Publications

The human tongue is a structurally complex and extremely flexible organ. In order to better understand the mechanical basis for lingual deformations, we modeled a primitive movement of the tongue, sagittal tongue bending. We hypothesized that sagittal bending is a synergistic deformation derived from co-contraction of the longitudinalis and transversus muscles. Our model of tongue bending was based on classical bimetal strip theory, in which curvature is produced when one muscle layer contracts more so than another. Contraction was modulated via mismatched thermal expansion coefficients and temperature change (to simulate muscular contraction). Our results demonstrated that synergistic contraction produced curvature and strain results which were in better correspondence to empirical results derived from tagging MRI than were the results of contraction of the longitudinalis muscle alone. This fundamental reliance of tongue bending on the synergistic contraction of its intrinsic fibers supports the muscular hydrostat theory of tongue function.

The myoarchitecture of the tongue is comprised of a complex array of muscle fiber bundles, which form the structural basis for lingual deformations during speech and swallowing. We used magnetic resonance imaging of the water diffusion tensor to display the primary and secondary fiber architectural attributes of the excised bovine tongue. Fiber orientation mapping provides a subdivision of the tongue into its principal intrinsic and extrinsic muscular components. The anterior tongue consists of a central region of orthogonally oriented intrinsic fibers surrounded by an axially oriented muscular sheath. The posterior tongue consists principally of a central region of extrinsic fibers, originating at the inferior surface and projecting in a fan-like manner in the superior, lateral, and posterior directions, and lateral populations of extrinsic fibers directed posterior-inferior and posterior-superior. Analysis of cross-fiber anisotropy indicates a basic contrast of design between the extrinsic and the intrinsic fibers. Whereas the extrinsic muscles exhibit a uniaxial architecture typical of skeletal muscle, the intrinsic core muscles, comprised of the verticalis and the transversus muscles, show strong cross-fiber anisotropy. This pattern is consistent with the theory that the tongue's core functions as a muscular hydrostat in that conjoint contraction of the transverse and vertical fibers enable the tissue to expand at right angles to these fibers. These findings suggest that three-dimensional analysis of diffusion tensor magnetic resonance imaging provides a structural basis for understanding the micromechanics of the mammalian tongue.

In clinical practice, the assessment of lung mechanics is limited to a global physiological evaluation, which measures, in the aggregate, the contributions of the pulmonary parenchyma, pleura, and chest wall. In this study, we used an MR imaging methodology which applies two-dimensional bands of inverted magnetization directly onto the pulmonary parenchyma, thus allowing for the quantification of local pulmonary tissue deformation, or strain, throughout inhalation. Our results showed that the magnitude of strain was maximal at the base and apex of the lung, but was curtailed at the hilum, the anatomical site of the poorly mobile bronchial and vascular insertions. In-plane shear strain mapping showed mostly positive shear strain, predominant at the apex throughout inhalation, and increasing with expanding lung volume. Anisotropy mapping showed that superior-inferior axial strain was greater than medial-lateral axial strain at the apex and base, while the opposite was true for the middle lung field. This study demonstrates that localized pulmonary deformation can be measured in vivo with tagging MRI, and quantified by applying finite strain definitions from continuum mechanics.

The determination of principal fiber directions in structurally heterogeneous biological tissue substantially contributes to an understanding of its mechanical function in vivo. In this study we have depicted structural heterogeneity through the model of the mammalian tongue, a tissue comprised of a network of highly interwoven fibers responsible for producing numerous variations of shape and position. In order to characterize the three-dimensional-resolved microscopic myoarchitecture of the intrinsic musculature of the tongue, we viewed its fiber orientation at microscopic and macroscopic length scales using NMR (diffusion tensor MRI) and optical (two-photon microscopy) imaging methods. Diffusion tensor imaging (DTI) of the excised core region of the porcine tongue resulted in an array of 3D diffusion tensors, in which the leading eigenvector corresponded to the principal fiber orientation at each location in the tissue. Excised axially oriented lingual core tissues (fresh or paraffin-embedded) were also imaged with a mode-locked Ti-Sapphire laser, (76 MHz repetition rate, 150 femtosecond pulse width), allowing for the visualization of individual myofibers at in situ orientation. Fiber orientation was assessed by computing the 3D autocorrelation of discrete image volumes, and deriving the minimal eigenvector of the center voxel Hessian matrix. DTI of the fibers, comprising the intrinsic core of the tongue, demonstrated directional heterogeneity, with two distinct populations of fibers oriented orthogonal to each other and in-plane to the axial perspective. Microscopic analysis defined this structural heterogeneity as discrete regions of in-plane parallel fibers, with an angular separation of ~80 degrees, thereby recapitulating the macroscopic angular relationship. This analysis, conceived at two different length scales, demonstrates that the lingual core is a spatially complex tissue, composed of repeating orthogonally oriented and in-plane fiber patches, which are capable of jointly producing hydrostatic elongation and displacement.

Our goal was to quantify intramural mechanics in the tongue through an assessment of local strain during the physiological phases of swallowing. Subjects were imaged with an ultrafast gradient echo magnetic resonance imaging (MRI) pulse sequence after the application of supersaturated magnetized bands in the x and y directions. Local strain was defined through deformation of discrete triangular elements defined by these bands and was depicted graphically either as color-coded two-dimensional strain maps or as three-dimensional octahedra whose axes correspond to the principal strains for each element. During early accommodation, the anterior tongue showed positive strain (expansive) in the anterior-posterior direction (x), whereas the middle tongue showed negative strain (contractile) in the superior-inferior direction (y). During late accommodation, the anterior tongue displayed increased positive x-direction and y-direction strain, whereas the posterior tongue displayed increased negative y-direction strain. These findings were consistent with contraction of the anterior-located intrinsic muscles and the posterior-located genioglossus and hyoglossus muscles. During propulsion, posterior displacement of the tongue was principally associated with positive strain directed in the x and y directions. These findings were consistent with posterior passive stretch in the midline due to contraction of the laterally inserted styloglossus muscle, as well as contraction of the posterior located transversus muscle. We conclude that MRI of lingual deformation during swallowing resolves the synergistic contractions of the intrinsic and extrinsic muscle groups.

Contraction of the tongue musculature during speech and swallowing is associated with characteristic patterns of tissue deformation. In order to quantify local deformation (strain) in the human tongue, we used a non-invasive NMR tagging technique that represents tissue as discrete deforming elements. Subjects were studied with a fast gradient echo pulse sequence (TR,TE 2.3/0.8 ms, slice thickness 10 mm, and effective spatial resolution 1.3x1.3 mm). Individual elements were defined by selectively supersaturating bands of magnetic spills in resting tongue tissue along the antero-posterior and superior inferior directions of the mid-sagittal plane, resulting in a rectilinear square grid. Axial and shear strains relative to the rest condition were determined for each clement and represented by two-dimensional surface strain maps. During forward protrusion, the anterior tongue underwent positive antero posterior strain (elongation) (maximum 200%) and symmetrical negative medial lateral and superior inferior strain (contraction). During sagittal curl directed to the hard palate, the tongue exhibited positive asymmetrical antero posterior strain (maximum 160%) that increased radially as a function of distance from the center of curvature (r = 0.9216, p<0.0005), and commensurate negative strain in the medial lateral direction. Similarly, the magnitude of anterior posterior strain during left-directed tongue curl was proportional to the distance from the curved inner surface (r = O.8978, p<0.0005). We conclude that the regulation of tongue position for the motions studied was related to regional activation of the intrinsic lingual musculature.