Biomechanical and Cortical Control of Tongue Movements During Chewing and Swallowing.

Tongue function is vital for chewing and swallowing and lingual dysfunction is often associated with dysphagia. Better treatment of dysphagia depends on a better understanding of hyolingual morphology, biomechanics, and neural control in humans and animal models. Recent research has revealed significant variation among animal models in morphology of the hyoid chain and suprahyoid muscles which may be associated with variation in swallowing mechanisms. The recent deployment of XROMM (X-ray Reconstruction of Moving Morphology) to quantify 3D hyolingual kinematics has revealed new details on flexion and roll of the tongue during chewing in animal models, movements similar to those used by humans. XROMM-based studies of swallowing in macaques have falsified traditional hypotheses of mechanisms of tongue base retraction during swallowing, and literature review suggests that other animal models may employ a diversity of mechanisms of tongue base retraction. There is variation among animal models in distribution of hyolingual proprioceptors but how that might be related to lingual mechanics is unknown. In macaque monkeys, tongue kinematics-shape and movement-are strongly encoded in neural activity in orofacial primary motor cortex, giving optimism for development of brain-machine interfaces for assisting recovery of lingual function after stroke. However, more research on hyolingual biomechanics and control is needed for technologies interfacing the nervous system with the hyolingual apparatus to become a reality.

Morphological disparity and evolutionary transformations in the primate hyoid apparatus.

The hyoid apparatus plays an integral role in swallowing, respiration, and vocalization in mammals. Most placental mammals have a rod-shaped basihyal connected to the basicranium via both soft tissues and a mobile bony chain-the anterior cornu-whereas anthropoid primates have broad, shield-like or even cup-shaped basihyals suspended from the basicranium by soft tissues only. How the unique anthropoid hyoid morphology evolved is unknown, and hyoid morphology of nonanthropoid primates is poorly documented. Here we use phylogenetic comparative methods and linear morphometrics to address knowledge gaps in hyoid evolution among primates and their euarchontan outgroups. We find that dermopterans have variable reduction of cornu elements. Cynocephalus volans are sexually dimorphic in hyoid morphology. Tupaia and all lemuroids except Daubentonia have a fully ossified anterior cornu connecting a rod-shaped basihyal to the basicranium; this is the ancestral mammalian pattern that is also characteristic of the last common ancestor of Primates. Haplorhines exhibit a reduced anterior cornu, and anthropoids underwent further increase in basihyal aspect ratio values and in relative basihyal volume. Convergent with haplorhines, lorisoid strepsirrhines independently evolved a broad basihyal and reduced anterior cornua. While a reduced anterior cornu is hypothesized to facilitate vocal tract lengthening and lower formant frequencies in some mammals, our results suggest vocalization adaptations alone are unlikely to drive the iterative reduction of anterior cornua within Primates. Our new data on euarchontan hyoid evolution provide an anatomical basis for further exploring the form-function relationships of the hyoid across different behaviors, including vocalization, chewing, and swallowing.

Comparative skeletal anatomy of neonatal ursids and the extreme altriciality of the giant panda.

Mammalian neonates are born at a wide range of maturity levels. Altricial newborns are born with limited sensory agency and require extensive parental care. In contrast, precocial neonates are relatively mature physically and often capable of independent function shortly after birth. In extant mammals, placental newborns vary from altricial to precocial, while marsupials and monotremes are all extremely altricial at birth. Bears (family Ursidae) have one of the lowest neonatal-maternal mass ratios in placental mammals, and are thought to also have the most altricial placental newborns. In particular, giant pandas (Ailuropoda melanoleuca) are thought to be exceptionally altricial at birth, and possibly marsupial-like. Here we used micro-computer (micro-computed) tomography scanning to visualize the skeletal anatomy of ursid neonates and compare their skeletal maturity with the neonates of other caniform outgroups. Specifically, we asked whether ursid neonates have exceptionally altricial skeletons at birth compared with other caniform neonates. We found that most bear neonates are similar to outgroup neonates in levels of skeletal ossification, with little variation in degree of ossification between ursine bears neonates (i.e. bears of the subfamily Ursinae). Perinatal giant pandas, however, have skeletal maturity levels most similar to a 42-45-day-old beagle fetus (~70% of total beagle gestation period). No bear exhibits the skeletal heterochronies seen in marsupial development. With regards to skeletal development, ursine bears are not exceptionally altricial relative to other caniform outgroups, but characterized largely by the drastic difference between newborn and adult body sizes. A review on the existing hypotheses for ursids' unique reproductive strategy suggests that the extremely small neonatal-maternal mass ratio of ursids may be related to the recent evolution of large adult body size, while life history characteristics retained an ancestral condition. A relatively short post-implantation gestation time may be the proximal mechanism behind the giant panda neonates' small size relative to maternal size and altricial skeletal development at birth.

