Ontogenetic changes to muscle architectural properties within the jaw-adductor musculature of Macaca fascicularis.

OBJECTIVES: Changes to soft- and hard-tissue components of the masticatory complex during development can impact functional performance by altering muscle excursion potential, maximum muscle forces, and the efficiency of force transfer to specific bitepoints. Within Macaca fascicularis, older individuals exploit larger, more mechanically resistant food items and more frequently utilize wide-gape jaw postures. We therefore predict that key architectural and biomechanical variables will scale during ontogeny to maximize bite force and gape potential within older, larger-bodied individuals. MATERIALS AND METHODS: We analyzed 26 specimens of M. fascicularis, representing a full developmental spectrum. The temporalis, superficial masseter, and deep masseter were dissected to determine muscle mass, fiber length, and physiologic cross-sectional area (PCSA). Lever-arm lengths were also measured for each muscle, alongside the height of the temporomandibular joint (TMJ) and basicranial length. These variables were scaled against two biomechanical variables (jaw length and condyle-molar length) to determine relative developmental changes within these parameters. RESULTS: During ontogeny, muscle mass, fiber length, and PCSA scaled with positive allometry relative to jaw length and condyle-molar length within all muscles. TMJ height also scaled with positive allometry, while muscle lever arms scaled with isometry relative to jaw length and with positive allometry (temporalis) or isometry (superficial and deep masseter) relative to condyle-molar length. CONCLUSION: Larger individuals demonstrate adaptations during development towards maximizing gape potential and bite force potential at both an anterior and posterior bitepoint. These data provide anatomical evidence to support field observations of dietary and behavioral differences between juvenile and adult M. fascicularis.

Mechanical adaptation of trabecular bone morphology in the mammalian mandible.

Alveolar bone, together with the underlying trabecular bone, fulfils an important role in providing structural support against masticatory forces. Diseases such as osteoporosis or periodontitis cause alveolar bone resorption which weakens this structural support and is a major cause of tooth loss. However, the functional relationship between alveolar bone remodelling within the molar region and masticatory forces is not well understood. This study investigated this relationship by comparing mammalian species with different diets and functional loading (Felis catus, Cercocebus atys, Homo sapiens, Sus scrofa, Oryctolagus cuniculus, Ovis aries). We performed histomorphometric analyses of trabecular bone morphology (bone volume fraction, trabecular thickness and trabecular spacing) and quantified the variation of bone and tooth root volumes along the tooth row. A principal component analysis and non-parametric MANOVA showed statistically significant differences in trabecular bone morphology between species with contrasting functional loading, but these differences were not seen in sub-adult specimens. Our results support a strong, but complex link between masticatory function and trabecular bone morphology. Further understanding of a potential functional relationship could aid the diagnosis and treatment of mandibular diseases causing alveolar bone resorption, and guide the design and evaluation of dental implants.

The biting performance of Homo sapiens and Homo heidelbergensis.

Modern humans have smaller faces relative to Middle and Late Pleistocene members of the genus Homo. While facial reduction and differences in shape have been shown to increase biting efficiency in Homo sapiens relative to these hominins, facial size reduction has also been said to decrease our ability to resist masticatory loads. This study compares crania of Homo heidelbergensis and H. sapiens with respect to mechanical advantages of masticatory muscles, force production efficiency, strains experienced by the cranium and modes of deformation during simulated biting. Analyses utilize X-ray computed tomography (CT) scan-based 3D models of a recent modern human and two H. heidelbergensis. While having muscles of similar cross-sectional area to H. heidelbergensis, our results confirm that the modern human masticatory system is more efficient at converting muscle forces into bite forces. Thus, it can produce higher bite forces than Broken Hill for equal muscle input forces. This difference is the result of alterations in relative in and out-lever arm lengths associated with well-known differences in midfacial prognathism. Apparently at odds with this increased efficiency is the finding that the modern human cranium deforms more, resulting in greater strain magnitudes than Broken Hill when biting at the equivalent tooth. Hence, the facial reduction that characterizes modern humans may not have evolved as a result of selection for force production efficiency. These findings provide further evidence for a degree of uncoupling between form and function in the masticatory system of modern humans. This may reflect the impact of food preparation technologies. These data also support previous suggestions that differences in bite force production efficiency can be considered a spandrel, primarily driven by the midfacial reduction in H. sapiens that occurred for other reasons. Midfacial reduction plausibly resulted in a number of other significant changes in morphology, such as the development of a chin, which has itself been the subject of debate as to whether or not it represents a mechanical adaptation or a spandrel.

