3D Hyolingual Kinematics Reveal New Insights Into the Biomechanical and Neural Control of Chewing and Swallowing in Macaque Primates

Abstract

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.