicate that anterior carotid position has evolved because of erect head posture. The cranium of Oligocene anthropoideans thus provides no support for the hypothesized tarsier-anthropoidean clade.     

Masticatory stress, orbital orientation and the evolution of the primate postorbital bar

A postorbital bar is one of a suite of derived features which distinguishes basal primates from their putative sister taxon, plesiadapiforms. Two hypotheses have been put forward to explain postorbital bar development and variation in circumorbital form: the facial torsion model and visual predation hypothesis. To test the facial torsion model, we employ strain data on circumorbital and mandibular loading patterns in representative primates with a postorbital bar and masticatory apparatus similar to basal primates. To examine the visual predation hypothesis, we employ metric data on orbit orientation in Paleocene and Eocene primates, as well as several clades of visual predators and foragers that vary interspecifically in postorbital bar formation.A comparison of galago circumorbital and mandibular peak strains during powerful mastication demonstrates that circumorbital strains are quite low. This indicates that, as in anthropoids, the strepsirhine circumorbital region is excessively overbuilt for countering routine masticatory loads. The fact that circumorbital peak-strain levels are uniformly low in both primate suborders undermines any model which posits that masticatory stresses are determinants of circumorbital form, function and evolution. This is interpreted to mean that sufficient cortical bone must exist to prevent structural failure due to non-masticatory traumatic forces. Preliminary data also indicate that the difference between circumorbital and mandibular strains is greater in larger taxa.Comparative analyses of several extant analogs suggest that the postorbital bar apparently provides rigidity to the lateral orbital margins to ensure a high level of visual acuity during chewing and biting. The origin of the primate postorbital bar is linked to changes in orbital convergence and frontation at smaller sizes due to nocturnal visual predation and increased encephalization. By incorporating in vivo and fossil data, we reformulate the visual predation hypothesis of primate origins and thus offer new insights into major adaptive transformations in the primate skull.     

Masticatory-stress hypotheses and the supraorbital region of primates

The purpose of this study is to test various masticatory-stress hypotheses about the evolution and function of well-developed browridges of higher primates. This was done by measuring and analyzing patterns of in vivo bone strain recorded from three-element rosette strain gages bonded to the supraorbital region and to other portions of the bony face of Macaca fascicularis and Papio anubis during mastication and incision. The magnitude and direction of the principal strains recorded support Endo's hypothesis that the supraorbital region during mastication and incision is bent in the frontal plane (Endo, 1966). Our data do not, however, support his hypothesis that the supraorbital region is bent more during incision than during mastication. The data also demonstrate that overall levels of supraorbital strain are not larger in more prognathic subjects. Most importantly, the data indicate that the supraorbital region of nonhuman catarrhines is strained very little during mastication and incision. This indicates that there is much more supraorbital bone than is necessary both to counter masticatory loads and to provide an adequate safety factor to failure for these loads. This in turn suggests that the macaque and baboon browridges can be considerably reduced in size and still maintain these required structural characteristics. Thus, our experiments provide no support whatsoever for those hypotheses that directly link browridge morphology to masticatory stress (cf. Endo, 1966; Russell, 1983, 1985). A recent review of Endo's original work indicates that this latter statement is also true for humans (Picq and Hylander, 1989). We conclude, therefore, that there is no good reason to believe that enlarged browridges in living and/or fossil primates are structural adaptations to counter intense masticatory forces. The evolution of browridge morphology in primates is best explained on the basis of factors related to the position of the brain relative to the orbits (Moss and Young, 1960). When these structures are widely separated, as in gorillas, the large intervening space must be bridged with bone. In addition, enough bone must be present within the supraorbital and bridged regions to prevent structural failure due to non-masticatory external forces associated with highly active primates (e.g., accidental traumatic forces applied to the orbits and neurocranium). This requirement results in both pronounced browridges and in much more supraorbital bone than is necessary to counter routine cyclical stress during mastication and incision. This in turn explains why bone strains recorded from the supraorbital region are extremely small relative to other portions of the primate face during mastication and incision.     

Interspecific perspective on mechanical and nonmechanical models of primate circumorbital morphology.

