Validation of an Echidna Forelimb Musculoskeletal Model Using XROMM and diceCT

Abstract

In evolutionary biomechanics, musculoskeletal computer models of extant and extinct taxa are often used to estimate joint range of motion (ROM) and muscle moment arms (MMAs), two parameters which form the basis of functional inferences. However, relatively few experimental studies have been performed to validate model outputs. Previously, we built a model of the short-beaked echidna (Tachyglossus aculeatus) forelimb using a traditional modelling workflow, and in this study we evaluate its behaviour and outputs using experimental data. The echidna is an unusual animal representing an edge-case for model validation: it uses a unique form of sprawling locomotion, and possesses a suite of derived anatomical features, in addition to other features reminiscent of extinct early relatives of mammals. Here we use diffusible iodine-based contrast-enhanced computed tomography (diceCT) alongside digital and traditional dissection to evaluate muscle attachments, modelled muscle paths, and the effects of model alterations on the MMA outputs. We use X-ray Reconstruction of Moving Morphology (XROMM) to compare ex vivo joint ROM to model estimates based on osteological limits predicted via single-axis rotation, and to calculate experimental MMAs from implanted muscles using a novel geometric method. We also add additional levels of model detail, in the form of muscle architecture, to evaluate how muscle torque might alter the inferences made from MMAs alone, as is typical in evolutionary studies. Our study identifies several key findings that can be applied to future models. 1) A light-touch approach to model building can generate reasonably accurate muscle paths, and small alterations in attachment site seem to have minimal effects on model output. 2) Simultaneous movement through multiple degrees of freedom, including rotations and translation at joints, are necessary to ensure full joint ROM is captured; however, single-axis ROM can provide a reasonable approximation of mobility depending on the modelling objectives. 3) Our geometric method of calculating MMAs is consistent with model-predicted MMAs calculated via partial velocity, and is a potentially useful tool for others to create and validate musculoskeletal models. 4) Inclusion of muscle architecture data can change some functional inferences, but in many cases reinforced conclusions based on MMA alone.

Keywords: SIMM; biomechanics; joint; mobility; muscle; muscle moment arm; range of motion; translation.

FIGURE 1

Different components of the musculoskeletal modelling process as detailed in the text.

FIGURE 2

Experimental set-up for ex vivo passive manipulation of echidna cadaver forelimbs. After markers were placed in bones and muscles, each animal was covered with plastic wrap to prevent drying out, tied to a custom-made carbon fibre platform oriented to allow limb manipulation, and placed in the field of view of two refurbished c-arm fluoroscopes for data collection.

FIGURE 3

Maximal Range of Motion (ROM) at the echidna forelimb joints. (A) scapulocoracoid-clavicle-interclavicle joint, (B) glenohumeral joint, (C) humeroradioulnar joint. Experimentally-estimated ROMs (pooled raw data) for each echidna specimen E44, E46 and E48 (coloured arcs, total ROM in parentheses) compared with initial model-predicted ROMs based on single DOF rotations (black arc, limits in bold text) about the X (red), Y (green) and Z (blue) axes. The dotted line represents the limb’s reference position. See Table 1 for more details.

FIGURE 4

Three-dimensional (3D) joint ROM at the glenohumeral joint (top row, blue) and humeroradioulnar joint (bottom row, orange). Note that axis scale differs between plots. The 3D envelopes encompass cosine-corrected experimental ROMs wrapped in a concave hull (alpha value 20), whilst the plotted points behind in the same colour show the uncorrected experimental ROMs. The initial model-predicted maximum ROMs for single DOF rotations from the zero (reference) position have been superimposed on the 3D plots as red (X), green (Y), and blue (Z) cubes (data from Regnault and Pierce (2018)). Individual specimen trial sets are illustrated in Supplementary Figure S4.

FIGURE 5

Representative trials (left) and frequency distributions of MMAs for all kinematic trials (right) for muscles crossing the scapulocoracoid-clavicle-interclavicle joint. Representative trials for: (A) m. clavodeltoideus, (B) m. pectoralis cranial origin, (C) m. pectoralis caudal origin, (D) m. latissimus dorsi vertebral origin. The boxplots (E–H) show the distribution and median values of MMAs for all trials: (E) m. clavodeltoideus, (F) m. pectoralis cranial origin, (G) m. pectoralis caudal origin, (H) m. latissimus dorsi vertebral origin. Positive and negative MMAs are plotted as separate boxplots for each DOF. SIMM = model-predicted MMAs based on partial velocity; Maya = experimentally-calculated MMAs based on the geometric method.

