Feedback control from the jaw joints during biting: An investigation of the reptile Sphenodon using multibody modelling
Introduction
The New Zealand Tuatara, Sphenodon, is a lizard-like reptile that is the sole living representative of a group (Rhynchocephalia) that was widespread at the time of the dinosaurs (Jones, 2008). Its feeding apparatus is unusual in combining a jaw joint that allows a pro-oral shearing with a tooth arrangement in which the lower teeth bite into a gap between parallel rows of teeth on the upper jaw and palate (Gorniak et al., 1982). These teeth are also fused to crest of the jaw bone (acrodonty) so that the boundary between tooth and bone is unclear (Kieser et al., 2009). By contrast, the teeth of mammals and crocodiles are held in sockets by a flexible periodontal ligament (McIntosh et al., 2002, Ross et al., 2007). This ligament is considered to have a protective function during biting because it contains mechanoreceptors whose feedback modulates muscle activity and prevents excessive forces being applied to the teeth (e.g. Dong et al., 1993). When the ligament is absent, as it is in Sphenodon and modern lizards (e.g. Kieser et al., 2009, Luan et al., 2009), feedback from other receptors must serve to limit joint and tooth damage. This may be particularly important when, as in Sphenodon (Robinson, 1976), teeth are not replaced. In mammals, there are additional receptors in the teeth (pulp cavities, dentine tubules), jaw muscles, and jaw joints (capsule, associated ligaments) (Dong et al., 1993, Matthews et al., 1976, Paphangkorakit and Osborn, 1989, Zimny, 1988), and at least some of these are known to occur in non-mammalian tetrapods (Crowe, 1992).
Receptors in and around the jaw joints may function ensuring that pressure within the jaw joints, and stresses in the joint capsule and associated ligaments remain below potentially damaging thresholds by modulating muscle activity accordingly. Experimental evidence is lacking because direct measurement of joint forces in vivo would involve invasive procedures to fix sensing equipment within the joint capsule. This difficulty is compounded when dealing with small joints such as those in Sphenodon. Even if direct measurements were possible, there is the potential for altered jaw function due to obstructed movement and pain within the joint. An alternative approach is to use virtual simulations, with computational studies that involve constructing geometrically accurate three-dimensional models from X-ray scan images becoming increasingly popular (e.g. Curtis et al., 2008, Moazen et al., 2008, Rayfield, 2007, Strait et al., 2007).
Here we adopt this alternative approach, using a three-dimensional multibody computer model of the skull and neck of Sphenodon to investigate the relationships between muscle, joint, and bite forces. Unilateral biting simulations were performed with both deformable and non-deformable food items at varying positions within the mouth to assess the effect of maximum bite and muscle forces on joint forces, and to assess the effect of varying bite point on joint feedback control capabilities.
Section snippets
Methods
Micro-computed tomography (micro-CT) data of the head of an adult Sphenodon (LDUCZ×036, Grant Museum of Zoology, UCL; cranial length=67.7 mm) were used to generate three-dimensional, rigid body computer models of the cranium, lower jaws, and neck. These models were imported into ADAMS multibody modelling software (MSC Software Corp., USA) in preparation for a multibody analysis. All soft tissue structures, constraints, contacts, and mass/inertial properties were assigned to the model as
Results
Fig. 3 shows the results for the incompressible food simulation. Here two linked plots are shown; the upper plot presents joint forces and bite force throughout the biting simulation, while the lower plot presents the activation levels of the working and balancing side muscle groups. As would be expected, increased activity in the balancing side muscle groups increases balancing side joint forces and bite force. Working side joint forces fall with increasing balancing side muscle activity,
Discussion
This study used a complex, three-dimensional multibody computer model to investigate the effect of simulating feedback between jaw joint forces and muscle activation during biting, the target being equal working and balancing side joint forces. As with all modelling studies of this type there are inevitably approximations and simplifications. Muscles are complex structures, often possessing high levels of pennation and compartmentalisation. They are not simply straight line force actuators as
Conflict of interest statement
The authors confirm that there is no conflict of interest in the manuscript.
Acknowledgements
We would like to acknowledge the Biotechnology and Biological Sciences Research Council (BBSRC) who provided the funding for this research (Grants: BB/E007465/1, BB/E009204/1 and BB/E007813/1).
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