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The ‘sprawling–parasagittal’ transition was a major postural shift that occurred in the ancestors of mammals, [PSE1] underpinned by musculoskeletal reorganization of the limbs. However, ‘when’ and ‘how’ this important postural shift occurred is unknown. While the anatomical changes characterizing this transition can be traced through the fossil record, how these relate to functional changes, and the acquisition of parasagittal posture, remains poorly understood. Here, we produced three-dimensional musculoskeletal models of the forelimbs of extant (n=3) and fossil (n=8) taxa that phylogenetically and functionally span the sprawling–parasagittal transition. We calculated joint range of motion (ROM) to determine a 3D pose space, using the novel APSE algorithm (Accelerated Pose Searching with Electrostatics). We then estimated muscle moment arms (MMAs) across the entire pose space for all muscles crossing the shoulder and elbow joints. Models of extant species were validated against empirical measures of ROM and MMA derived from ex vivo XROMM (X-ray reconstruction of moving morphology). Among extant species, our parasagittal taxon occupied a distinct region of pose-space, with more retracted and depressed shoulder joint angles. MMA data show increased emphasis on shoulder elevation associated with a parasagittal posture, but greater shoulder depression in sprawlers. Results from the fossil species show complex, non-linear patterns of forelimb transformation, demonstrating that the ‘sprawling-parasagittal’ transition is characterized by homoplasy and postural variation within the mammalian lineage.
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Anticipatory weight shift between arms when reaching from a crouched posture
Reaching movements performed from a crouched body posture require a shift of body weight from both arms to one arm. This situation has remained unexamined despite the analogous load requirements during step initiation and the many studies of reaching from a seated or standing posture. To determine whether the body weight shift involves anticipatory or exclusively reactive control, we obtained force plate records, hand kinematics, and arm muscle activity from 11 healthy right-handed participants. They performed reaching movements with their left and right arm in two speed contexts, “comfortable” and “as fast as possible,” and two postural contexts, a less stable knees-together posture and a more stable knees-apart posture. Weight-shifts involved anticipatory postural actions (APAs) by the reaching and stance arms that were opposing in the vertical axis and aligned in the side-to-side axis similar to APAs by the legs for step initiation. Weight-shift APAs were correlated in time and magnitude, present in both speed contexts, more vigorous with the knees placed together, and similar when reaching with the dominant and nondominant arm. The initial weight-shift was preceded by bursts of muscle activity in the shoulder and elbow extensors (posterior deltoid and triceps lateral) of the reach arm and shoulder flexor (pectoralis major) of the stance arm, which indicates their causal role; leg muscles may have indirectly contributed but were not recorded. The strong functional similarity of weight-shift APAs during crouched reaching to human stepping and cat reaching suggests that they are a core feature of posture-movement coordination. NEW & NOTEWORTHY This work demonstrates that reaching from a crouched posture is preceded by bimanual anticipatory postural adjustments (APAs) that shift the body weight to the stance limb. Weight-shift APAs are more robust in an unstable body posture (knees together) and involve the shoulder and elbow extensors of the reach arm and shoulder flexor of the stance arm. This pattern mirrors the forelimb coordination of cats reaching and humans initiating a step.
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- Award ID(s):
- 1814846
- PAR ID:
- 10354696
- Date Published:
- Journal Name:
- Journal of Neurophysiology
- Volume:
- 126
- Issue:
- 4
- ISSN:
- 0022-3077
- Page Range / eLocation ID:
- 1361 to 1374
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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The ‘sprawling-parasagittal’ transition was a major postural shift in the ancestors of mammals, resulting in musculoskeletal reorganization of the forelimbs that underpins modern mammal locomotor diversity. However, ‘when’ and ‘how’ this important postural shift occurred is unknown. While the anatomical changes characterizing this transition can be traced through the fossil record, how these relate to functional changes, and the acquisition of parasagittal posture, remains poorly understood. We produced three-dimensional musculoskeletal models of the forelimbs of extant (n=3) and fossil (n=8) taxa that phylogenetically and functionally span the sprawling–parasagittal transition. We calculated joint range of motion (ROM) to determine a 3D pose-space, using the novel APSE algorithm (Accelerated Pose Searching with Electrostatics). We then estimated muscle moment arms (MMAs) across the entire pose space for all muscles crossing the shoulder and elbow joints. Models of extant species were validated against empirical measures of ROM and MMA derived from ex vivo XROMM (X-ray reconstruction of moving morphology). Among extant species, in both models and experiments, our parasagittal taxon occupied a distinct region of pose-space, with more retracted and depressed shoulder joint angles. MMA data show increased emphasis on shoulder elevation associated with a parasagittal posture, but greater shoulder depression in sprawlers. We hypothesised the fossil taxa would follow trends in these postural variables – e.g., increasing shoulder retraction and elevation MMAs through time – but they instead showed complex, non-linear patterns of forelimb transformation. We demonstrate that the ‘sprawling-parasagittal’ transition is characterized by considerable homoplasy and continuous postural variation throughout mammalian evolution.more » « less
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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
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- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1152/jn.00644.2020