Technological Analysis of the World's Earliest Shamanic Costume: A Multi-Scalar, Experimental Study of a Red Deer Headdress from the Early Holocene Site of Star Carr, North Yorkshire, UK.

Shamanic belief systems represent the first form of religious practice visible within the global archaeological record. Here we report on the earliest known evidence of shamanic costume: modified red deer crania headdresses from the Early Holocene site of Star Carr (c. 11 kya). More than 90% of the examples from prehistoric Europe come from this one site, establishing it as a place of outstanding shamanistic/cosmological significance. Our work, involving a programme of experimental replication, analysis of macroscopic traces, organic residue analysis and 3D image acquisition, metrology and visualisation, represents the first attempt to understand the manufacturing processes used to create these artefacts. The results produced were unexpected--rather than being carefully crafted objects, elements of their production can only be described as expedient.

Validity and sensitivity of a human cranial finite element model: implications for comparative studies of biting performance.

Finite element analysis (FEA) is a modelling technique increasingly used in anatomical studies investigating skeletal form and function. In the case of the cranium this approach has been applied to both living and fossil taxa to (for example) investigate how form relates to function or infer diet or behaviour. However, FE models of complex musculoskeletal structures always rely on simplified representations because it is impossible completely to image and represent every detail of skeletal morphology, variations in material properties and the complexities of loading at all spatial and temporal scales. The effects of necessary simplifications merit investigation. To this end, this study focuses on one aspect, model geometry, which is particularly pertinent to fossil material where taphonomic processes often destroy the finer details of anatomy or in models built from clinical CTs where the resolution is limited and anatomical details are lost. We manipulated the details of a finite element (FE) model of an adult human male cranium and examined the impact on model performance. First, using digital speckle interferometry, we directly measured strains from the infraorbital region and frontal process of the maxilla of the physical cranium under simplified loading conditions, simulating incisor biting. These measured strains were then compared with predicted values from FE models with simplified geometries that included modifications to model resolution, and how cancellous bone and the thin bones of the circum-nasal and maxillary regions were represented. Distributions of regions of relatively high and low principal strains and principal strain vector magnitudes and directions, predicted by the most detailed FE model, are generally similar to those achieved in vitro. Representing cancellous bone as solid cortical bone lowers strain magnitudes substantially but the mode of deformation of the FE model is relatively constant. In contrast, omitting thin plates of bone in the circum-nasal region affects both mode and magnitude of deformation. Our findings provide a useful frame of reference with regard to the effects of simplifications on the performance of FE models of the cranium and call for caution in the interpretation and comparison of FEA results.

The impact of simplifications on the performance of a finite element model of a Macaca fascicularis cranium.

In recent years finite element analysis (FEA) has emerged as a useful tool for the analysis of skeletal form-function relationships. While this approach has obvious appeal for the study of fossil specimens, such material is often fragmentary with disrupted internal architecture and can contain matrix that leads to errors in accurate segmentation. Here we examine the effects of varying the detail of segmentation and material properties of teeth on the performance of a finite element model of a Macaca fascicularis cranium within a comparative functional framework. Cranial deformations were compared using strain maps to assess differences in strain contours and Procrustes size and shape analyses, from geometric morphometrics, were employed to compare large scale deformations. We show that a macaque model subjected to biting can be made solid, and teeth altered in material properties, with minimal impact on large scale modes of deformation. The models clustered tightly by bite point rather than by modeling simplification approach, and fell out as being distinct from another species. However localized fluctuations in predicted strain magnitudes were recorded with different modeling approaches, particularly over the alveolar region. This study indicates that, while any model simplification should be undertaken with care and attention to its effects, future applications of FEA to fossils with unknown internal architecture may produce reliable results with regard to general modes of deformation, even when detail of internal bone architecture cannot be reliably modeled.

Masticatory biomechanics in the rabbit: a multi-body dynamics analysis.