Linear dimensions and angular orientations of the browridge, postorbital bar, and postorbital septum were obtained from a representative series of primates and compared with variables associated with several nonmechanical and biomechanical/mechanical models put forward to explain the form and function of the circumorbital region. Analyses of the results indicate that face size is the primary determinant of variation in primate circumorbital morphology. Anteroposterior browridge thickness is correlated with neural-orbital disjunction among anthropoid primates, but not among prosimians. This difference appears related to differences in the construction of the upper face and anterior cranial fossa between prosimians and anthropoids. Little support is demonstrated for the anterior dental loading model of browridge development. Mediolateral postorbital bar width and (to a lesser degree) browridge height are correlated with neurofacial torsion during mastication and variation in masticatory muscle size. These analyses further suggest that since circumorbital structures (especially the browridges) are located the farthest away from the chewing apparatus, they are least affected by masticatory stresses.     

Septa and processes: convergent evolution of the orbit in haplorhine primates and strigiform birds

According to the “nocturnal visual predation hypothesis” (NVPH), the convergent eyes and orbits of primates result from selection for improved stereoscopic depth perception to facilitate manual capture of prey at night. Within primates, haplorhines share additional derived orbital morphologies, including a postorbital septum and greater orbital convergence than any other mammalian clade. While the homology and function of the haplorhine septum remain controversial, experimental data suggest that septa evolved to inhibit mechanical disturbance of the orbital contents by the anterior temporalis muscle during mastication. According to this “insulation hypothesis,” haplorhines are particularly susceptible to disruption of the orbital contents because they have large and highly convergent eyes and orbits. However, comparative tests of the insulation hypothesis have been hindered by the morphological uniqueness of the haplorhine septum among mammals. Among birds, owls (Strigiformes) exhibit an expanded postorbital process that may be functionally analogous to the haplorhine septum. Here we present a comparative analysis of orbital morphology in 103 avian species that tests two hypotheses: (1) large, convergent orbits are associated with nocturnal visual predation, and (2) the strigiform postorbital process and haplorhine postorbital septum similarly function to insulate the eyes from contractions of mandibular adductors. Strigiforms, as nocturnal visual predators, possess relatively large orbits and exhibit the highest degree of orbital convergence in our sample. Notably, orbital convergence does not scale with orbit size in birds as in mammals. Owls are also unique among the birds examined in possessing extensive, plate-like postorbital processes that largely isolate the orbits from the temporal fossae. Furthermore, dissections of four owl species demonstrate that the expanded strigiform postorbital process deflects the path of mandibular adductors around the eye's inferolateral margin. These findings provide further comparative support for both the NVPH and the insulation hypothesis.     

A finite element analysis of masticatory stress hypotheses

Understanding how the skull transmits and dissipates forces during feeding provides insights into the selective pressures that may have driven the evolution of primate skull morphology. Traditionally, researchers have interpreted masticatory biomechanics in terms of simple global loading regimes applied to simple shapes (i.e., bending in sagittal and frontal planes, dorsoventral shear, and torsion of beams and cylinders). This study uses finite element analysis to examine the extent to which these geometric models provide accurate strain predictions in the face and evaluate whether simple global loading regimes predict strains that approximate the craniofacial deformation pattern observed during mastication. Loading regimes, including those simulating peak loads during molar chewing and those approximating the global loading regimes, were applied to a previously validated finite element model (FEM) of a macaque (Macaca fascicularis) skull, and the resulting strain patterns were compared. When simple global loading regimes are applied to the FEM, the resulting strains do not match those predicted by simple geometric models, suggesting that these models fail to generate accurate predictions of facial strain. Of the four loading regimes tested, bending in the frontal plane most closely approximates strain patterns in the circumorbital region and lateral face, apparently due to masseter muscle forces acting on the zygomatic arches. However, these results indicate that no single simple global loading regime satisfactorily accounts for the strain pattern found in the validated FEM. Instead, we propose that FE models replace simple cranial models when interpreting bone strain data and formulating hypotheses about craniofacial biomechanics.     

Muscular and osseous anatomy of the primate anterior temporal fossa and the functions of the postorbital septum

