Mammalian locomotion is generated by central pattern generators (CPGs) in the spinal cord, which produce alternating flexor and extensor activities controlling the locomotor movements of each limb. Afferent feedback signals from the limbs are integrated by the CPGs to provide adaptive control of locomotion. Responses of CPG-generated neural activity to afferent feedback stimulation have been previously studied during fictive locomotion in immobilized cats. Yet, locomotion in awake, behaving animals involves dynamic interactions between central neuronal circuits, afferent feedback, musculoskeletal system, and environment. To study these complex interactions, we developed a model simulating interactions between a half-center CPG and the musculoskeletal system of a cat hindlimb. Then, we analyzed the role of afferent feedback in the locomotor adaptation from a dynamic viewpoint using the methods of dynamical systems theory and nullcline analysis. Our model reproduced limb movements during regular cat walking as well as adaptive changes of these movements when the foot steps into a hole. The model generates important insights into the mechanism for adaptive locomotion resulting from dynamic interactions between the CPG-based neural circuits, the musculoskeletal system, and the environment.
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Reaction Forces and Rib Function During Locomotion in Snakes
Synopsis Locomotion in most tetrapods involves coordinated efforts between appendicular and axial musculoskeletal systems, where interactions between the limbs and the ground generate vertical (GV), horizontal (GH), and mediolateral (GML) ground-reaction forces that are transmitted to the axial system. Snakes have a complete absence of external limbs and represent a fundamental shift from this perspective. The axial musculoskeletal system of snakes is their primary structure to exert, transmit, and resist all motive and reaction forces for propulsion. Their lack of limbs makes them particularly dependent on the mechanical interactions between their bodies and the environment to generate the net GH they need for forward locomotion. As organisms that locomote on their bellies, the forces that enable the various modes of snake locomotion involve two important structures: the integument and the ribs. Snakes use the integument to contact the substrate and produce a friction-reservoir that exceeds their muscle-induced propulsive forces through modulation of scale stiffness and orientation, enabling propulsion through variable environments. XROMM work and previous studies suggest that the serially repeated ribs of snakes change their cross-sectional body shape, deform to environmental irregularities, provide synergistic stabilization for other muscles, and differentially exert and transmit forces to control propulsion. The costovertebral joints of snakes have a biarticular morphology, relative to the unicapitate costovertebral joints of other squamates, that appears derived and not homologous with the ancestral bicapitate ribs of Amniota. Evidence suggests that the biarticular joints of snakes may function to buttress locomotor forces, similar to other amniotes, and provide a passive mechanism for resisting reaction forces during snake locomotion. Future comparisons with other limbless lizard taxa are necessary to tease apart the mechanics and mechanisms that produced the locomotor versatility observed within Serpentes.
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- NSF-PAR ID:
- 10192794
- Date Published:
- Journal Name:
- Integrative and Comparative Biology
- Volume:
- 60
- Issue:
- 1
- ISSN:
- 1540-7063
- Page Range / eLocation ID:
- 215 to 231
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Abstract Muscles spanning multiple joints play important functional roles in a wide range of systems across tetrapods; however, their fundamental mechanics are poorly understood, particularly the consequences of anatomical position on mechanical advantage. Snakes provide an excellent study system for advancing this topic. They rely on the axial muscles for many activities, including striking, constriction, defensive displays, and locomotion. Moreover, those muscles span from one or a few vertebrae to over 30, and anatomy varies among muscles and among species. We characterized the anatomy of major epaxial muscles in a size series of corn snakes (
Pantherophis guttatus ) using diceCT scans, and then took several approaches to calculating contributions of each muscle to force and motion generated during body bending, starting from a highly simplistic model and moving to increasingly complex and realistic models. Only the most realistic model yielded equations that included the consequence of muscle span on torque‐displacement trade‐offs, as well as resolving ambiguities that arose from simpler models. We also tested whether muscle cross‐sectional areas or lever arms (total magnitude or pitch/yaw/roll components) were related to snake mass, longitudinal body region (anterior, middle, posterior), and/or muscle group (semispinalis‐spinalis, multifidus, longissimus dorsi, iliocostalis, and levator costae). Muscle cross‐sectional areas generally scaled with positive allometry, and most lever arms did not depart significantly from geometric similarity (isometry). The levator costae had lower cross‐sectional area than the four epaxial muscles, which did not differ significantly from each other in cross‐sectional area. Lever arm total magnitudes and components differed among muscles. We found some evidence for regional variation, indicating that functional regionalization merits further investigation. Our results contribute to knowledge of snake muscles specifically and multiarticular muscle systems generally, providing a foundation for future comparisons across species and bioinspired multiarticular systems. -