Multi-body dynamics is a powerful engineering tool which is becoming increasingly popular for the simulation and analysis of skull biomechanics. This paper presents the first application of multi-body dynamics to analyse the biomechanics of the rabbit skull. A model has been constructed through the combination of manual dissection and three-dimensional imaging techniques (magnetic resonance imaging and micro-computed tomography). Individual muscles are represented with multiple layers, thus more accurately modelling muscle fibres with complex lines of action. Model validity was sought through comparing experimentally measured maximum incisor bite forces with those predicted by the model. Simulations of molar biting highlighted the ability of the masticatory system to alter recruitment of two muscle groups, in order to generate shearing or crushing movements. Molar shearing is capable of processing a food bolus in all three orthogonal directions, whereas molar crushing and incisor biting are predominately directed vertically. Simulations also show that the masticatory system is adapted to process foods through several cycles with low muscle activations, presumably in order to prevent rapidly fatiguing fast fibres during repeated chewing cycles. Our study demonstrates the usefulness of a validated multi-body dynamics model for investigating feeding biomechanics in the rabbit, and shows the potential for complementing and eventually reducing in vivo experiments.

Developing a musculoskeletal model of the primate skull: predicting muscle activations, bite force, and joint reaction forces using multibody dynamics analysis and advanced optimisation methods.

An accurate, dynamic, functional model of the skull that can be used to predict muscle forces, bite forces, and joint reaction forces would have many uses across a broad range of disciplines. One major issue however with musculoskeletal analyses is that of muscle activation pattern indeterminacy. A very large number of possible muscle force combinations will satisfy a particular functional task. This makes predicting physiological muscle recruitment patterns difficult. Here we describe in detail the process of development of a complex multibody computer model of a primate skull (Macaca fascicularis), that aims to predict muscle recruitment patterns during biting. Using optimisation criteria based on minimisation of muscle stress we predict working to balancing side muscle force ratios, peak bite forces, and joint reaction forces during unilateral biting. Validation of such models is problematic; however we have shown comparable working to balancing muscle activity and TMJ reaction ratios during biting to those observed in vivo and that peak predicted bite forces compare well to published experimental data. To our knowledge the complexity of the musculoskeletal model is greater than any previously reported for a primate. This complexity, when compared to more simple representations provides more nuanced insights into the functioning of masticatory muscles. Thus, we have shown muscle activity to vary throughout individual muscle groups, which enables them to function optimally during specific masticatory tasks. This model will be utilised in future studies into the functioning of the masticatory apparatus.

The application of muscle wrapping to voxel-based finite element models of skeletal structures.

Finite elements analysis (FEA) is now used routinely to interpret skeletal form in terms of function in both medical and biological applications. To produce accurate predictions from FEA models, it is essential that the loading due to muscle action is applied in a physiologically reasonable manner. However, it is common for muscle forces to be represented as simple force vectors applied at a few nodes on the model's surface. It is certainly rare for any wrapping of the muscles to be considered, and yet wrapping not only alters the directions of muscle forces but also applies an additional compressive load from the muscle belly directly to the underlying bone surface. This paper presents a method of applying muscle wrapping to high-resolution voxel-based finite element (FE) models. Such voxel-based models have a number of advantages over standard (geometry-based) FE models, but the increased resolution with which the load can be distributed over a model's surface is particularly advantageous, reflecting more closely how muscle fibre attachments are distributed. In this paper, the development, application and validation of a muscle wrapping method is illustrated using a simple cylinder. The algorithm: (1) calculates the shortest path over the surface of a bone given the points of origin and ultimate attachment of the muscle fibres; (2) fits a Non-Uniform Rational B-Spline (NURBS) curve from the shortest path and calculates its tangent, normal vectors and curvatures so that normal and tangential components of the muscle force can be calculated and applied along the fibre; and (3) automatically distributes the loads between adjacent fibres to cover the bone surface with a fully distributed muscle force, as is observed in vivo. Finally, we present a practical application of this approach to the wrapping of the temporalis muscle around the cranium of a macaque skull.

Combining geometric morphometrics and functional simulation: an emerging toolkit for virtual functional analyses.

The development of virtual methods for anatomical reconstruction and functional simulation of skeletal structures offers great promise in evolutionary and ontogenetic investigations of form-function relationships. Key developments reviewed here include geometric morphometric methods for the analysis and visualization of variations in form (size and shape), finite element methods for the prediction of mechanical performance of skeletal structures under load and multibody dynamics methods for the simulation and prediction of musculoskeletal function. These techniques are all used in studies of form and function in biology, but only recently have they been combined in novel ways to facilitate biomechanical modelling that takes account of variations in form, can statistically compare performance, and relate performance to form and its covariates. Here we provide several examples that illustrate how these approaches can be combined and we highlight areas that require further investigation and development before we can claim a mature theory and toolkit for a statistical biomechanical framework that unites these methods.