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Abstract

Swallowing is essential to vertebrate life, yet its biomechanical basis is poorly understood compared to other behaviors such as chewing, suction feeding, reaching, and locomotion. Human swallowing biomechanics is of clinical interest for treating dysphagia, or difficulty swallowing, with neuromuscular rehabilitation. Swallowing is also of anthropological interest because purported adaptations for speech also allow food and air to mingle near an open larynx, which some argue renders humans maladapted to swallowing. However, this hypothesis has not been thoroughly tested and in fact is refuted by several studies of human feeding physiology. This dissertation uses a macaque (Macaca mulatta) model system to determine the biomechanical basis of two important movements involved in bolus propulsion and airway protection—tongue base retraction and hyoid superoanterior excursion—and examines how changes in hyolingual and craniofacial morphology over the course of human evolution and ontogeny affect hyolingual biomechanics. Tongue base retraction was caused by neither extrinsic lingual muscle shortening nor hydrostatic deformation. Kinematic evidence suggests that suprahyoid muscles cause tongue base retraction by regionally changing tongue volume, which is consistent with a hydraulic linkage between the suprahyoid muscles and the tongue. These suprahyoid muscles are not only active and shortening during tongue base retraction, but they also rotate as they move the hyoid. This rotation either amplifies or reduces hyoid velocity depending on the geometry of the muscle and the direction of rotation. In this way, suprahyoid muscles are functionally analogous to pennate muscles, which also exhibit fiber rotation and gearing. A computational model of hyoid range of motion demonstrates that hyoid descent—which is commonly assumed to be detrimental to swallowing—may actually help to maintain swallowing performance as the human face has shortened in recent evolutionary history, especially if tongue volume must be preserved to maintain a hydraulic linkage between the tongue and hyoid. Moreover, because mandibular morphology affects suprahyoid muscle length, selective pressure to maintain swallowing performance may have resulted in the emergence of humanity’s characteristic vertical mandibular symphysis and then chin. However, geometric constraints require human suprahyoid muscles to shorten relatively more when the hyoid is descended, which may leave humans vulnerable to dysphagia not because the human airway allows for more mixing of food and air near the larynx but rather because of fundamental constraints on vertebrate skeletal muscle biomechanics. Given that muscles from the cranium, mandible, pharynx, soft palate, larynx, sternum, and scapula all converge on this nexus of the neck, the mammalian hyolingual apparatus may have an underappreciated role in shaping the structures from which it is so elegantly suspended.

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