FIGURE 6

Three-dimensional (3D) MMAs of m. pectoralis at the glenohumeral joint, plotted in cosine-corrected ROM space for the SIMM model (using partial velocity) and Maya experimental data (using the geometric method). MMA sign is indicated by point colour (positive values are purple, negative values are orange) with colour intensity scaled to relative MMA magnitude as described in the Methods. ABAD = abduction-adduction; LAR = long-axis rotation (internal-external rotation); FE = flexion-extension.

FIGURE 7

Three-dimensional (3D) MMAs of m. latissimus dorsi at the glenohumeral joint, plotted in cosine-corrected ROM space for the SIMM model (using partial velocity) and Maya experimental data (using the geometric method). MMA sign is indicated by point colour (positive values are purple, negative values are orange) with colour intensity scaled to relative MMA magnitude as described in the Methods. ABAD = abduction-adduction; LAR = long-axis rotation (internal-external rotation); FE = flexion-extension.

FIGURE 8

Three-dimensional (3D) MMAs of m. clavodeltoideus and m. coracobrachialis longus at the glenohumeral joint, plotted in cosine-corrected ROM space for the SIMM model (using partial velocity) and Maya experimental data (using the geometric method). MMA sign is indicated by point colour (positive values are purple, negative values are orange) with colour intensity scaled to relative MMA magnitude as described in the Methods. ABAD = abduction-adduction; LAR = long-axis rotation (internal-external rotation); FE = flexion-extension.

FIGURE 9

Three-dimensional (3D) MMAs of m. biceps brachii and m. triceps brachii at the glenohumeral joint, plotted in cosine-corrected ROM space for the SIMM model (using partial velocity) and Maya experimental data (using the geometric method). MMA sign is indicated by point colour (positive values are purple, negative values are orange) with colour intensity scaled to relative MMA magnitude as described in the Methods. ABAD = abduction-adduction; LAR = long-axis rotation (internal-external rotation); FE = flexion-extension. Plot for these muscles MMAs at the humeroradioulnar joint can be found in Supplementary Figure S5.

FIGURE 10

Representative kinematic trials (left) and frequency distributions of MMAs for all kinematic trials (right) for muscles crossing the glenohumeral joint. Representative trials for (A) m. clavodeltoideus, (B) m. coracobrachialis, (C) m. pectoralis cranial origin, (D) m. pectoralis caudal origin, (E) m. latissimus dorsi scapular origin, (F) m. latissimus dorsi vertebral origin. The boxplots (G–L) show the distribution and median values of MMAs for all trials: (G) m. clavodeltoideus, (H) m. coracobrachialis, (I) m. pectoralis cranial origin, (J) m. pectoralis caudal origin, (K) m. latissimus dorsi scapular origin, (L) m. latissimus dorsi vertebral origin. Positive and negative MMAs are plotted as separate boxplots for each DOF. SIMM = model-predicted MMAs based on partial velocity; Maya = experimentally-calculated MMAs based on the geometric method.

FIGURE 11

Representative kinematic trials (left) and frequency distributions of MMAs for all kinematic trials (right) crossing the glenohumeral (top) and humeroradioulnar joints (bottom). Representative trials for (A) m. biceps brachii at glenohumeral joint, (B) m. triceps brachii at glenohumeral joint, (C) m. biceps brachii at humeroradioulnar joint, (D) m. triceps brachii at humeroradioulnar joint. The boxplots (E–H) show the distribution and median values of MMAs for all trials: (E) m. biceps brachii at glenohumeral joint, (F) m. triceps brachii at glenohumeral joint, (G) m. biceps brachii at humeroradioulnar joint, (H) m. triceps brachii at humeroradioulnar joint. Positive and negative MMAs are plotted as separate boxplots for each DOF. SIMM = model-predicted MMAs based on partial velocity; Maya = experimentally-calculated MMAs based on the geometric method.

FIGURE 12

Model-predicted MMAs and muscle torques at the glenohumeral joint, using the updated SIMM model muscle pathways from diceCT and for single-axis DOF rotations: (A) Summed MMAs, (B) Summed torques. Major muscles contributing to summed torque (dashed lines) are labelled for each rotational DOF: (C) Abduction-adduction, (D) Flexion-extension, (E) Internal-external rotation. LAT = m. latissimus dorsi, TRI-L = m. triceps brachii longus, SUBSC = m. subscapularis, CB = m. coracobrachialis, CLAV-D = m. clavodeltoideus. For details on individual muscles, see the Supplementary Material.