Characterizing tongue deformations during mastication using changes in planar components of three-dimensional angles.

Understanding of tongue deformations during mammalian mastication is limited, but has benefited from recent developments in multiplanar imaging technology. Here, we demonstrate how a standardized radiopaque marker implant configuration and biplanar fluoroscopy can quantify three-dimensional shape changes during chewing in pigs. Transverse and sagittal components of the three-dimensional angle between markers enable characterizing deformations in anatomically relevant directions. The transverse component illustrates bending to the left or to the right, which can occur symmetrically or asymmetrically, the latter sometimes indicating regional widening. The sagittal component reflects 'arching' or convex deformations in the dorsoventral dimension symmetrically or asymmetrically, the latter characteristic of twisting. Trends are detected in both the transverse and sagittal planes, and combinations thereof, to modify tongue shape in complex deformations. Both the transverse and sagittal components were also measured at key jaw and tongue positions, demonstrating variability particularly with respect to maximum and minimum gape. This highlights the fact that unlike tongue position, tongue deformations are more independent of jaw position, likely in response to the ever-changing bolus shape and position. From a methodological perspective, our study showcases advantages of a repeatable three-marker implant configuration suitable for animals of different sizes and highlights considerations for different implant patterns. This article is part of the theme issue 'Food processing and nutritional assimilation in animals'.

Regional Tongue Deformations During Chewing and Drinking in the Pig.

As a muscular hydrostat, the tongue undergoes complex deformations during most oral behaviors, including chewing and drinking. During thesebehaviors, deformations occur in concert with tongue and jaw movements to position and transport the bolus. Moreover, the various parts of the tongue may move and deform at similar timepoints relative to the gape cycle or they may occur at different timepoints, indicating regional biomechanical and functional variation. The goal of this study is to quantify tongue deformations during chewing and drinking in pigs by characterizing intrinsic changes in tongue dimensions (i.e., length and width) across multiple regions simultaneously. Tongue deformations are generally larger during chewing cycles compared to drinking cycles. Chewing and drinking also differ in the timing, relative to the gape cycle, of regional length and width, but not total length, deformations. This demonstrates functional differences in the temporal dynamics of localized shape changes, whereas the global properties of jaw-tongue coordination are maintained. Finally, differences in the trade-off between length and width deformations demonstrate that the properties of a muscular hydrostat are observed at the whole tongue level, but biomechanical variation (e.g., changes in movements and deformations) at the regional level exists. This study provides new critical insights into the regional contributions to tongue deformations as a basis for future work on multidimensional shape changes in soft tissues.

En tant qu'hydrostat musculaire, la langue subit des déformations complexes pendant la plupart des comportements oraux, en particulier au cours de la mastication et de l'ingestion de liquide. Au cours de ces comportements, les déformations se produisent de concert avec les mouvements de la langue et des mâchoires pour positionner et transporter le bolus. De plus, les différentes parties de la langue peuvent se déplacer et se déformer à des moments similaires ou différents par rapport au cycle d'ouverture de la bouche, indiquant une variation biomécanique et fonctionnelle régionale de la langue. L'objectif de cette étude est de quantifier les déformations de la langue pendant la mastication et l'ingestion d'eau chez le porc en caractérisant les changements intrinsèques des dimensions de la langue (i.e., longueur et largeur) des différentes régions de la langue simultanément. Les déformations de la langue sont généralement plus importantes pendant les cycles de mastication que pendant les cycles d'ingestion d'eau. La mastication et l'ingestion d'eau diffèrent également dans le timing (par rapport au cycle d'ouverture de la bouche) des déformations régionales de la langue en longueur et en largeur, mais pas en longueur totale. Cela démontre des différences fonctionnelles dans la dynamique temporelle des changements localisés de la forme de la langue alors que les propriétés globales de la coordination mâchoire-langue sont maintenues. Enfin, les différences dans le compromis mettant en jeu les déformations en longueur et en largeur démontrent que les propriétés d'un hydrostat musculaire sont observées au niveau de la langue entière, mais qu'il existe une variation biomécanique (par exemple, des changements dans les mouvements et les déformations) au niveau régional. Cette étude fournit de nouvelles informations essentielles sur les contributions régionales des déformations de la langue, qui serviront de base aux travaux futurs sur les changements multidimensionnels de forme dans les tissus mous.

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

Mastication and drinking are rhythmic and cyclic oral behaviors that require interactions between the tongue, jaw and a food or liquid bolus, respectively. During mastication, the tongue transports and positions the bolus for breakdown between the teeth. During drinking, the tongue aids in ingestion and then transports the bolus to the oropharynx. The objective of this study was to compare jaw and tongue kinematics during chewing and drinking in pigs. We hypothesized there would be differences in jaw gape cycle dynamics and tongue protraction-retraction between behaviors. Mastication cycles had an extended slow-close phase, reflecting tooth-food-tooth contact, whereas drinking cycles had an extended slow-open phase, corresponding to tongue protrusion into the liquid. Compared with chewing, drinking jaw movements were of lower magnitude for all degrees of freedom examined (jaw protraction, yaw and pitch), and were bilaterally symmetrical with virtually no yaw. The magnitude of tongue protraction-retraction (Txt), relative to a mandibular coordinate system, was greater during mastication than during drinking, but there were minimal differences in the timing of maximum and minimum Txt relative to the jaw gape cycle between behaviors. However, during drinking, the tongue tip is often located outside the oral cavity for the entire cycle, leading to differences between behaviors in the timing of anterior marker maximum Txt. This demonstrates that there is variation in tongue-jaw coordination between behaviors. These results show that jaw and tongue movements vary significantly between mastication and drinking, which hints at differences in the central control of these behaviors.