Many adaptive explanations for anthropoid origins incorporate hypotheses regarding the function of the postorbital septum. Two hypotheses are evaluated here: Cachel's ([1979b] Am. J. Phys. Anthropol. 50:1–18) hypothesis that the anthropoid postorbital septum evolved to augment muscle attachment area in the anterior temporal fossa and Cartmill's ([1980] in RL Ciochon and AB Chiarelli (eds.): Evolutionary Biology of the New World Monkeys and Continental Drift. New York: Plenum, pp. 243–274.) hypothesis that the septum evolved to insulate the foveate eye of haplorhines from movements in the temporal fossa during mastication. Dissections of the masticatory muscles of 55 species of primates, with emphasis on the anatomy of the anterior temporal fossa, reveal that in all anthropoids the temporal muscles take origin from the portion of the septum formed by the frontal bone. In some platyrrhines this muscle is anterior temporalis, and in others it is zygomatico-mandibularis. In tarsiers and most platyrrhines, muscle attachment to the zygomatic portion of the postorbital septum is very restricted (and of possibly varying homologies), whereas in catarrhines the zygomatico-mandibularis arises from the postorbital ridge on the zygomatic portion of the septum. This suggests that, contrary to Cachel's hypothesis, the earliest anthropoids did not have extensive areas of muscle attachment on the postorbital septum, a suggestion supported by the bony morphology of Catopithecus browni. Dissections also indicate that in all haplorhines the anteriormost temporal fibers curve around the postorbital septum between origin and insertion, implying that, were the septum not present, the anterior temporal muscles would disturb the orbital contents when contracting. This suggests that insulation may have been the septum's original function, even in the absence of a retinal fovea. In anthropoids, the rostral migration of the line of action of the anterior temporal muscles relative to the eye is attributed to their possession of extreme degrees of both orbital frontation and convergence; in tarsiers it is attributed to their possession of both massively hypertrophied eyes and moderately convergent and frontated orbits. It is argued that the postorbital septum is most likely to have evolved in a morphological context similar to that exhibited by omomyids. © 1995 Wiley-Liss, Inc.     

Function of the mammalian postorbital bar

Complete postorbital bars, bony arches that encompass the lateral aspect of the eye and form part of a circular orbit, have evolved homoplastically multiple times during mammalian evolution. Numerous functional hypotheses have been advanced for postorbital bars, the most promising being that postorbital bars function to stiffen the lateral orbit in taxa that have significant angular deviation between the temporal fossa and the bony orbit. Without a stiff lateral orbit the anterior temporalis muscle and fascia potentially would pull on the postorbital ligament, deform the orbit, and cause disruption of oculomotor precision. Morphometric data were collected on 1,329 specimens of 324 taxa from 16 orders of extant eutherian and metatherian mammals in order to test whether the orientation of the orbit relative to the temporal fossa is correlated with the replacement of the postorbital ligament with bone. The allometric and ecological influences on orbit orientation across mammals are also explored. The morphometric results corroborate the hypothesis: Shifts in orbit orientation relative to the temporal fossa are correlated with the size of the postorbital processes, which replace the ligament. The allometric and ecological factors that influence orbit orientation vary across taxa. Postorbital bars stiffen the lateral orbital wall. Muscle pulleys, ligaments, and other connective tissue attach to the lateral orbital wall, including the postorbital bar. Without a stiff lateral orbit, deformation due to temporalis contraction would displace soft tissues contributing to normal oculomotor function.     

Compressive and tensile mechanical properties of the porcine nasal septum

The expanding nasal septal cartilage is believed to create a force that powers midfacial growth. In addition, the nasal septum is postulated to act as a mechanical strut that prevents the structural collapse of the face under masticatory loads. Both roles imply that the septum is subject to complex biomechanical loads during growth and mastication. The purpose of this study was to measure the mechanical properties of the nasal septum to determine (1) whether the cartilage is mechanically capable of playing an active role in midfacial growth and in maintaining facial structural integrity and (2) if regional variation in mechanical properties is present that could support any of the postulated loading regimens. Porcine septal samples were loaded along the horizontal or vertical axes in compression and tension, using different loading rates that approximate the in vivo situation. Samples were loaded in random order to predefined strain points (2–10%) and strain was held for 30 or 120 seconds while relaxation stress was measured. Subsequently, samples were loaded until failure. Stiffness, relaxation stress and ultimate stress and strain were recorded. Results showed that the septum was stiffer, stronger and displayed a greater drop in relaxation stress in compression compared to tension. Under compression, the septum displayed non-linear behavior with greater stiffness and stress relaxation under faster loading rates and higher strain levels. Under tension, stiffness was not affected by strain level. Although regional variation was present, it did not strongly support any of the suggested loading patterns. Overall, results suggest that the septum might be mechanically capable of playing an active role in midfacial growth as evidenced by increased compressive residual stress with decreased loading rates. However, the low stiffness of the septum compared to surrounding bone does not support a strut role. The relatively low stiffness combined with high stress relaxation under fast loading rates suggests that the nasal septum is a stress dampener, helping to absorb and dissipate loads generated during mastication.     

