XROMM analysis of tooth occlusion and temporomandibular joint kinematics during feeding in juvenile miniature pigs.

Like humans, domestic pigs are omnivorous and thus are a common model for human masticatory function. Prior attempts to characterize food-tooth interactions and jaw movements associated with mastication have been limited to aspects of the oral apparatus that are visible externally (with videography) and/or to 2D movements of oral structures (with monoplanar videofluoroscopy). We used XROMM, a 3D technique that combines CT-based morphology with biplanar videofluoroscopy, to quantify mandibular kinematics, tooth occlusion and mandibular condylar displacements within the temporomandibular joint (TMJ) during feeding. We observed that the pig TMJ moved detectably in only three of six possible degrees of freedom during mastication: two rotations, pitch and yaw; and one translation, protraction-retraction. Asymmetrical yaw around a dorsoventral axis produced the observed alternating left-right chewing cycles responsible for food reduction. Furthermore, the relative motions of the upper and lower premolars contained a substantial mesiodistal component in addition to the buccolingual component, resulting in an oblique (rather than a strictly transverse) power stroke. This research demonstrates the capacity of XROMM to explore the kinematic underpinnings of key masticatory movements, such as the occlusal power stroke, by integrating tooth, joint and rigid body jaw movements. XROMM also allowed us to test kinematic hypotheses based on skeletal anatomy with actual kinematics observed during naturalistic feeding behaviors. We observed that the soft tissue structures of the TMJ appear to play a significant role in limiting the range of motion of a joint, and thus analyses based solely on osseous morphology may over-estimate joint mobility.

In vivo bone strain and finite element modeling of the mandible of Alligator mississippiensis.

Forces experienced during feeding are thought to strongly influence the morphology of the vertebrate mandible; in vivo strain data are the most direct evidence for deformation of the mandible induced by these loading regimes. Although many studies have documented bone strains in the mammalian mandible, no information is available on strain magnitudes, orientations or patterns in the sauropsid lower jaw during feeding. Furthermore, strain gage experiments record the mechanical response of bone at a few locations, not across the entire mandible. In this paper, we present bone strain data recorded at various sites on the lower jaw of Alligator mississippiensis during in vivo feeding experiments. These data are used to understand how changes in loading regime associated with changes in bite location are related to changes in strain regime on the working and balancing sides of the mandible. Our results suggest that the working side mandible is bent dorsoventrally and twisted about its long-axis during biting, and the balancing side experiences primarily dorsoventral bending. Strain orientations are more variable on the working side than on the balancing side with changes in bite point and between experiments; the balancing side exhibits higher strain magnitudes. In the second part of this paper, we use principal strain orientations and magnitudes recorded in vivo to evaluate a finite element model of the alligator mandible. Our comparison demonstrates that strain orientations and mandibular deformation predicted by the model closely match in vivo results; however, absolute strain magnitudes are lower in the finite element model.

Kinematics of the quadrate bone during feeding in mallard ducks.

Avian cranial kinesis, in which mobility of the quadrate, pterygoid and palatine bones contribute to upper bill elevation, is believed to occur in all extant birds. The most widely accepted model for upper bill elevation is that the quadrate rotates rostrally and medially towards the pterygoid, transferring force to the mobile pterygoid-palatine complex, which pushes on the upper bill. Until now, however, it has not been possible to test this hypothesis in vivo because quadrate motions are rapid, three-dimensionally complex and not visible externally. Here we use a new in vivo X-ray motion analysis technique, X-ray reconstruction of moving morphology (XROMM), to create precise (±0.06 mm) 3-D animations of the quadrate, braincase, upper bill and mandible of three mallard ducks, Anas platyrhynchos. We defined a joint coordinate system (JCS) for the quadrato-squamosal joint with the axes aligned to the anatomical planes of the skull. In this coordinate system, the quadrate's 3-D rotations produce an elliptical path of pterygoid process motion, with medial and rostrodorsal then lateral and rostrodorsal motion as the upper bill elevates. As the upper bill depresses, the pterygoid process continues along the ellipsoidal path, with lateral and caudoventral then medial and caudoventral motion. We also found that the mandibular rami bow outwards (streptognathy) during mandibular depression, which may cause the lateral component of quadrate rotation that we observed. Relative to the JCS aligned with the anatomical planes of the skull, a second JCS aligned with quadrato-squamosal joint anatomy did not produce a simpler description of quadrate kinematics.

X-ray reconstruction of moving morphology (XROMM): precision, accuracy and applications in comparative biomechanics research.

