Muscle moment arms and sensitivity analysis of a mouse hindlimb musculoskeletal model

Abstract

Musculoskeletal modelling has become a valuable tool with which to understand how neural, muscular, skeletal and other tissues are integrated to produce movement. Most musculoskeletal modelling work has to date focused on humans or their close relatives, with few examples of quadrupedal animal limb models. A musculoskeletal model of the mouse hindlimb could have broad utility for questions in medicine, genetics, locomotion and neuroscience. This is due to this species’ position as a premier model of human disease, having an array of genetic tools for manipulation of the animal in vivo, and being a small quadruped, a category for which few models exist. Here, the methods used to develop the first three‐dimensional (3D) model of a mouse hindlimb and pelvis are described. The model, which represents bones, joints and 39 musculotendon units, was created through a combination of previously gathered muscle architecture data from microdissections, contrast‐enhanced micro‐computed tomography (CT) scanning and digital segmentation. The model allowed muscle moment arms as well as muscle forces to be estimated for each musculotendon unit throughout a range of joint rotations. Moment arm analysis supported the reliability of musculotendon unit placement within the model, and comparison to a previously published rat hindlimb model further supported the model's reliability. A sensitivity analysis performed on both the force‐generating parameters and muscle's attachment points of the model indicated that the maximal isometric muscle moment is generally most sensitive to changes in either tendon slack length or the coordinates of insertion, although the degree to which the moment is affected depends on several factors. This model represents the first step in the creation of a fully dynamic 3D computer model of the mouse hindlimb and pelvis that has application to neuromuscular disease, comparative biomechanics and the neuromechanical basis of movement. Capturing the morphology and dynamics of the limb, it enables future dissection of the complex interactions between the nervous and musculoskeletal systems as well as the environment.

Dynamic Musculoskeletal Functional Morphology: Integrating diceCT and XROMM

“…We demonstrate how diceCT can be incorporated into XROMM and EMG workflows to study over a dozen muscles, many of which are difficult to access surgically for FMM. Moreover, because in silico studies have demonstrated that measures of joint moment are sensitive to the accuracy of muscle attachment site location (Hutchinson et al, 2015;Charles et al, 2016b), we demonstrate the sensitivity of XROMM-based muscle kinematics to variation in attachment site location. We also demonstrate that these methods are precise enough to measure in vivo muscle fiber linear and angular velocity in our model system, the hyolingual apparatus of the rhesus macaque (Macaca mulatta).…”

“…Not only does diceCT have the potential to improve our ability to measure musculo‐tendon morphology, but it also enables data collection from museum specimens that were previously inaccessible to destructive techniques. Applications of diceCT and other staining methods include the digital dissection of muscles too small or complex for traditional dissection (Metscher, ; Jeffery et al, ; Holliday et al, ; Porro and Richards, ), determining muscle orientation in models of bite force (Gignac and Erickson, ; Sellers et al, ), reconstructing three‐dimensional muscle architecture (Kupczik et al, ; Dickinson et al, 2018), and improving the accuracy of inverse dynamic modeling of joint moments (Charles et al, ). One of diceCT's key strengths in muscle functional morphology is its potential to measure muscle architecture in situ , which may generate more accurate measures of joint moment if architecture varies along the length of the muscle's attachment site.…”

“…While the example described here involves in vivo data collection, Autodesk Maya's powerful animation capabilities and XROMM's user-friendly scripts could be used for in silico modeling to evaluate how skeletal motion affects whole-muscle length, orientation, and moment arm, as has been performed with other modeling software (Hutchinson et al, 2005;Delp et al, 2007;Hutchinson et al, 2015;Charles et al, 2016b). Given that visible iodine staining is reversible by either leaching or soaking in sodium thiosulfate (Gignac et al, 2016;Morhardt et al, 2016), this method could be applied to museum specimens with intact soft tissue without damaging or destroying the specimens.…”

Gearing effects of the patella (knee extensor muscle sesamoid) of the helmeted guineafowl during terrestrial locomotion

“…Smith et al ., 2007; Johnson et al ., 2008; Charles et al ., 2016) or do not analyse the patellofemoral joint separately from the knee joint (e.g. O'Neill et al ., 2013).…”

“…Equivalent data from other species are rare, as most studies of pelvic limb moment arms in species with patellae either ignore it (e.g. Smith et al, 2007;Johnson et al, 2008;Charles et al, 2016) or do not analyse the patellofemoral joint separately from the knee joint (e.g. O'Neill et al, 2013).…”