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

Abstract

The anatomy of the mammalian tongue consists of an intricate array of variably aligned and extensively interwoven muscle fibers. As a result, it is particularly difficult to resolve the relationship between the tongue's microscopic anatomy and tissue-scale mechanical function. In order to address this question, we employed a method, diffusion spectrum imaging (DSI) with tractography, for displaying the macroscopic orientational properties of the tissue's constituting myofibers. DSI measures spatially variant proton displacement for a given 3D imaging segment (voxel), reflecting the principal orientation(s) of its myofibers. Tractography uses the angular similarity displayed by the principal fiber populations of multiple adjacent voxels to generate tract-like structures. DSI with tractography thus defines a unique set of tracts based on the net orientational behavior of the myofiber populations at different positions in the tissue. By this approach, we demonstrate a novel myoarchitectural pattern for the bovine tongue, consisting of short and orthogonally aligned crossing fiber tracts in the intrinsic core region, and longer, parallel-aligned fiber tracts on the tissue margins and in the regions of extrinsic fiber insertion. The identification of locally aligned myofiber populations by DSI with tractography allows us to reconsider lingual anatomy, not in conventional microscopic terms, but as a set of heterogeneously aligned and macroscopically resolved myofiber tracts. We postulate that the properties associated with these myofiber tracts predict the mechanical behavior of the tissue and thus constitute a method to relate structure and function for anatomically complex muscular tissues.

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

“…To address inaccuracies in assessing fiber direction in the case of intravoxel crossing, we developed DSI, which determines the alignment of geometrically heterogeneous fiber populations by deriving the complete 3-D spindisplacement function per voxel, and yields an ensemble pdf for the complete set of possible molecular displacements. 6,7 In order to relate the tissue's highly complex myoarchitecture with the myriad possible deformations occurring during physiological motion, we employed streamline tractography to align similar vector directions and thus generate mesoscale myofiber tracts, 8 whose length and orientation are believed to constitute structural templates for local contractility. In the current study, we have extended this methodology to a considerably higher resolution ͑voxel size of ϳ100 m 3 ͒ at 9.4 T. In so doing, we have confirmed previous concepts involving the merged architecture of the intrinsic and extrinsic fiber populations of the mammalian tongue and have determined a novel fiber configuration for the transversus and verticalis fibers of the intrinsic core of the tongue specific to the mouse model.…”

“…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. 8 On the basis of these formulations, we have postulated that tissue myoarchitecture may be depicted as an array of variably aligned myofiber tracts, which, in concert, comprise a mesoscale template for local tissue contractility.…”

The three‐dimensional arrangement of the myocytes in the ventricular walls

“…Using this technique, Gilbert et al (2006) have been able to demonstrate with exquisite accuracy the alignment of skeletal myocytes in the bovine tongue. We have also used the technique, demonstrating the alignment of the myocytes in the porcine heart.…”

In vivo 3 T MR diffusion tensor imaging for detection of the fibre architecture of the human uterus: a feasibility and quantitative study

“…There have been several MR-DTI feasibility studies in animals showing the anatomical fibre distribution in skeletal muscle, tongue and heart [5][6][7]. There have also been some studies on in vivo human skeletal muscle [8,9], tongue [10] and ventricular myocardium [11].…”