Resolving the three-dimensional myoarchitecture of bovine esophageal wall with diffusion spectrum imaging and tractography

Abstract

In order to determine the three-dimensional (3D) resolved muscular anatomy of the mammalian esophagus, we have examined its myoarchitecture with diffusion spectrum magnetic resonance imaging (DSI) and tractography. DSI measures diffusion displacement as a function of magnetic gradients of varied direction and intensity and displays the displacement profile as a 3D contour per voxel. In tractography, the orientation vectors of maximum diffusion/voxel are identified, and intervoxel associations are constructed by a streamline algorithm based on angular similarity in order to generate mesoscale myofiber tracts. We demonstrate that the proximal body of the esophagus consists of helically aligned crossing fiber populations that overlap between layers in the form of a "zipper" region along the length of the tissue. With increasingly distal position along the length of the tissue, helix angle and skeletal muscle prevalence are reduced such that fibers align themselves in the most distal location into distinct inner circular and outer longitudinal smooth muscle layers. We conclude that esophageal myoanatomy consists of crossing myofibers exhibiting a decreasing degree of helicity as a function of axial position and propose that this unique geometric construct provides a mechanism to resist distension and promote aboral flow.

Patterns of Intersecting Fiber Arrays Revealed in Whole Muscle with Generalized Q-Space Imaging

“…Furthermore, through this technique, we demonstrate, to our knowledge, two novel structures in the mouse tongue, the looplike muscles located in the superior and inferior regions of the anterior tongue, approximately analogous to the superior and inferior longitudinalis in humans. The presence of complex fiber geometries, such as merging, crossing, or helicity contribute substantially to the function of various other muscular hydrostats, such as the heart (14,17) and the esophagus (14,16,17), and numerous Animalia appendages, such as the elephant trunk (25,26,54) or octopus tentacles (55,56). Acknowledging the influences of multidirectional contractions, the understanding of muscular architecture may support continuum models of force generation in the setting of such hydrostats.…”

“…Angular separation so defined forms the underlying construct of the myofiber tract (mesoscale) obtained during streamlining, linking PDF diffusional maxima from one voxel to neighboring voxels. Tract coherence is, in turn, dependent upon voxel-scale angular resolution and the allowable tract generation angle, and has been validated through histological comparison (16,17,39) and microscopic correlation (14,38).…”

“…During diffusion-weighted MR imaging, magnetic field gradients of varying magnitudes and orientations are applied in order to define macroscopic anisotropy (8). Methods have been proposed to derive fiber orientation from diffusivity resolved at the voxel scale, such as diffusion tensor imaging (4,9,10), or multiple compartment models (11,12), and those resolved at the subvoxel scale, such as Q-ball imaging (13) and diffusion spectrum imaging (14)(15)(16)(17)(18). Voxel-scale analysis, however, does not accurately portray crossing or diverging fiber geometries (15,18,19), whereas subvoxel scale analysis conventionally requires exceedingly long imaging times, and is thus impractical for in vivo imaging of muscular organs.…”

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.…”

Circular and longitudinal muscles shortening indicates sliding patterns during peristalsis and transient lower esophageal sphincter relaxation

“…However, Miller and colleagues (3,16) showed that CM contraction also contributes to axial esophageal shortening because of the spiral morphology of CM in the distal esophagus. Gilbert et al (4) used diffusion tensor imaging and fiber tracking to show that CM fibers are arranged in spiral rather than circular fashion. Spiral angle of the CM increases from the proximal to distal esophagus.…”