Human Hyoid Descent is Adaptive rather than Maladaptive for Swallowing Performance: An Experimental and Computational Argument

Abstract

PurposeDistinctive features of the human supralaryngeal vocal tract have been argued to be adaptive for speech and maladaptive for swallowing. However, this maladaptive hypothesis has not been thoroughly tested and in fact is refuted by studies of normal human feeding physiology. This study validates a computational model of hyolingual biomechanics derived from an previously validated experimental nonhuman primate model system and examines how changes in hyolingual and craniofacial morphology over the course of human evolution and ontogeny affect hyolingual biomechanics during swallowing. In particular, we examine superoanterior excursion of the hyoid, which is often reduced in human patients with dysphagia and therefore used here as a surrogate for swallowing performance.MethodsA computational model of hyolingual range of motion during swallowing in Macaca mulatta was developed in R using in vivo data. Model outputs were compared against in vivo macaque data to determine the model's goodness of fit using a receiver operating characteristics (ROC) curve; model predictive power was estimated using the area under the ROC curve. Several aspects of macaque craniofacial and hyoid morphology were then altered towards the human condition with consequent adjustments made to muscle lengths, and the model calculated hyoid displacement during swallowing for each condition. A model was considered viable if its range of motion included a target of hyoid excursion derived from in vivo macaque and human data.ResultsThe macaque model had a sensitivity of 0.79, specificity of 0.82, and accuracy of 88% compared to in vivo data. A humanoid model predicts hyoid excursion within normal limits of healthy humans. Altering macaque morphology to approach the human condition by lowering the hyoid and making the symphysis vertical had little effect on model performance. Isolated shortening of the mandible significantly decreased hyoid excursion unless the symphysis was also made more vertical. Moreover, as the model was made more humanoid, both hyoid descent and physiologically maximal muscle shortening were necessary to approximate target hyoid excursion.ConclusionsHyoid descent—which is commonly assumed to be detrimental to swallowing—may actually maintain swallowing performance as the human face has shortened in recent evolutionary history. 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. Geometric constraints require human suprahyoid muscles to perform at their physiological limits when the hyoid is descended. Such extreme performance requirements may leave humans vulnerable to dysphagia not because of airway morphology alone but because of physiologic constraints.