X-Ray Reconstruction of Moving Morphology (XROMM) comprises a set of 3D X-ray motion analysis techniques that merge motion data from in vivo X-ray videos with skeletal morphology data from bone scans into precise and accurate animations of 3D bones moving in 3D space. XROMM methods include: (1) manual alignment (registration) of bone models to video sequences, i.e., Scientific Rotoscoping; (2) computer vision-based autoregistration of bone models to biplanar X-ray videos; and (3) marker-based registration of bone models to biplanar X-ray videos. Here, we describe a novel set of X-ray hardware, software, and workflows for marker-based XROMM. Refurbished C-arm fluoroscopes retrofitted with high-speed video cameras offer a relatively inexpensive X-ray hardware solution for comparative biomechanics research. Precision for our biplanar C-arm hardware and analysis software, measured as the standard deviation of pairwise distances between 1 mm tantalum markers embedded in rigid objects, was found to be +/-0.046 mm under optimal conditions and +/-0.084 mm under actual in vivo recording conditions. Mean error in measurement of a known distance between two beads was within the 0.01 mm fabrication tolerance of the test object, and mean absolute error was 0.037 mm. Animating 3D bone models from sets of marker positions (XROMM animation) makes it possible to study skeletal kinematics in the context of detailed bone morphology. The biplanar fluoroscopy hardware and computational methods described here should make XROMM an accessible and useful addition to the available technologies for studying the form, function, and evolution of vertebrate animals.

Quantitative analysis of the effect of prey properties on feeding kinematics in two species of lizards.

Studies of the functional morphology of feeding have typically not included an analysis of the potential for the kinematics of the gape cycle to vary based on the material properties of the prey item being consumed. Variation in prey properties is expected not only to reveal variation in feeding function, but allows testing of the functional role of the phases of the gape cycle. The jaw kinematics of two species of lizards are analyzed when feeding trials are conducted using quantitative control of prey mass, hardness and mobility. For both species, there were statistically significant prey effects on feeding kinematics for all the prey properties evaluated (i.e. prey mass, hardness and mobility). Of these three prey properties, prey mass had a more significant effect on feeding kinematics than prey hardness or mobility. Revealing the impact of varying prey properties on feeding kinematics helps to establish the baseline level of functional variability in the feeding system. Additionally, these data confirm the previously hypothesized functional role of the slow open (SO) phase of the gape cycle as allowing for physical conformation of the tongue to the surface of the food bolus in preparation for further intraoral transport.

Inertial feeding in the teiid lizard Tupinambis merianae: the effect of prey size on the movements of hyolingual apparatus and the cranio-cervical system.

In most terrestrial tetrapods, the transport of prey through the oral cavity is accomplished by movements of the hyolingual apparatus. Morphological specializations of the tongue in some lizard taxa are thought to be associated with the evolution of vomerolfaction as the main prey detection mode. Moreover, specializations of the tongue are hypothesized to compromise the efficiency of the tongue during transport; thus, driving the evolution of inertial transport. Here we use a large teiid lizard, Tupinambis merianae, as a model system to test the mechanical link between prey size and the use of inertial feeding. We hypothesize that an increase in prey size will lead to the increased recruitment of the cranio-cervical system for prey transport and a reduced involvement of the tongue and the hyolingual apparatus. Discriminant analyses of the kinematics of the cranio-cervical, jaw and hyolingual systems show that the transport of large prey is indeed associated with a greater utilization of the cranio-cervical system (i.e. neck and head positioning). The tongue retains a kinematic pattern characteristic of lingual transport in other lizards but only when processing small prey. Our data provide evidence for an integration of the hyolingual and cranio-cervical systems; thus, providing partial support for an evolutionary scenario whereby the specialization of the tongue for chemoreception has resulted in the evolution of inertial transport strategies.

The evolution of cranial design and performance in squamates: Consequences of skull-bone reduction on feeding behavior.