Electromyography of the anterior temporalis and masseter muscles of owl monkeys (Aotus trivirgatus) and the function of the postorbital septum

Anthropoids and tarsiers are distinguished from all other vertebrates by the possession of a postorbital septum, which is formed by the frontal, alisphenoid, and zygomatic bones. Cartmill [(1980) In: Evolutionary Biology of the New World Monkeys and Continental Drift. New York: Plenum, p 243-274] suggested that the postorbital septum evolved in the stem lineage of tarsiers and anthropoids to insulate the eye from movements arising in the temporal fossa. Ross [(1996) Am J Phys Anthropol 91:305-324] suggested that the septum insulates the orbital contents from incursions by the line of action of the anterior temporal muscles caused by the unique combination of high degrees of orbital frontation and convergence. Both of these hypotheses must explain why insulation of the orbital contents could not be achieved by decreasing the size of the anterior temporal musculature with a corresponding increase in size of the remaining jaw adductors, rather than evolving a postorbital septum. One possibility is that the anterior temporalis is an important contributor to vertically directed bite forces during all biting and chewing activities. Another possibility is that reduction in anterior temporal musculature would compromise the ability to produce powerful bite forces, either at the incisors or along the postcanine toothrow. To evaluate these hypotheses, electromyographic (EMG) recordings were made from the masseter muscle and the anterior and posterior portions of the temporalis muscles of two owl monkeys, Aotus trivirgatus. The EMG data indicate that anterior temporalis activity relative to that of the superficial masseter is lower during incision than mastication. In addition, activity of the anterior temporalis is not consistently higher than the posterior temporalis during incision. The data indicate relatively greater activity of anterior temporalis compared to other muscles during isometric biting on the postcanine toothrow. This may be due to decreased activity in superficial masseter and posterior temporalis, rather than elevated anterior temporalis activity. The anterior temporalis is not consistently less variable in activity than the superficial masseter and posterior temporalis. The EMG data gathered here indicate no reason for suggesting that the anterior temporal muscles in anthropoids are utilized especially for incisal preparation of hard fruits. Maintenance of relatively high EMG activity in anterior temporalis across a wide range of biting behaviors is to be expected in a vertically oriented and rostrally positioned muscle such as this because, compared to the posterior temporalis, superficial masseter and medial pterygoid, it can contribute relatively larger vertical components of force to bites along the postcanine toothrow. The in vivo data do not support this hypothesis, possibly because of effects of bite point and bite force orientation.     

Patterns of strain in the macaque ulna during functional activity

In vivo bone strain experiments were performed on the ulnae of three female rhesus macaques to test how the bone deforms during locomotion. The null hypothesis was that, in an animal moving its limbs predominantly in sagittal planes, the ulna experiences anteroposterior bending. Three rosette strain gauges were attached around the circumference of the bone slightly distal to midshaft. They permit a complete characterization of the ulna's loading environment. Strains were recorded during walking and galloping activities. Principal strains and strain directions relative to the long axis of the bone were calculated for each gauge site. In all three animals, the lateral cortex experienced higher tensile than compressive principal strains during the stance phase of walking. Compressive strains predominated at the medial cortex of two animals (the gauge on this cortex of the third animal did not function). The posterior cortex was subject to lower strains; the nature of the strain was highly dependent on precise gauge position. The greater principal strains were aligned closely with the long axis of the bone in two animals, whereas they deviated up to 45° from the long axis in the third animal. A gait change from walk to gallop was recorded for one animal. It was not accompanied by an incremental change in strain magnitudes. Strains are at the low end of the range of strain magnitudes recorded for walking gaits of nonprimate mammals. The measured distribution of strains in the rhesus monkey ulna indicates that mediolateral bending, rather than anteroposterior bending, is the predominant loading regime, with the neutral axis of bending running from anterior and slightly medial to posterior and slightly lateral. A variable degree of torsion was superimposed over this bending regime. Ulnar mediolateral bending is apparently caused by a ground reaction force vector that passes medial to the forearm. The macaque ulna is not reinforced in the plane of bending. The lack of buttressing in the loaded plane and the somewhat counterintuitive bending direction recommend caution with regard to conventional interpretations of long bone cross-sectional geometry. Am J Phys Anthropol 106:87–100, 1998. © 1998 Wiley-Liss, Inc.     

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.     

The functional significance of primate mandibular form.

