Abstract
During primate swallowing, tongue base retraction (TBR) drives the food bolus across the oropharynx towards the esophagus and flips the epiglottis over the laryngeal inlet, protecting against penetration and aspiration of food into the airway. Despite the importance of TBR for swallowing performance, the mechanics of TBR are poorly understood. Using biplanar videoradiography (XROMM) of four macaque monkeys, we tested the extrinsic muscle shortening hypothesis, which posits that shortening of the hyoglossus and styloglossus muscles pulls the tongue base posteriorly, and the muscular hydrostat or intrinsic tongue muscle hypothesis, which suggests that, because the tongue is composed of incompressible fluid, intrinsic muscle shortening increases tongue length and displaces the tongue base posteriorly. Our data falsify these hypotheses. Instead we 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. Our hydraulic mechanism is consistent with available data on human tongue swallowing kinematics. Rehabilitation for poor tongue base retraction might benefit from including suprahyoid muscle exercises during treatment.
Highlights
Conserved during tongue base retraction (TBR); i.e., the tongue functions as a muscular hydrostat
Our data refute the hypothesis that tongue base retraction during swallowing is due to shortening of hyoglossus, palatoglossus, and styloglossus muscles
A role for hydrostatic deformation in early tongue base retraction is refuted by our data showing that tongue base and posterior oral tongue volume increase as oral volume decreases, demonstrating that regional tongue deformation is more complicated than previously assumed by the muscular hydrostat hypothesis
Summary
Conserved during TBR; i.e., the tongue functions as a muscular hydrostat. This seems to not be the case in pig tongues, which exhibit regional changes in volume during feeding[21,22], raising doubts about the validity of the muscular hydrostat model. When the lower jaw is elevated the oral volume is floored by suprahyoid muscles–digastrics, mylohyoid, geniohyoid, hyoglossus, stylohyoid muscles—which, depending on their levels of activity, can variably stiffen and shorten, to modulate pressure in the oral volume These structures have been hypothesized to drive specialized aspects of tongue function in at least one species of mammal[23,24,25,26,27] but their influence on tongue deformation, tongue base retraction mechanics, is largely unstudied. This uncertainty led us to develop a third hypothesis—the hydraulic hypothesis—which posits that hyoid protraction and mouth floor elevation cause TBR via a hydraulic linkage between the tongue and suprahyoid muscles. This hypothesis is falsified if regional tongue base volume does not increase as the hyoid elevates and protracts, the mouth floor elevates, and the oral volume decreases
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