Primate Swallowing Is Powered by Both Rotation and Contraction of Suprahyoid Muscles

Swallowing biomechanics in primates and other mammals is poorly understood, and the effect of hyoid descent on swallowing biomechanics lacks experimental interrogation. In macaques, which share similar swallowing kinematics with humans, the base of the tongue and the food bolus are hypothesized to be driven into the oropharynx by a hydraulic mechanism, at the core of which is elevation and protraction of the hyoid. Here, the musculoskeletal mechanisms driving these hyoid movements are experimentally evaluated in macaque primates.

We integrate XROMM-based measures of mandibular, cranial, and hyolingual kinematics with electromyography of suprahyoid and lingual muscles to evaluate the underlying kinetics of swallowing.

All suprahyoid muscles rotate during swallowing and tongue base retraction. Hyoid elevation and protraction are powered by concentric activation and rotation of posterior mylohyoid and both digastric muscle bellies, followed by concentric activation of geniohyoid muscle. Genioglossus is predominantly active early in swallowing.

Morphology, function, and coordination of suprahyoid and lingual muscles are especially important determinants of swallowing performance in macaques, and probably humans. Here, we characterize suprahyoid muscle biomechanics within a dynamic framework of architectural gear ratios and pulley systems that optimize hyoid elevation velocity to quickly "prime the pump" and subsequent hyoid protraction power and/or force to drive the hydraulic mechanism of tongue base retraction. Because of muscle rotation, primate hyolingual muscle function is particularly dependent on hyoid posture and muscle geometry, which may have important implications for the evolution of swallowing biomechanics in human evolution.