Purpose Distinctive 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. Methods A 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. Results The 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. Conclusions Hyoid 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.

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Hyolingual kinematics are difficult to measure, but are central to hypotheses regarding musculoskeletal mechanisms and motor control. Recent application of biplanar videoradiography to the study of hyolingual kinematics in nonhuman primates provides new insight into tongue movements during chewing and swallowing, and into the role of hyoid movement in tongue base retraction and the oral phase of swallowing. During grape chewing, complex shape changes in the tongue were dominated by a combination of flexion in the tongue’s sagittal planes and roll about its long axis. As hypothesized for humans, in macaques during tongue retraction the molar region of the tongue rolls to the chewing side simultaneous with sagittal flexion, while the tongue tip flexes to the balancing side. Twisting and flexion reach their maxima early in the fast close phase of chewing cycles, positioning the food bolus between the approaching teeth prior to the power stroke. The muscular drivers of these movements are likely to include a combination of intrinsic and extrinsic tongue muscles. Nerve block of tactile sensation from trigeminal innervated oral structures decreased feeding performance, and the fast open phase of the gape cycle became significantly longer, relative to the other phases. The tongue made similar shapes in both the control and nerve block conditions, but the pattern of tongue‐jaw coordination became significantly more variable after the block. Disruption of oral somatosensation impacts feeding performance by introducing variability into the typically tight pattern of tongue‐jaw coordination. During primate swallowing, tongue base retraction (TBR) drives the food bolus across the oropharynx towards the esophagus but the mechanics of TBR are poorly understood. XROMM of four macaque monkeys falsifies both the hypothesis that extrinsic tongue muscle shortening pulls the tongue base posteriorly, and the muscular hydrostat hypothesis that intrinsic muscle shortening displaces the tongue base posteriorly by increasing tongue length. Our data suggest a novel hydraulic mechanism of TBR: shortening and rotation of suprahyoid muscles compresses the tongue between the hard palate, hyoid and mouth floor, squeezing the midline tongue base and food bolus back into the oropharynx. Hyoid elevation and protraction are powered by concentric activation and rotation of mylohyoid and digastric, followed by concentric activation of geniohyoid. This research suggests that structure, function, and coordination of mylohyoid and geniohyoid muscles are especially important determinants of swallowing performance in macaques, and probably humans.