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

Abstract

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’.

Introduction: food processing and nutritional assimilation in animals

“…Similar interactions can be hypothesized for animals that alter their dietary niche, e.g. through seasonal exploitation of fallback foods, in animals that drastically alter their posture during feeding, such as for instance behavioural changes including hanging upside-down during mastication, as seen in bats [ 77 ], due to postural changes across evolution, as explored by Li et al [ 67 ], or due to ontogenetic changes such as for instance chewing and swallowing before and after laryngeal descent, as encountered by most mammals, and to a particularly dramatic extent by ungulate males [ 78 ]. Associated implications for optimal performance could include changes in the pattern of activation of muscles driving the feeding system, novel interactions between contracting muscles and elastic action of the tendons that connect them to the bones they move, or a combination thereof.…”

“…[65,66]), but assessments of performance often extend beyond these measures. For example, Li et al [67] define swallowing performance as the safe and efficient bolus transport from the oral cavity to the oesophagus, whereas Clauss et al [68] explore the relationships between chewing and digestive efficiency through a washing mechanism. Beale et al [36] and Raubenheimer et al [69] both assess performance through nutritional and secondary compound intake.…”

“…For example, Li et al . [ 67 ] define swallowing performance as the safe and efficient bolus transport from the oral cavity to the oesophagus, whereas Clauss et al . [ 68 ] explore the relationships between chewing and digestive efficiency through a washing mechanism .…”