The ontogeny of sexual dimorphism in the African apes

The relationship between the growth spurt and the onset of sexual maturity is problematic in nonhuman primates. Growth data on the cranium and postcranium of dentally aged pygmy chimpanzees, common chimpanzees, and gorillas are reported here. In all three species, male means generally exceed female means throughout growth, with the exception that females exhibit a spurt during one dental-age stage when they become generally larger than the males. This female spurt occurs earlier in an absolute and relative sense in the gorillas than the chimpanzees. These growth data support field and laboratory observations suggesting that female gorillas become sexually mature earlier than do female chimpanzees. Gorillas are thus characterized by a greater degree of “sexual bimaturism” than are the chimpanzees. Implications of these differences in terms of size dimorphism, mating systems, and morphology are discussed.     

Cyclic development of contact behavior in apes and humans

Nursing and mother-infant distance were observed in three orangutans, two gorillas, one chimpanzee and four humans. All four species showed periods of a recurrence of greater time spent nursing and in contact with the mother. The initial regressive or reattachment period occurred similarly in all four species at between 6–12 months of age. An orangutan observed for two years showed a second period at 19–21 months. Other studies of weight gain in the three ape species coincidently peaked at the same time. When estimated peaks of individuals of each species were summed, the resulting graphs showed a differentiation of species rates of development. Gorillas developed most rapidly, orangutans developed most slowly, while chimpanzees and humans developed within the middle range.     

Functional analysis of the rabbit temporomandibular joint using dynamic biplane imaging

The dynamic function of the rabbit temporomandibular joint (TMJ) was analyzed through non-invasive, three-dimensional skeletal kinematics, providing essential knowledge for understanding normal joint motion. The objective of this study was to evaluate and determine repeatable measurements of rabbit TMJ kinematics. Maximal distances, as well as paths were traced and analyzed for the incisors and for the condyle–fossa relationship. From one rabbit to another, the rotations and translations of both the incisors and the condyle relative to the fossa contained multiple clear, repeatable patterns. The slope of the superior/inferior incisor distance with respect to the rotation about the transverse axis was repeatable to 0.14 mm/deg and the right/left incisor distance with respect to the rotation about the vertical axis was repeatable to 0.03 mm/deg. The slope of the superior/inferior condylar translation with respect to the rotational movement about the transverse axis showed a consistent relationship to within 0.05 mm/deg. The maximal translations of the incisors and condyles were also consistent within and between rabbits. With an understanding of the normal mechanics of the TMJ, kinematics can be used to compare and understand TMJ injury and degeneration models.     

Relative growth of the limbs and trunk in the African apes

Examination of relative growth and allometry is important for our understanding of the African apes, as they represent a closely related group of species of increasing body size. This study presents a comparison of ontogenetic relative growth patterns of some postcranial dimensions in Pan paniscus, Pantroglodytes, and Gorilla gorilla. Interspecific proportion differences among the three species are also analyzed. It is stressed that reliable ontogenetic information can only be obtained if subadults are examined-growth data cannot be inferred from static adult scaling. Results indicate that some postcranial relative growth patterns are very similar in the three species, suggesting differential extrapolation of a common growth pattern, whereas for other proportion comparisons the growth trends differ markedly among the species, producing distinct shape differences in the adults Interspecific shape changes among the three species are characterized by positive allometry of chest girth and negative allometry of body height and leg length. It is suggested that relative decrease of leg length with increasing body size among the African pongids might be expected on biomechanical grounds, in order to maintain similar locomotor abilities of climbing arborealism and quadrupedal terrestrialism. Relative to body weight or trunk length, the limbs of the bonobo (Pan paniscus) are longer than in the common chimpanzee or the gorilla, with a lower intermembral index. This may most closely resemble the primitive condition for the African apes.     

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.     