A stress analysis of the primate mandible suggests that vertically deep jaws in the molar region are usually an adaptation to counter increased sagittal bending stress about the balancing-side mandibular corpus during unilateral mastication. This increased bending stress about the balancing side is caused by an increase in the amount of balancing-side muscle force. Furthermore, this increased muscle force will also cause an increase in dorso-ventral shear stress along the mandibular symphysis. Since increased symphyseal stress can be countered by symphyseal fusion and as increased bending stress can be countered by a deeper jaw, deep jaws and symphyseal fusion are often part of the same functional pattern. In some primates (e.g., Cercocebus albigena), deep jaws are an adaptation to counter bending in the sagittal plane during powerful incisor biting, rather than during unilateral mastication. The stress analysis of the primate mandible also suggests that jaws which are transversely thick in the molar region are an adaptation to counter increased torsion about the long axis of the working-side mandibular corpus during unilateral mastication. Increased torsion of the mandibular corpus can be caused by an increase in masticatory muscle force, an increase in the transverse component of the postcanine bite force and/or an increase in premolar use during mastication. Patterns of masticatory muscle force were estimated for galagos and macaques, demonstrating that the ratio of working-side muscle force to balancing-side muscle force is approximately 1.5:1 in macaques and 3.5:1 in galagos during unilateral isometric molar biting. These data support the hypothesis that mandibular symphyseal fusion is an adaptative response to maximize unilateral molar bite force by utilizing a greater percentage of balancing-side muscle force.     

Morphology of the interorbital region of Saimiri sciureus

The skull of the platyrrhine primate Saimiri sciureus is distinguished by a large interorbital fenestra. Juvenile skulls still show a bony interorbital septum with some small gaps. A morphogenetic study was undertaken to better understand the structures of the interorbital region, which represents a linkage between the base of the braincase and the nasal skeleton. Already in early ontogenetic stages a reduction of the posterior portion of the nasal capsule and of the cartilaginous interorbital septum are observed, resulting in the formation of a primary interorbital fenestra. A bony interorbital septum is mainly formed in perinatal age stages by ossification of the presphenoid and by medial fusion of the frontals; the primary interorbital fenestra is retained as a small opening. It only occurs in late juvenile stages when the definitive interorbital fenestra develops by by secondary transformation of bone into a membrane of dense connective tissue; this process is most probably caused by mechanical friction of the very closely approximated eyes of both sides.     

Experimental analysis of temporomandibular joint reaction force in macaques

Mandibular bone strain in the region immediately below the temporomandibular ligament was analyzed in adult and sub-adult Macaca fascicularis and Macaca mulatta. Following recovery from the general anesthetic, the monkeys were presented food objects, a wooden rod, or a specially designed bite-force transducer. Bone strain was recorded during incisal biting and mastication of food, and also during isometric biting of the rod and/or the transducer. The bone strain data suggest the following: The macaque TMJ is loaded by a compressive reaction force during the power stroke of mastication and incision of food, and during isometric molar and incisor biting. TMJ reaction forces are larger on the contralateral side during both mastication and isometric molar biting. Patterns of ipsilateral TMJ reaction force in macaques during isometric biting vary markedly in response to the position of the bite point. During biting along the premolars or first two molars a compressive reaction force acts about the ipsilateral TMJ; however, when the bite point is positioned along the M3, the ipsilateral TMJ has either very little compressive stress, no stress, or it is loaded in tension.     

Deformation of nasal septal cartilage during mastication

The cartilaginous nasal septum plays a major role in structural integrity and growth of the face, but its internal location has made physiologic study difficult. By surgically implanting transducers in 10 miniature pigs (Sus scrofa), we recorded in vivo strains generated in the nasal septum during mastication and masseter stimulation. The goals were (1) to determine whether the cartilage should be considered as a vertical strut supporting the nasal cavity and preventing its collapse, or as a damper of stresses generated during mastication and (2) to shed light on the overall pattern of snout deformation during mastication. Strains were recorded simultaneously at the septo‐ethmoid junction and nasofrontal suture during mastication. A third location in the anterior part of the cartilage was added during masseter stimulation and manipulation. Contraction of jaw closing muscles during mastication was accompanied by anteroposterior compressive strains (around ?1,000 με) in the septo‐ethmoid junction. Both the orientation and the magnitude of the strain suggest that the septum does not act as a vertical strut but may act in absorbing loads generated during mastication. The results from masseter stimulation and manipulation further suggest that the masticatory strain pattern arises from a combination of dorsal bending and/or shearing and anteroposterior compression of the snout. J. Morphol., 2009. © 2009 Wiley‐Liss, Inc.     

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.