Monotremes are a group of egg-laying mammals, possessing a mosaic of ancestral and derived anatomical features. Despite much interest in monotremes from phylogenetic, morphological, and ecological perspectives, they have been the subject of relatively few biomechanical studies. In this study, we examined shoulder and proximal forelimb muscle anatomy and architecture in the short-beaked echidna, Tachyglossus aculeatus, through contrast-enhanced computed tomography and gross dissection. Muscle architecture is a major determinant of muscle function and can indicate specialized muscle roles, such as the capacity for generating large forces (through large physiological cross-sectional area, PCSA) or working ranges (through long fascicle lengths). We hypothesized that some muscles would exhibit architectural specializations convergent with other fossorial and/or sprawling animals, and that other muscles would reflect the echidna’s unusual anatomy and locomotor style. Instead, we found the shoulder and proximal forelimb muscles in echidna to have little variation in their architecture. The muscles generally had long fascicles and small-to-intermediate PCSAs, consistent with force production over a wide working range. Further, muscles did not show overt differences in architecture that, in therian mammals, have been linked to increased forelimb mobility and the transition from sprawling to parasagittal posture. Our measures of architectural disparity placed the echidna closer to the tegu lizard than other sprawling fossorial mammals (e.g., mole). The low architectural diversity found in the echidna’s shoulder and proximal forelimb muscles is interpreted as a lack of functional specialization into distinct roles. We hope our study will contribute to greater understanding of monotreme anatomy and biomechanical function, and to the reconstruction of musculoskeletal evolution in mammals.
more »
« less
ROLE OF FORELIMB MORPHOLOGY IN MUSCLE SENSORIMOTOR FUNCTIONS DURING LOCOMOTION IN THE CAT
ABSTRACT Previous studies established strong links between morphological characteristics of mammalian hindlimb muscles and their sensorimotor functions during locomotion. Less is known about the role of forelimb morphology in motor outputs and generation of sensory signals. Here, we measured morphological characteristics of 46 forelimb muscles from 6 cats. These characteristics included muscle attachments, physiological cross-sectional area (PCSA), fascicle length, etc. We also recorded full-body mechanics and EMG activity of forelimb muscles during level overground and treadmill locomotion in 7 and 16 adult cats of either sex, respectively. We computed forelimb muscle forces along with force- and length-dependent sensory signals mapped onto corresponding cervical spinal segments. We found that patterns of computed muscle forces and afferent activities were strongly affected by the muscle’s moment arm, PCSA, and fascicle length. Morphology of the shoulder muscles suggests distinct roles of the forelimbs in lateral force production and movements. Patterns of length-dependent sensory activity of muscles with long fibers (brachioradialis, extensor carpi radialis) closely matched patterns of overall forelimb length, whereas the activity pattern of biceps brachii matched forelimb orientation. We conclude that cat forelimb muscle morphology contributes substantially to locomotor function, particularly to control lateral stability and turning, rather than propulsion.
more »
« less
- Award ID(s):
- 2024414
- PAR ID:
- 10656748
- Editor(s):
- Carson, Richard; Macefield, Vaughan
- Publisher / Repository:
- John Wiley & Sons Ltd
- Date Published:
- Volume:
- 603
- Issue:
- 2
- Page Range / eLocation ID:
- 447-487
- Subject(s) / Keyword(s):
- Muscle morphology, cat forelimb, somatosensory feedback, motor function, locomotion
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Abstract Quantitative functional anatomy of amniote thoracic and abdominal regions is crucial to understanding constraints on and adaptations for facilitating simultaneous breathing and locomotion. Crocodilians have diverse locomotor modes and variable breathing mechanics facilitated by basal and derived (accessory) muscles. However, the inherent flexibility of these systems is not well studied, and the functional specialisation of the crocodilian trunk is yet to be investigated. Increases in body size and trunk stiffness would be expected to cause a disproportionate increase in muscle force demands and therefore constrain the basal costal aspiration mechanism, necessitating changes in respiratory mechanics. Here, we describe the anatomy of the trunk muscles, their properties that determine muscle performance (mass, length and physiological cross‐sectional area [PCSA]) and investigate their scaling in juvenileAlligator mississippiensisspanning an order of magnitude in body mass (359 g–5.5 kg). Comparatively, the expiratory muscles (transversus abdominis,rectus abdominis,iliocostalis), which compress the trunk, have greater relative PCSA being specialised for greater force‐generating capacity, while the inspiratory muscles (diaphragmaticus,truncocaudalis ischiotruncus,ischiopubis), which create negative internal pressure, have greater relative fascicle lengths, being adapted for greater working range and contraction velocity. Fascicle lengths of the accessorydiaphragmaticusscaled with positive allometry in the alligators examined, enhancing contractile capacity, in line with this muscle's ability to modulate both tidal volume and breathing frequency in response to energetic demand during terrestrial locomotion. Theiliocostalis, an accessory expiratory muscle, also demonstrated positive allometry in fascicle lengths and mass. All accessory muscles of the infrapubic abdominal wall demonstrated positive allometry in PCSA, which would enhance their force‐generating capacity. Conversely, the basal tetrapod expiratory pump (transversus abdominis) scaled isometrically, which may indicate a decreased reliance on this muscle with ontogeny. Collectively, these findings would support existing anecdotal evidence that crocodilians shift their breathing mechanics as they increase in size. Furthermore, the functional specialisation of thediaphragmaticusand compliance of the body wall in the lumbar region against which it works may contribute to low‐cost breathing in crocodilians.more » « less