The ontogeny of sexual dimorphism in the facial skeleton of the African apes

This paper aims to test the contribution of ontogenetic scaling to sexual dimorphism of the facial skeleton in the African apes. Specifically, it addresses whether males and females of each species share a common postnatal ontogenetic shape trajectory for the facial skeleton. Where trajectories are found to differ, it is tested whether male and female trajectories: 1) diverge early, or 2) diverge later after sharing a common trajectory earlier in the postnatal period. Where ontogenetic shape trajectories are found to be shared, it is also tested whether males and females are ontogenetically scaled. This study uses geometric morphometric analyses of 28 landmarks from the facial skeletons of 137 G. g. gorilla (62 adults; 75 juveniles), 95 P. paniscus (34 adults; 61 juveniles), and 115 P. t. troglodytes (58 adults; 57 juveniles). On average, males and females share a common ontogenetic shape trajectory until around the eruption of the second permanent molars. In addition, for the same period, males and females in each species share a common ontogenetic scaling trajectory. After this period, males and females diverge both from each other and from the common juvenile ontogenetic shape and scaling trajectories within each species. Thus, the male and female facial skeleton shows ontogenetic scaling until around the point of the eruption of the second molar (i.e., around puberty and the development of secondary sexual characteristics), but subsequent sexual dimorphism occurs via divergent trajectories and not via ontogenetic scaling.     

Cytokine profile in the synovial fluid of patients with temporomandibular joint disorders: A systematic review

The aim of this study was to review the cytokine profiles in the synovial fluid (SF) of patients with temporomandibular joint disorders (TMJD). Databases were searched from 1965 till September 2015 using different combinations of the following key words: “Temporomandibular joint”; “Cytokine”; “disorder”; and “synovial fluid” and “inflammation”. Titles and abstracts of studies identified using the above-described protocol were screened and checked for agreement. Full-texts of articles judged by title and abstract to be relevant were read and independently evaluated. Hand-searching of the reference lists of potentially relevant original and review articles was also performed. The pattern of the present systematic review was customized to mainly summarize the relevant data. Fifteen studies were included. In 12 studies, cytokine profile of patients with TMJD was assessed using enzyme linked immunosorbent assay; and in 2 studies, histological analysis was performed to assess the cytokine profile of patients with TMJD. Patients with TMJD presented raised levels of interleukin (IL)-6 in 8 studies, IL-1beta (1β) in 5 studies and tumor necrosis factor-alpha (TNF-α) in 5 studies. Two studies showed no significant difference in TNF-α levels in patients with and without TMJD; and IL-1β levels were comparable in patients with and without TMJD in 2 studies. Raised levels of IL-6, TNF-α, IL-1β, IL-8, and IFN-γ in the SF have been associated with inflammation in patients with TMJD. Cytokines IL-10, osteoclastogenesis inhibitory factor/osteoprotegerin (OCIF/OPG), and VEGF found in the SF of TMJs could have an anti-inflammatory effect.     

Capsaicin receptor expression in the rat temporomandibular joint

Experimentally, temporomandibular joint (TMJ) nerve units respond to capsaicin, which is used clinically to treat TMJ pain. However, the existence of capsaicin receptors in the TMJ has not previously been clearly demonstrated. Immunohistochemical analysis has revealed the presence of transient receptor potential vanilloid subtype 1 (TRPV1) expression in the nerves and synovial lining cells of the TMJ. TRPV1-immunoreactive nerves are distributed in the synovial membrane of the joint capsule and provide branches to the joint compartment. The disc periphery is supplied by TRPV1 nerves that are mostly associated with small arterioles, and occasional nerves penetrate to the synovial lining layer. Double immunofluorescence has shown that many TRPV1-immunoreactive nerves are labeled with neuropeptide calcitonin gene-related peptide, whereas few are labeled with IB4-lectin. The results provide evidence for the presence of TRPV1 in both nerves and synovial lining cells, which might thus be involved in the mechanism of nociception and inflammation in the TMJ. This study was supported by a grant-in-aid for Scientific Research (C), no. 15591938, from the Japanese Ministry of Education, Science, Sports, Culture, and Technology (to M.A.K.).     

Expression and localization of versican during postnatal development of rat temporomandibular joint disc

To analyze the growth-related changes in extracellular matrix components in temporomandibular joint (TMJ) discs, the expression and localization of the core protein of a large chondroitin sulphate proteoglycan, versican, in rat TMJ discs during postnatal development (2–32 weeks) were examined using Western blot analysis, real-time quantitative PCR and immunohistochemistry. Western blot analysis showed that rat TMJ discs predominantly expressed one isoform (V1) and the core protein sharply increased after birth, reached a peak at 8 weeks, and then gradually decreased up to 32 weeks. Real-time quantitative PCR with TaqMan probes indicated that mRNA expression of versican was highest at 2 weeks and gradually decreased with growth. An immunohistochemical study showed that staining for versican was weak and evenly distributed in TMJ discs at 2 weeks. Regional differences in staining for versican became prominent after 8 weeks; staining was intense in the anterior and posterior peripheral attachments, and weak in the central part of the discs. These results demonstrate that growth-related changes and regional differences exist in the expression of versican in the TMJ discs of growing rats, and these probably reflect the changes in the biomechanical environment caused by the development of orofacial functions.     