Soft robotic snakes made of compliant materials can continuously deform their bodies and, therefore, mimic the biological snakes' flexible and agile locomotion gaits better than their rigid-bodied counterparts. Without wheel support, to date, soft robotic snakes are limited to emulating planar locomotion gaits, which are derived via kinematic modeling and tested on robotic prototypes. Given that the snake locomotion results from the reaction forces due to the distributed contact between their skin and the ground, it is essential to investigate the locomotion gaits through efficient dynamic models capable of accommodating distributed contact forces. We present a complete spatial dynamic model that utilizes a floating-base kinematic model with distributed contact dynamics for a pneumatically powered soft robotic snake. We numerically evaluate the feasibility of the planar and spatial rolling gaits utilizing the proposed model and experimentally validate the corresponding locomotion gait trajectories on a soft robotic snake prototype. We qualitatively and quantitatively compare the numerical and experimental results which confirm the validity of the proposed dynamic model.more » « less
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Abstract Investigating skeletal adaptations to bipedalism informs our understanding of form–function relationships. The calcaneus is an important skeletal element to study because it is a weight‐bearing bone with a critical locomotor role. Although other calcaneal regions have been well studied, we lack a clear understanding of the functional role of the lateral plantar process (LPP). The LPP is a bony protuberance on the inferolateral portion of the calcaneus thought to aid the tuberosity in transmission of ground reaction forces during heel‐strike. Here, we analyze LPP internal trabecular structure relative to other calcaneal regions to investigate its potential functional affinities. Human calcanei (
n = 20) were micro‐CT scanned, and weighted spherical harmonic analysis outputs were used to position 251 volumes of interest (VOI) within each bone. Trabecular thickness (Tb.Th), spacing (Tb.Sp), degree of anisotropy (DA), and bone volume fraction (BV/TV) were calculated for each VOI. Similarities in BV/TV and DA (p = 0.2741) between the LPP and inferior tuberosity support suggestions that the LPP is a weight‐bearing structure that may transmit forces in a similar direction. The LPP significantly differs from the inferior tuberosity in Tb.Th and Tb.Sp (p < 0.05). Relatively thinner, more closely spaced trabeculae in the LPP may serve to increase internal surface area to compensate for its relatively small size compared to the tuberosity. Significant differences in all parameters between LPP and joint articular surfaces indicate that trabecular morphology is differently adapted for the transmission of forces associated with body mass through joints. -
null (Ed.)The small structures that decorate biological surfaces can significantly affect behavior, yet the diversity of animal–environment interactions essential for survival makes ascribing functions to structures challenging. Microscopic skin textures may be particularly important for snakes and other limbless locomotors, where substrate interactions are mediated solely through body contact. While previous studies have characterized ventral surface features of some snake species, the functional consequences of these textures are not fully understood. Here, we perform a comparative study, combining atomic force microscopy measurements with mathematical modeling to generate predictions that link microscopic textures to locomotor performance. We discover an evolutionary convergence in the ventral skin structures of a few sidewinding specialist vipers that inhabit sandy deserts—an isotropic texture that is distinct from the head-to-tail-oriented, micrometer-sized spikes observed on a phylogenetically broad sampling of nonsidewinding vipers and other snakes from diverse habitats and wide geographic range. A mathematical model that relates structural directionality to frictional anisotropy reveals that isotropy enhances movement during sidewinding, whereas anisotropy improves movement during slithering via lateral undulation of the body. Our results highlight how an integrated approach can provide quantitative predictions for structure–function relationships and insights into behavioral and evolutionary adaptations in biological systems.more » « less
- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1093/icb/icaa033