-
The evolution of upright limb posture in mammals may have enabled modifications of the forelimb for diverse locomotor ecologies. A rich fossil record of non-mammalian synapsids holds the key to unraveling the transition from “sprawling” to “erect” limb function in the precursors to mammals, but a detailed understanding of muscle functional anatomy is a necessary prerequisite to reconstructing postural evolution in fossils. Here we characterize the gross morphology and internal architecture of muscles crossing the shoulder joint in two morphologically-conservative extant amniotes that form a phylogenetic and morpho-functional bracket for non-mammalian synapsids: the Argentine black and white tegu Salvator merianae and the Virginia opossum Didelphis virginiana . By combining traditional physical dissection of cadavers with nondestructive three-dimensional digital dissection, we find striking similarities in muscle organization and architectural parameters. Despite the wide phylogenetic gap between our study species, distal muscle attachments are notably similar, while differences in proximal muscle attachments are driven by modifications to the skeletal anatomy of the pectoral girdle that are well-documented in transitional synapsid fossils. Further, correlates for force production, physiological cross-sectional area (PCSA), muscle gearing (pennation), and working range (fascicle length) are statistically indistinguishable for an unexpected number of muscles. Functional tradeoffs between force production and working range reveal muscle specializations that may facilitate increased girdle mobility, weight support, and active stabilization of the shoulder in the opossum—a possible signal of postural transformation. Together, these results create a foundation for reconstructing the musculoskeletal anatomy of the non-mammalian synapsid pectoral girdle with greater confidence, as we demonstrate by inferring shoulder muscle PCSAs in the fossil non-mammalian cynodont Massetognathus pascuali .more » « less
-
Traditional work loop studies, that use sinusoidal length trajectories with constant frequencies, lack the complexities of in vivo muscle mechanics observed in modern studies. This study refines methodology of the “avatar” method (a modified work loop) to infer in vivo muscle mechanics using ex vivo experiments with mouse extensor digitorum longus (EDL) muscles. The “avatar” method involves using EDL muscles to replicate in vivo time varying force, as demonstrated by previous studies focusing on guinea fowl lateral gastrocnemius (LG). The present study extends this method by using in vivo length trajectories and electromyographic (EMG) activity from rat medial gastrocnemius (MG) during various gaits on a treadmill. Methodological enhancements from previous work, including adjusted stimulation protocols and systematic variation of starting length, improved predictions of in vivo time varying force production (R2 0.80 – 0.96). The study confirms there are significant influence of length, stimulation, and their interactions on work loop variables (peak force, length at peak force, highest and average shortening velocity, and maximum and minimum active velocity), highlighting the importance of these interactions when muscles produce in vivo forces. We also investigated the limitations of traditional work loops in capturing muscle dynamics in legged locomotion (R2 0.01 – 0.71). While in vivo length trajectories enhanced force prediction, accurately predicting work per cycle remained challenging. Overall, the study emphasizes the utility of the avatar method in elucidating dynamic muscle mechanics and highlights areas for further investigation to refine its application in understanding in vivo muscle function.more » « less
-
null (Ed.)Abstract The domestic dog is interesting to investigate because of the wide range of body size, body mass, and physique in the many breeds. In the last several years, the number of clinical and biomechanical studies on dog locomotion has increased. However, the relationship between body structure and joint load during locomotion, as well as between joint load and degenerative diseases of the locomotor system (e.g. dysplasia), are not sufficiently understood. Collecting this data through in vivo measurements/records of joint forces and loads on deep/small muscles is complex, invasive, and sometimes unethical. The use of detailed musculoskeletal models may help fill the knowledge gap. We describe here the methods we used to create a detailed musculoskeletal model with 84 degrees of freedom and 134 muscles. Our model has three key-features: three-dimensionality, scalability, and modularity. We tested the validity of the model by identifying forelimb muscle synergies of a walking Beagle. We used inverse dynamics and static optimization to estimate muscle activations based on experimental data. We identified three muscle synergy groups by using hierarchical clustering. The activation patterns predicted from the model exhibit good agreement with experimental data for most of the forelimb muscles. We expect that our model will speed up the analysis of how body size, physique, agility, and disease influence neuronal control and joint loading in dog locomotion.more » « less
An official website of the United States government