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

Mastication and drinking are rhythmic and cyclic oral behaviors that require interactions between the tongue, jaw and a food or liquid bolus, respectively. During mastication, the tongue transports and positions the bolus for breakdown between the teeth. During drinking, the tongue aids in ingestion and then transports the bolus to the oropharynx. The objective of this study was to compare jaw and tongue kinematics during chewing and drinking in pigs. We hypothesized there would be differences in jaw gape cycle dynamics and tongue protraction-retraction between behaviors. Mastication cycles had an extended slow-close phase, reflecting tooth-food-tooth contact, whereas drinking cycles had an extended slow-open phase, corresponding to tongue protrusion into the liquid. Compared with chewing, drinking jaw movements were of lower magnitude for all degrees of freedom examined (jaw protraction, yaw and pitch), and were bilaterally symmetrical with virtually no yaw. The magnitude of tongue protraction-retraction (Txt), relative to a mandibular coordinate system, was greater during mastication than during drinking, but there were minimal differences in the timing of maximum and minimum Txt relative to the jaw gape cycle between behaviors. However, during drinking, the tongue tip is often located outside the oral cavity for the entire cycle, leading to differences between behaviors in the timing of anterior marker maximum Txt. This demonstrates that there is variation in tongue-jaw coordination between behaviors. These results show that jaw and tongue movements vary significantly between mastication and drinking, which hints at differences in the central control of these behaviors.

Unilateral lingual nerve transection alters jaw-tongue coordination during mastication in pigs.

During chewing, movements and deformations of the tongue are coordinated with jaw movements to manage and manipulate the bolus and avoid injury. Individuals with injuries to the lingual nerve report both tongue injuries due to biting and difficulties in chewing, primarily because of impaired bolus management, suggesting that jaw-tongue coordination relies on intact lingual afferents. Here, we investigate how unilateral lingual nerve (LN) transection affects jaw-tongue coordination in an animal model (pig, Sus scrofa). Temporal coordination between jaw pitch (opening-closing) and 1) anteroposterior tongue position (i.e., protraction-retraction), 2) anteroposterior tongue length, and 3) mediolateral tongue width was compared between pre- and post-LN transection using cross-correlation analyses. Overall, following LN transection, the lag between jaw pitch and the majority of tongue kinematics decreased significantly, demonstrating that sensory loss from the tongue alters jaw-tongue coordination. In addition, decrease in jaw-tongue lag suggests that, following LN transection, tongue movements and deformations occur earlier in the gape cycle than when the lingual sensory afferents are intact. If the velocity of tongue movements and deformations remains constant, earlier occurrence can reflect less pronounced movements, possibly to avoid injuries. The results of this study demonstrate that lingual afferents participate in chewing by assisting with coordinating the timing of jaw and tongue movements. The observed changes may affect bolus management performance and/or may represent protective strategies because of altered somatosensory awareness of the tongue.NEW & NOTEWORTHY Chewing requires coordination between tongue and jaw movements. We compared the coordination of tongue movements and deformation relative to jaw opening-closing movements pre- and post-lingual nerve transection during chewing in pigs. These experiments reveal that the timing of jaw-tongue coordination is altered following unilateral disruption of sensory information from the tongue. Therefore, maintenance of jaw-tongue coordination requires bilateral sensory information from the tongue.

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

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.

The effect of unilateral lingual nerve injury on the kinematics of mastication in pigs.

OBJECTIVE: This study evaluates the effect of unilateral lingual sensory loss on the spatial and temporal dynamics of jaw movements during pig chewing. DESIGN: X-ray Reconstruction of Moving Morphology (XROMM) was used to reconstruct the 3-dimensional jaw movements of 6 pigs during chewing before and after complete unilateral lingual nerve transection. The effect of the transection were evaluated at the temporal and spatial level using Multiple Analysis of Variance. Temporal variables include gape cycle and phase durations, and the corresponding relative phase durations. Spatial variables include the amplitude of jaw opening, jaw yaw, and mandibular retraction-protraction. RESULTS: The temporal and spatial dynamics of jaw movements did not differ when chewing ipsilateral versus contralateral to the transection. When compared to pre-transection data, 4 of the 6 animals showed significant changes in temporal characteristics of the gape cycle following the transection, irrespective of chewing side, but the specific response to the lesion was highly dependent on the animal. On the other hand, in affected individuals the amplitude of jaw movements was altered similarly in all 3 dimensions: jaw opening and protraction-retraction increased whereas jaw yaw decreased. CONCLUSION: The variable impact of this injury in this animal model suggests that individuals use different compensatory strategies to adjust or maintain the temporal dynamics of the gape cycle. Because the amplitude of jaw movements are more adversely affected than their timing, results suggest that maintaining the tongue-jaw coordination is critical and this can come at the expense of bolus handling and masticatory performance.