Laura C. Fitton

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.

Masticatory loadings and cranial deformation in Macaca fascicularis: a finite element analysis sensitivity study.

Biomechanical analyses are commonly conducted to investigate how craniofacial form relates to function, particularly in relation to dietary adaptations. However, in the absence of corresponding muscle activation patterns, incomplete muscle data recorded experimentally for different individuals during different feeding tasks are frequently substituted. This study uses finite element analysis (FEA) to examine the sensitivity of the mechanical response of a Macaca fascicularis cranium to varying muscle activation patterns predicted via multibody dynamic analysis. Relative to the effects of varying bite location, the consequences of simulated variations in muscle activation patterns and of the inclusion/exclusion of whole muscle groups were investigated. The resulting cranial deformations were compared using two approaches; strain maps and geometric morphometric analyses. The results indicate that, with bite force magnitude controlled, the variations among the mechanical responses of the cranium to bite location far outweigh those observed as a consequence of varying muscle activations. However, zygomatic deformation was an exception, with the activation levels of superficial masseter being most influential in this regard. The anterior portion of temporalis deforms the cranial vault, but the remaining muscles have less profound effects. This study for the first time systematically quantifies the sensitivity of an FEA model of a primate skull to widely varying masticatory muscle activations and finds that, with the exception of the zygomatic arch, reasonable variants of muscle loading for a second molar bite have considerably less effect on cranial deformation and the resulting strain map than does varying molar bite point. The implication is that FEA models of biting crania will generally produce acceptable estimates of deformation under load as long as muscle activations and forces are reasonably approximated. In any one FEA study, the biological significance of the error in applied muscle forces is best judged against the magnitude of the effect that is being investigated.

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.

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. Anat Rec, 298:107–121, 2015.

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.

The Mechanical Significance of the Temporal Fasciae in Macaca fascicularis: An Investigation Using Finite Element Analysis

Computational finite element analyses (FEAs) of the skull predict structural deformations under user specified loads and constraints, with results normally presented as stress and strain distributions over the skulls surface. The applied loads are generally a representation of the major adductor musculature, with the skull constrained at bite positions and at the articulating joints. However, virtually all analyses ignore potentially important anatomical structures, such as the fasciae that cover the temporalis muscle and attach onto the zygomatic arch. In vivo experimental studies have shown that removal of the temporal fasciae attachment onto the zygomatic arch in Cebus monkeys results in significant bone adaptation and remodeling in this region, suggesting the fasciae play an important role in stabilising the arch during biting. Here we investigate this potential stabilising role by carrying out FEAs of a macaque skull with and without temporal fasciae included. We explore the extent to which the zygomatic arch might be stabilized during biting by a synchronized tensioning of the temporal fasciae, acting to oppose masseteric contraction forces. According to our models, during temporalis muscle bulging the forces generated within the tensioned temporal fasciae are large enough to oppose the pull of the masseter. Further, a near bending‐free state of equilibrium within the arch can be reached, even under forceful biting. We show that it is possible to eliminate the high strain gradients in and around the zygomatic arch that are present in past computational studies, with strains being more uniform in magnitude than previously thought. Anat Rec, 2011.

Virtual Functional Morphology: Novel Approaches to the Study of Craniofacial Form and Function

Recent developments in simulating musculoskeletal functioning in the craniofacial complex using multibody dynamic analysis and finite elements analysis enable comprehensive virtual investigations into musculoskeletal form and function. Because the growth of the craniofacial skeleton is strongly influenced by mechanical functioning, these methods have potential in investigating the normal and abnormal development of the skull: loading history during development can be predicted and bony adaptations to these loads simulated. Thus these methods can be used to predict the impact of altered loading or modifications of skull form early in ontogeny on the subsequent development of structures. Combining functional models with geometric morphometric methods (GMM), which are principally concerned with the study of variations of form, offers the opportunity to examine variations in form during development and the covariations between form and factors such as functional performance. Such a combination of functional models and GMM can potentially be applied in many useful ways, for example: to build and modify functional models, to assess the outcomes of remodelling studies by comparing the results with morphological changes during ontogeny, and to compare the outcomes of finite element analyses within a multivariate framework. Studies using these tools can not only investigate the development of the skull but also the mechanical processes and thus to some degree, behaviours underlying the development of variation among extant and fossil skeletal elements. By bringing together these tools from quite different comparative traditions, a novel and potentially powerful framework for simulation and statistical biomechanical analyses of form and function emerges. This paper reviews these recent developments in the context of the evolutionary and functional influences on skull development.

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.

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.

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.