Dental topographic change with macrowear and dietary inference in Homunculus patagonicus.

Homunculus patagonicus is a stem platyrrhine from the late Early Miocene, high-latitude Santa Cruz Formation, Argentina. Its distribution lies farther south than any extant platyrrhine species. Prior studies on the dietary specialization of Homunculus suggest either a mixed diet of fruit and leaves or a more predominantly fruit-eating diet. To gain further insight into the diet of Homunculus, we examined how the occlusal surfaces of the first and second lower molars of Homunculus change with wear by using three homology-free dental topographic measures: Dirichlet normal energy (DNE), orientation patch count rotated (OPCR), and relief index (RFI). We compared these data with wear series of three extant platyrrhine taxa: the folivorous Alouatta, and the frugivorous Ateles and Callicebus (titi monkeys now in the genus Plecturocebus). Previous studies found Alouatta and Ateles exhibit distinctive patterns of change in occlusal morphology with macrowear, possibly related to the more folivorous diet of the former. Based on previous suggestions that Homunculus was at least partially folivorous, we predicted that changes in dental topographic metrics with wear would follow a pattern more similar to that seen in Alouatta than in Ateles or Callicebus. However, wear-induced changes in Homunculus crown sharpness (DNE) and complexity (OPCR) are more similar to the pattern observed in the frugivorous Ateles and Callicebus. Based on similar wear modalities of the lower molars between Homunculus and Callicebus, we infer that Homunculus had a primarily frugivorous diet. Leaves may have provided an alternative dietary resource to accommodate fluctuation in seasonal fruiting abundance in the high-latitude extratropical environment of late Early Miocene Patagonia.

Head posture impacts mammalian hyoid position and suprahyoid muscle length: implication for swallowing biomechanics.

Instantaneous head posture (IHP) can extensively alter resting hyoid position in humans, yet postural effects on resting hyoid position remain poorly documented among mammals in general. Clarifying this relationship is essential for evaluating interspecific variation in hyoid posture across evolution, and understanding its implications for hyolingual soft tissue function and swallowing motor control. Using Didelphis virginiana as a model, we conducted static manipulation experiments to show that head flexion shifts hyoid position rostrally relative to the cranium across different gapes. IHP-induced shifts in hyoid position along the anteroposterior axis are comparable to in vivo hyoid protraction distance during swallowing. IHP also has opposite effects on passive genio- and stylohyoid muscle lengths. High-speed biplanar videoradiography suggests Didelphis consistently swallows at neutral to flexed posture, with stereotyped hyoid kinematics across different head postures. IHP change can affect suprahyoid muscle force production by shifting their positions on the length-tension curve, and redirecting lines of action and the resultant force from supra- and infrahyoid muscles. We hypothesize that demands on muscle performance may constrain the range of swallowing head postures in mammals. This article is part of the theme issue 'Food processing and nutritional assimilation in animals'.

Three-dimensional mandibular kinematics of mastication in the marsupial Didelphis virginiana.

Didelphis virginiana (the Virginia opossum) is often used as an extant model for understanding feeding behaviour in Mesozoic mammaliaforms, primarily due to their morphological similarities, including an unfused mandibular symphysis and tribosphenic molars. However, the three-dimensional jaw kinematics of opossum chewing have not yet been fully quantified. We used biplanar videofluoroscopy and the X-Ray Reconstruction of Moving Morphology workflow to quantify mandibular kinematics in four wild-caught opossums feeding on hard (almonds) and soft (cheese cubes) foods. These data were used to test hypotheses regarding the importance of roll versus yaw in chewing by early mammals, and the impact of food material properties (FMPs) on jaw kinematics. The magnitude of roll exceeds that of yaw, but both are necessary for tooth-tooth or tooth-food-tooth contact between complex occlusal surfaces. We confirmed the utility of the four vertical kinematic gape cycle phases identified in tetrapods but we further defined two more in order to capture non-vertical kinematics. Statistical tests support the separation of chew cycle phases into two functional groups: occlusal and non-occlusal phases. The separation of slow close into two (occlusal) phases gives quantitative kinematic support for the long-hypothesized multifunctionality of the tribosphenic molar. This article is part of the theme issue 'Food processing and nutritional assimilation in animals'.

Digest: Microhabitat use and developmental timing shape anuran limb evolution.

Do frog limb shapes reflect microhabitat use against the backdrop of shared ancestry, body size variation, and developmental constraints? Stepanova and Womack found that when phylogeny and body size are controlled, microhabitat use is a key factor in explaining anuran limb evolution. The shape of distal limb elements in anuran limbs also evolves at a higher rate than proximal elements, suggesting that a relaxation of developmental constraints in distal elements may be shared across tetrapod limb development.