Anatomical basis of lingual hydrostatic deformation

Richard J Gilbert,Terry A Gaige,Vitaly J Napadow,Van J Wedeen

doi:10.1242/jeb.007096

Abstract

The mammalian tongue is believed to fall into a class of organs known as muscular hydrostats, organs for which muscle contraction both generates and provides the skeletal support for motion. We propose that the myoarchitecture of the tongue, consisting of intricate arrays of muscular fibers, forms the structural basis for hydrostatic deformation. Owing to the fact that maximal diffusion of the ubiquitous water molecule occurs orthogonal to the short axis of most fiber-type cells, diffusion-weighted magnetic resonance imaging (MRI) measurements can be used to derive information regarding 3-D fiber orientation in situ. Image data obtained in this manner suggest that the tongue consists of a complex juxtaposition of muscle fibers oriented in orthogonal arrays, which provide the basis for multidirectional contraction and isovolemic deformation. From a mechanical perspective, the lingual tissue may be considered as set of continuous coupled units of compression and expansion from which 3-D strain maps may be derived. Such functional data demonstrate that during physiological movements, such as protrusion, bending and swallowing, hydrostatic deformation occurs via synergistic contractions of orthogonally aligned intrinsic and extrinsic fibers. Lingual deformation can thus be represented in terms of models demonstrating that synergistic contraction of fibers at orthogonal or near-orthogonal directions to each other is a necessary condition for volume-conserving deformation. Evidence is provided in support of the supposition that hydrostatic deformation is based on the contraction of orthogonally aligned intramural fibers functioning as a mechanical continuum.

Highlights

We contend that the ability of the mammalian tongue to carry out its large array of physiological motions is based on its muscular anatomy, which is composed of complex fiber arrays aligned at various angles orthogonal to the direction of deformation
We propose that these fiber alignments comprise the structural underpinnings for hydrostatic deformation and are fundamental to the generation of lingual force
The fiber planes of the tongue sheath are concentric with the surface of the tongue and locally parallel to the adjacent surface of the tissue. This approach resolves the constituent muscles of the tongue based on the principal directions of its fibers and the angular dispersion of these fibers within the imaged element. By this formulation, the principal fiber orientation at each location in the image corresponds to the leading eigenvector of the diffusion tensor, whereas the second eigenvector identifies the orientation of maximum fiber angle dispersion in each voxel