Effects of food properties on chewing in pigs: Flexibility and stereotypy of jaw movements in a mammalian omnivore

Abstract

Chewing is a rhythmic oral behavior that requires constant modifications of jaw movements in response to changes in food properties. The food-specific kinematic response is dependent on the potential for kinematic flexibility allowed by morphology and modulation of motor control. This study investigates the effects of food toughness and stiffness on the amplitude and variability of jaw movements during chewing in a typical omnivorous mammalian model (pigs). Jaw movements were reconstructed using X-ray Reconstruction Of Moving Morphology (XROMM) and kinematic data associated with the amplitude of jaw pitch (opening-closing) and jaw yaw (mediolateral rotation) were extracted for each cycle. Between-food differences were tested for the amplitude of jaw movements during each phase of the gape cycle, as well as in their respective within-food variability, or stereotypy, as indicated by coefficients of variation. With increasing toughness, jaw pitch amplitude is decreased during fast close, larger and more stereotyped during slow close, smaller but more variable during slow open, and more variable during fast open. In addition, when chewing on tougher foods, the amplitude of jaw yaw during slow close only increases in a subset of individuals, but all become less variable (i.e., more stereotyped). In contrast, increasing food stiffness has no effect on the amplitude or the variability of jaw pitch, whereas jaw yaw increases significantly in the majority of individuals studied. Our data demonstrate that food stiffness and toughness both play a role in modulating gape cycle dynamics by altering the trajectory of jaw movements, especially during the slow-close phase and tooth-food-tooth contact, albeit differently. This highlights how a generalist oral morphology such as that of pigs (e.g., bunodont teeth lacking precise occlusion, permissive temporomandibular joint allowing extensive condylar displacements in 3 dimensions) enables organisms to not only adjust chewing movements in their amplitude, but also in their variability.

Jaw Kinematics and Tongue Protraction-Retraction during Chewing and Drinking in the Pig

“…Finally, previous work on pigs also shows that of the three available translational DoF, jaw movements during chewing only use anteroposterior (Tx) translations (Brainerd et al, 2010;Menegaz et al, 2015;Montuelle et al, 2018;2019;2020a). We show here that this is also the case for drinking.…”

“…Variability was indeed higher for chewing than drinking cycles for both absolute and relative duration of the first opening phase, and the opposite was observed for the second opening phase. As occlusion extends into the first opening phase (Montuelle et al, 2020a), this higher variability during chewing may be attributed to the changing bolus properties.…”

“…First, we will determine whether mastication and drinking use the same degrees of freedom during their respective gape cycles. Previous studies have demonstrated that two rotations, jaw pitch and jaw yaw, and anteroposterior translation (i.e., jaw protraction-retraction) are used during chewing gape cycles (Montuelle et al, 2020a;Menegaz et al, 2015). Whereas jaw pitch reflects jaw opening and closing, jaw yaw reflects rotation about a vertical axis contributing to the characteristic "sidedness" of 6 unilateral chewing to facilitate tooth occlusion (see Grossnickle, 2017 and references therein).…”

Jaw kinematics and tongue protraction–retraction during chewing and drinking in the pig

“…Finally, previous work on pigs also shows that of the three available translational DoF, jaw movements during chewing cycles only use anteroposterior (Tx) translations (Brainerd et al, 2010;Menegaz et al, 2015;Montuelle et al, 2018Montuelle et al, , 2019Montuelle et al, , 2020a. We show here that this is also the case for drinking cycles.…”

“…First, we will determine whether both behaviors use the same degrees of freedom during their respective gape cycles. Previous studies have demonstrated that two rotations, jaw pitch and jaw yaw, and anteroposterior translation (i.e., jaw protraction-retraction) are used during mastication (Brainerd et al, 2010;Menegaz et al, 2015;Montuelle et al, 2020a). Whereas jaw pitch reflects jaw opening and closing, jaw yaw reflects rotation about a vertical axis contributing to the characteristic "sidedness" of mastication.…”