Handedness in great apes: A review of findings

We present data on hand preference in great apes and discuss them in the context of theoretical models of hand preference in nonhuman primates presented by MacNeilageet al. (1987) and by Fagot and Vauclair (1991). We also discuss several methodological and statistical issues as they pertain to the assessment of hand preference in great apes and other primate species. Finally, we present a comparative framework for the study of hand preference, emphasizing the importance of studies with great apes in developing evolutionary models of hemispheric specialization.     

Convergence of nociceptive information from temporomandibular joint and tooth pulp afferents on C1 spinal neurons in the rat

The aim of the present study was to test the hypothesis that there is a convergence of afferent inputs from the temporomandibular joint (TMJ) on C1 spinal neurons responding to electrical stimulation of the tooth pulp (TP). In 14 pentobarbital anesthetized rats, the extracellular single unit activity of 31 C1 spinal neurons and the amplitude in a digastric muscle electromyogram (n = 31) increased proportionally during 1.0-3.5 times the threshold for the jaw-opening reflex (JOR). Of 31 C1 spinal neurons responsive to TP afferents, 28 (approximately 90%) were also excited by electrical stimulation of the ipsilateral TMJ capsule. All neurons tested were divided into three categories of nociceptive specific, wide dynamic range and non-responsive as to their responsiveness to mechanical stimuli (pin prick and touch) of the somatic receptive field (skin of the face, neck, jaw and upper forearm) and TMJ capsule. Nineteen (68%) of 28 C1 spinal neurons received nociceptive information from C fibers of the TMJ capsule. These results suggest that there is a convergence of noxious information from the TMJ and TP afferents on the same C1 spinal neurons, which importantly contribute to pain perception from the TMJ region.     

Activation of the hypoxia-inducible factor-1 in overloaded temporomandibular joint, and induction of osteoclastogenesis

Vascular endothelial growth factor (Vegf) was previously shown to be expressed specifically in the condylar cartilage of temporomandibular joint-osteoarthritis (TMJ-OA) model rats. Here we demonstrate for the first time that hypoxia-inducible factor-1α (Hif-1α) is activated in mature chondrocytes of temporomandibular joint-osteoarthritis (TMJ-OA) model rat by mechanical overload, and that activated Hif-1 in chondrocytes can induce osteoclastogenesis via repression of osteoprotegerin (Opg) expression.In rat TMJs, degeneration of the condylar cartilage became prominent in proportion to the duration of overloading. Hif-1α expression was observed specifically in mature and hypertrophic chondrocytes, and Hif-1α-positivity, level of Vegf expression, and tartrate-resistant acid phosphatase (TRAP)-positive cell numbers all increased in the same manner. When ATDC5 cells induced differentiation by insulin were cultured under hypoxia, Hif-1α induction was observed in mature stage, but not in immature stage. Inductions of Hif-1-target genes showed a similar expression pattern. In addition, expression of Opg decreased in hypoxia, and Hif-1α played a role, in part, in its regulation.     

Phyletic size change and brain/body allometry: A consideration based on the African pongids and other primates

A problematic aspect of brain/body allometry is the frequency of interspecific series which exhibit allometry coefficients of approximately 0.33. This coefficient is significantly lower than the 0.66 value which is usually taken to be the interspecific norm. A number of explanations have been forwarded to account for this finding. These include (1) intraspecificallometry explanations, (2) nonallometric explanations, and (3) Jerison’s “extraneurons” hypothesis, among others. The African apes, which exhibit a lowered interspecific allometry coefficient, are used here to consider previous explanations. These are found to be inadequate in a number of ways, and an alternative explanation is proposed. This explanation is based on patterns of brain and body size change during ontogeny and phytogeny. It is argued that the interspecific allometry coefficient in African apes parallels the intraspecific one because similar ontogenetic modifications of body growth separate large and small forms along each curve. In both cases, body size differences are produced primarily by growth in later postnatal periods, during which little brain growth occurs. Data on body growth, neonatal scaling, and various lifehistory traits support this explanation. This work extends previous warnings that sizecorrected estimates of relative brain size may not correspond very closely to our understanding of the behavioral capacities of certain species in lineages characterized by rapid change in body size.     

