Skeletal muscle diffusion tensor-MRI fiber tracking: rationale, data acquisition and analysis methods, applications and future directions

Abstract

The mechanical functions of muscles involve the generation of force and the actuation of movement by shortening or lengthening under load. These functions are influenced, in part, by the internal arrangement of muscle fibers with respect to the muscle's mechanical line of action. This property is known as muscle architecture. In this review, we describe the use of diffusion tensor (DT)-MRI muscle fiber tracking for the study of muscle architecture. In the first section, the importance of skeletal muscle architecture to function is discussed. In addition, traditional and complementary methods for the assessment of muscle architecture (brightness-mode ultrasound imaging and cadaver analysis) are presented. Next, DT-MRI is introduced and the structural basis for the reduced and anisotropic diffusion of water in muscle is discussed. The third section discusses issues related to the acquisition of skeletal muscle DT-MRI data and presents recommendations for optimal strategies. The fourth section discusses methods for the pre-processing of DT-MRI data, the available approaches for the calculation of the diffusion tensor and the seeding and propagating of fiber tracts, and the analysis of the tracking results to measure structural properties pertinent to muscle biomechanics. Lastly, examples are presented of how DT-MRI fiber tracking has been used to provide new insights into how muscles function, and important future research directions are highlighted. Copyright © 2016 John Wiley & Sons, Ltd.

Keywords: diffusion MRI; muscle architecture; muscle mechanics; non-invasive; skeletal muscle.

Figure 1

Example fiber tracking of (A) fusiform muscle (semitendinosus) and (B) pennate muscle (soleus). A) Lateral and posterior view of the semitendinosus which shows its long muscle fibers and substantial surface of the tendon of insertion. B) Lateral and anterior view of the soleus. The lateral view shows the long fibers of the posterior and marginal soleus, whereas the anterior view clearly shows the pennate structure of the anterior soleus.

Figure 2

B-mode ultrasound image of the tibialis anterior muscle. The top margin of the image displays the skin and subcutaneous fat overlying the anterior compartment of the leg. Deep to this, the tibialis anterior muscle is shown. A bipennate structure is noted, with a superficial compartment and a deep compartment. The high signal structure separating the compartments is the aponeurosis, or central tendon into which the fibers insert. The tangent line T_a indicates its orientation, while the tangent line T_f indicates the local fascicle orientation. The angle between these lines is θ.

Figure 3

Fiber tracking of the tibialis anterior muscle using different fiber tracking stopping criteria. (A, C) Allowed angle change of 0° – 10° per fiber tracking step. (B, D) Allowed angle change of 0° – 30° per fiber tracking step. (A, B) Allowed FA range of 0.20 – 0.50. (C, D) Allowed FA range of 0.15 – 0.75. The different stopping criteria affect the length of the fibers, the apparent tendon insertion points, and the amount of spurious fibers (as primarily observed in the areas enclosed by the white boxes and ellipses), whereas the muscle belly appears similar for different tracking parameters.

Figure 4

Illustration of different fiber tracking seeding methods. (A, C) Fiber tracking is seeded from the yellow region of interest. (B, D) Fiber tracts are seeded in the whole muscle volume (WV). Only those fibers which cross the yellow region of interest are visualized. Whole volume seeding results in denser more homogeneous fiber tracking throughout the whole tibialis anterior muscle. (C, D) Fiber tracking results can be further refined by adding one or more AND (or NOT) ROIs shown in green. Only those fibers that cross both green regions of interest are visualized.

Figure 5

Illustration of method for calculating the pennation angle. The green plane indicates the plane lying tangent to the seed point s, from which a fiber tract emerges (red curved line). The white lines indicate the direction vector r and the normal unit vector n̂ This figure was previously published (52) and is used with permission of the Journal of Applied Physiology.