Mapping Complex Myoarchitecture in the Bovine Tongue with Diffusion-Spectrum Magnetic Resonance Imaging

Abstract

The ability to resolve complex fiber populations in muscular tissues is important for relating tissue structure with mechanical function. To address this issue in the case of tongue, we employed diffusion spectrum imaging (DSI), an MRI method for determining three-dimensional myoarchitecture where myofiber populations are variably aligned. By specifically varying gradient field strength, molecular displacement in a tissue can be determined by Fourier-transforming the echo intensity against gradient strength at fixed gradient pulse spacing. The displacement profiles are visualized by graphing three-dimensional isocontour icons for each voxel, with the isocontour shape and size representing the magnitude and direction of the constituting fiber populations. To validate this method, we simulated a DSI experiment within the constraints of arbitrary crossing fibers, and determined that DSI accurately depicts the angular relationships between these fibers. Considering the fiber relationships in the whole bovine tongue, we compared the images obtained by DSI with those obtained by diffusion tensor imaging in an anterior slice of the lingual core, a region known to possess extensive fiber crossing. In contrast to diffusion tensor imaging, which depicts the anterior core solely as a region with low anisotropy due to the presence of mixed-orientation fiber populations, DSI shows two distinct fiber populations, with an explicit orthogonal relationship to each other. In imaging the whole lingual tissue, we discerned arrays of crossing and noncrossing fibers involving the intrinsic and extrinsic muscles, which merged at regions of interface. We conclude that DSI has the capacity to determine three-dimensional fiber orientation in structurally complex muscular tissues.

Three‐dimensional myoarchitecture of the bovine tongue demonstrated by diffusion spectrum magnetic resonance imaging with tractography

“…In this article, we use the term PDF to refer to the observed average distribution obtained from DSI processing of the signal. The use of DSI for imaging lingual fiber populations has been previously described (Gilbert et al, 2006). In brief, during DSI, diffusion-weighted images are acquired for a sphere of q vectors with indexed values in a Cartesian grid in q-space in order to produce a three-dimensional probability distribution.…”

“…In the current study, we have employed a variation on the above diffusion-weighted methods, termed diffusion spectrum imaging (DSI), to resolve intravoxel complexity of fiber orientation characteristic for the tongue (Wedeen et al, 2000;Tuch, 2002;Lin et al, 2003;Gilbert et al, 2006). We combined this method with tractography (Basser, 1998), a method defining macroscopic scale geometric associations of fibers on the basis of the similarity of their alignment from one location to another in the tissue.…”

Multiscale structural analysis of mouse lingual myoarchitecture employing diffusion spectrum magnetic resonance imaging and multiphoton microscopy

“…Examples of such tissues include the tongue, 1,2 heart, 3 vasculature, 4 and gastrointestinal tract. 5 We have previously demonstrated the feasibility of imaging 3-D myoarchitecture in whole tissues through the use of diffusion spectrum magnetic resonance imaging ͑DSI͒, 6,7 a method that resolves the orientation of complex multifiber arrays by the identification of one or multiple diffusion maxima per voxel. These diffusion maxima may also be associated into mesoscale constructs ͑myofiber tracts͒ defined by the angular similarity exhibited by the principal diffusion vectors in multiple adjacent voxels.…”

“…11 We propose that the specific orientational distribution function ͑ODF͒ for fiber alignment, derived either from DSI or TPM, constitutes a common metric by which fiber orientation can be related at the scale of the single cell, multicellular array, and the tissue. The tongue is a particularly interesting model for this form of study because we have previously determined, in both in vitro, 6,7,12 and in vivo 13 studies, that its myoarchitecture contains continuous arrays of crossing fibers, and we have inferred from its underlying structure the basis for its physiological deformations. [14][15][16] We have specifically shown in the case of the tongue the capacity to derive net microscopic fiber orien-tation employing TPM and autocorrelation analysis in the case of single fields of view.…”

A Bloch-Torrey Equation for Diffusion in a Deforming Media

“…Knowledge of this diffusion in cases of various biological tissues such as cardiac muscle [1][2][3][4][5] , skeletal muscles [6][7][8][9], brain [10][11][12][13], tongue [14][15][16], spinal cord [17,18] or other [19] is therefore a probe into their intrinsic structures. Diffusion measurement using the Diffusion Tensor Magnetic Resonance Imaging (DTMRI) technique is a powerful tool for exploring the microscopic structure of tissues.…”