Shox2-deficiency leads to dysplasia and ankylosis of the temporomandibular joint in mice

The temporomandibular joint (TMJ) is a unique synovial joint whose development differs from the formation of other synovial joints. Mutations have been associated with the developmental defects of the TMJ only in a few genes. In this study, we report the expression of the homeobox gene Shox2 in the cranial neural crest derived mesenchymal cells of the maxilla-mandibular junction and later in the progenitor cells and undifferentiated chondrocytes of the condyle as well as the glenoid fossa of the developing TMJ. A conditional inactivation of Shox2 in the cranial neural crest-derived cells causes developmental abnormalities in the TMJ, including dysplasia of the condyle and glenoid fossa. The articulating disc forms but fuses with the fibrous layers of the condyle and glenoid fossa, clinically known as TMJ ankylosis. Histological examination indicates a delay in development in the mutant TMJ, accompanied by a significantly reduced rate of cell proliferation. In situ hybridization further demonstrates an altered expression of several key osteogenic genes and a delayed expression of the osteogenic differentiation markers. Shox2 appears to regulate the expression of osteogenic genes and is essential for the development and function of the TMJ. The Shox2 conditional mutant thus provides a unique animal model of TMJ ankylosis.     

Effects of several temporomandibular disorders on the stress distributions of temporomandibular joint: a finite element analysis

The aim of this study was to evaluate stress distributions in the temporomandibular joints (TMJs) with temporomandibular disorders (TMDs) for comparison with healthy TMJs. A model of mandible and normal TMJs was developed according to CT images. The interfaces between the discs and the articular cartilages were treated as contact elements. Nonlinear cable elements were used to simulate disc attachments. Based on this model, seven models of various TMDs were established. The maximum stresses of the discs with anterior, posterior, medial and lateral disc displacement (ADD, PDD, MDD and LDD) were 12.09, 9.33, 10.71 and 6.07 times magnitude of the identically normal disc, respectively. The maximum stresses of the posterior articular eminences in ADD, PDD, MDD, LDD, relaxation of posterior attachments and disc perforation models were 21, 59, 46, 21, 13 and 15 times greater than the normal model, respectively. TMDs could cause increased stresses in the discs and posterior articular eminences.     

Biomechanical association of dental and temporomandibular pathology in a medieval Nubian population

An analysis of the relationship between oral pathology and degenerative change at the temporomandibular joint (TMJ) was undertaken on an archaeological sample of 122 adult crania from the Medieval site of Kulubnarti in Sudanese Nubia. The crania were sorted into 2 groups: those demonstrating clearly visible bony changes at the joint (TMJ+) and those without visible change (TMJ-). These groups were compared according to 1) age; 2) sex; 3) active dental pathologies (abscesses, caries, partial socket resorption); 4) tooth loss with complete socket resorption; and 5) dental attrition. No statistically significant association was evident between degenerative change at the TMJ and age, active dental pathologies, or dental attrition; however, sex differences and posterior tooth loss with complete socket resorption revealed a significant correspondence to degenerative TMJ changes. Both of these factors agree with the clinical literature and with biomechanical models (most notably that of Hylander) based upon modern populations. Furthermore, the results support the contention that paleopathological conditions can be analyzed from a clinical and functional biomechanical perspective.     

Memory processing in great apes: the effect of time and sleep

Following encoding, memory remains temporarily vulnerable to disruption. Consolidation refers to offline time-dependent processes that continue after encoding and stabilize, transform or enhance the memory trace. Memory consolidation resulting from sleep has been reported for declarative and non-declarative memories in humans. We first investigated the temporal course of memory retrieval in chimpanzees, bonobos and orangutans. We found that the amount of retrieved information was time dependent: apes' performance degraded after 1 and 2 h, stabilized after 4 h, started to increase after 8 and 12 h and fully recovered after 24 h. Second, we show that although memories during wakefulness were highly vulnerable to interference from events similar to those witnessed during the original encoding event, an intervening period of sleep not only stabilized apes' memories into more permanent ones but also protected them against interference.