The evolution of cranial design in lepidosaurians is characterized by a general trend toward the loss of cranial elements. The evolution of relatively lighter skulls in squamates appears tightly coupled to a reduction in relative mass of the jaw adductor, implying functional consequences for bite force and feeding behavior. Interestingly, among squamates the postorbital bar was reduced or lost at least twice independently and taxa characterized by the loss of these cranial elements (e.g., geckos and varanids) are generally reported as having a mobile skull. In Gekkotans, the loss of the postorbital bar was accompanied by a reduction of the supratemporal bar, resulting in a pronounced cranial kinesis. Our data show that having a kinetic skull has functional consequences and results in a reduction in bite force. The lower bite force may in turn be responsible for the decreased feeding efficiency as reflected in the longer duration of intra-oral transport cycles. Gekkotans, however, appear to exploit their intracranial mobility in ways that increases the velocity of jaw movement during opening and closing, which may allow them to capture more elusive prey. The morphological changes observed in the evolution of the cranial system in squamates appear tightly linked to functional and constructional demands on the skull, making squamate skull evolution a model system to investigate the consequences of morphological changes in a complex integrated system of performance, behavior, and ecology.

Modulation of intra-oral processing in mammals and lepidosaurs.

The mammalian masticatory apparatus is distinguished from the intra-oral processing systems of other amniotes by a number of morphological and functional features, including transverse movements of the teeth during the power stroke, precise occlusion, suspension of the teeth in the socket by a periodontal ligament, diphyodonty (reduction to two generations of teeth), a hard palate, and the presence of a single bone (the dentary) in the lower jaw which articulates with the skull at the temporomandibular jaw joint. The evolution of these features is commonly argued to have improved the efficiency of food processing in the oral cavity. The present aricle highlights the existence in mammals of the fusimotor system and afferent fibers from the periodontal ligament through which the CNS modulates the responses by the muscle spindles. Published data suggest that the fusimotor system and the periodontal afferents are important components in feed-forward (or anticipatory) control of chewing behavior. We hypothesize that this feed-forward control is used to maintain relatively constant cycle lengths in mammals in the face of intra-sequence and inter-sequence variation in material properties of the food, and that this enables them to maintain a higher average chewing frequency than that of lizards. These predictions were evaluated using data on mean cycle length and its variance from the literature and from our own files. On average, mammals have less variable cycle lengths than do lizards and shorter cycle lengths than do lizards of similar size. We hypothesize that by decreasing variance in cycle length, presumably close to the natural frequency of their feeding systems, mammals minimize energy expenditure during chewing, allowing them to chew for longer, thereby maintaining the high rates of food intake required for their high metabolic rates.

Comparison of beam theory and finite-element analysis with in vivo bone strain data from the alligator cranium.

The mechanical behavior of the vertebrate skull is often modeled using free-body analysis of simple geometric structures and, more recently, finite-element (FE) analysis. In this study, we compare experimentally collected in vivo bone strain orientations and magnitudes from the cranium of the American alligator with those extrapolated from a beam model and extracted from an FE model. The strain magnitudes predicted from beam and FE skull models bear little similarity to relative and absolute strain magnitudes recorded during in vivo biting experiments. However, quantitative differences between principal strain orientations extracted from the FE skull model and recorded during the in vivo experiments were smaller, and both generally matched expectations from the beam model. The differences in strain magnitude between the data sets may be attributable to the level of resolution of the models, the material properties used in the FE model, and the loading conditions (i.e., external forces and constraints). This study indicates that FE models and modeling of skulls as simple engineering structures may give a preliminary idea of how these structures are loaded, but whenever possible, modeling results should be verified with either in vitro or preferably in vivo testing, especially if precise knowledge of strain magnitudes is desired.

Bone strain gradients and optimization in vertebrate skulls.

It is often stated that the skull is optimally designed for resisting feeding forces, where optimality is defined as maximum strength with minimum material. Running counter to this hypothesis are bone strain gradients--variation in bone strain magnitudes across the skull--which in the primate skull have been hypothesized to suggest that different parts of the skull are optimized for different functions. In this paper strain gradients in the skulls of four genera of primates, Sus, and Alligator were documented and compared. Strain gradients were pervasive in all taxa sampled. Patterns of strain gradients showed inter-taxon differences, but strains in the mandible and zygomatic arch were always higher than those in the circumorbital and neurocranial regions. Strain magnitudes in Alligator were twice as high as those in mammals. Strain gradients were also positively allometric; i. e., larger primates show steeper gradients (larger differences) between the mandible and circumorbital region than smaller primates. Different strain magnitudes in different areas of the same animal are hypothesized to reflect optimization to different criteria. It is therefore hardly surprising that the skull, in which numerous functional systems are found, exhibits very steep gradients. Inter-specific differences in strain magnitudes at similar sites also suggest inter-specific differences in optimality criteria. The higher strain magnitudes in the Alligator skull suggest that the Alligator skull may be designed to experience extremely high strains less frequently whereas the primate skull may be designed to resist lower strains more frequently.