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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Similar stretch reflexes and behavioral patterns are expressed by the dominant and nondominant arms during postural control
Limb dominance is evident in many daily activities, leading to the prominent idea that each hemisphere of the brain specializes in controlling different aspects of movement. Past studies suggest that the dominant arm is primarily controlled via an internal model of limb dynamics that enables the nervous system to produce efficient movements. In contrast, the nondominant arm may be primarily controlled via impedance mechanisms that rely on the strong modulation of sensory feedback from individual joints to control limb posture. We tested whether such differences are evident in behavioral responses and stretch reflexes following sudden displacement of the arm during posture control. Experiment 1 applied specific combinations of elbow-shoulder torque perturbations (the same for all participants). Peak joint displacements, return times, end point accuracy, and the directional tuning and amplitude of stretch reflexes in nearly all muscles were not statistically different between the two arms. Experiment 2 induced specific combinations of joint motion (the same for all participants). Again, peak joint displacements, return times, end point accuracy, and the directional tuning and amplitude of stretch reflexes in nearly all muscles did not differ statistically when countering the imposed loads with each arm. Moderate to strong correlations were found between stretch reflexes and behavioral responses to the perturbations with the two arms across both experiments. Collectively, the results do not support the idea that the dominant arm specializes in exploiting internal models and the nondominant arm in impedance control by increasing reflex gains to counter sudden loads imposed on the arms during posture control. NEW & NOTEWORTHY A prominent hypothesis is that the nervous system controls the dominant arm through predictive internal models and the nondominant arm through impedance mechanisms. We tested whether stretch reflexes of muscles in the two arms also display such specialization during posture control. Nearly all behavioral responses and stretch reflexes did not differ statistically but were strongly correlated between the arms. The results indicate individual signatures of feedback control that are common for the two arms.
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- Award ID(s):
- 1814846
- NSF-PAR ID:
- 10294746
- Date Published:
- Journal Name:
- Journal of Neurophysiology
- Volume:
- 126
- Issue:
- 3
- ISSN:
- 0022-3077
- Page Range / eLocation ID:
- 743 to 762
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Abstract Existing models of human walking use low-level reflexes or neural oscillators to generate movement. While appropriate to generate the stable, rhythmic movement patterns of steady-state walking, these models lack the ability to change their movement patterns or spontaneously generate new movements in the specific, goal-directed way characteristic of voluntary movements. Here we present a neuromuscular model of human locomotion that bridges this gap and combines the ability to execute goal directed movements with the generation of stable, rhythmic movement patterns that are required for robust locomotion. The model represents goals for voluntary movements of the swing leg on the task level of swing leg joint kinematics. Smooth movements plans towards the goal configuration are generated on the task level and transformed into descending motor commands that execute the planned movements, using internal models. The movement goals and plans are updated in real time based on sensory feedback and task constraints. On the spinal level, the descending commands during the swing phase are integrated with a generic stretch reflex for each muscle. Stance leg control solely relies on dedicated spinal reflex pathways. Spinal reflexes stimulate Hill-type muscles that actuate a biomechanical model with eight internal joints and six free-body degrees of freedom. The model is able to generate voluntary, goal-directed reaching movements with the swing leg and combine multiple movements in a rhythmic sequence. During walking, the swing leg is moved in a goal-directed manner to a target that is updated in real-time based on sensory feedback to maintain upright balance, while the stance leg is stabilized by low-level reflexes and a behavioral organization switching between swing and stance control for each leg. With this combination of reflex-based stance leg and voluntary, goal-directed control of the swing leg, the model controller generates rhythmic, stable walking patterns in which the swing leg movement can be flexibly updated in real-time to step over or around obstacles.
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Abstract There is a functional trade‐off in the design of skeletal muscle. Muscle strength depends on the number of muscle fibers in parallel, while shortening velocity and operational distance depend on fascicle length, leading to a trade‐off between the maximum force a muscle can produce and its ability to change length and contract rapidly. This trade‐off becomes even more pronounced as animals increase in size because muscle strength scales with area (length2) while body mass scales with volume (length3). In order to understand this muscle trade‐off and how animals deal with the biomechanical consequences of size, we investigated muscle properties in the pectoral girdle of varanid lizards. Varanids are an ideal group to study the scaling of muscle properties because they retain similar body proportions and posture across five orders of magnitude in body mass and are highly active, terrestrially adapted reptiles. We measured muscle mass, physiological cross‐sectional area, fascicle length, proximal and distal tendon lengths, and proximal and distal moment arms for 27 pectoral girdle muscles in 13 individuals across 8 species ranging from 64 g to 40 kg. Standard and phylogenetically informed reduced major axis regression was used to investigate how muscle architecture properties scale with body size. Allometric growth was widespread for muscle mass (scaling exponent >1), physiological cross‐sectional area (scaling exponent >0.66), but not tendon length (scaling exponent >0.33). Positive allometry for muscle mass was universal among muscles responsible for translating the trunk forward and flexing the elbow, and nearly universal among humeral protractors and wrist flexors. Positive allometry for PCSA was also common among trunk translators and humeral protractors, though less so than muscle mass. Positive scaling for fascicle length was not widespread, but common among humeral protractors. A higher proportion of pectoral girdle muscles scaled with positive allometry than our previous work showed for the pelvic girdle, suggesting that the center of mass may move cranially with body size in varanids, or that the pectoral girdle may assume a more dominant role in locomotion in larger species. Scaling exponents for physiological cross‐sectional area among muscles primarily associated with propulsion or with a dual role were generally higher than those associated primarily with support against gravity, suggesting that locomotor demands have at least an equal influence on muscle architecture as body support. Overall, these results suggest that larger varanids compensate for the increased biomechanical demands of locomotion and body support at higher body sizes by developing larger pectoral muscles with higher physiological cross‐sectional areas. The isometric scaling rates for fascicle length among locomotion‐oriented pectoral girdle muscles suggest that larger varanids may be forced to use shorter stride lengths, but this problem may be circumvented by increases in limb excursion afforded by the sliding coracosternal joint.
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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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Sport-related injuries to articular structures often alter the sensory information conveyed by joint structures to the nervous system. However, the role of joint sensory afferents in motor control is still unclear. Here, we evaluate the role of knee joint sensory afferents in the control of quadriceps muscles, hypothesizing that such sensory information modulates control strategies that limit patellofemoreal joint loading. We compared locomotor kinematics and muscle activity before and after inhibition of knee sensory afferents by injection of lidocaine into the knee capsule of rats. We evaluated whether this inhibition reduced the strength of correlation between the activity of vastus medialis (VM) and vastus lateralis (VL) both across strides and within each stride, coordination patterns that limit net mediolateral patellofemoral forces. We also evaluated whether this inhibition altered correlations among the other quadriceps muscle activity, the time-profiles of individual EMG envelopes, or movement kinematics. Neither the EMG envelopes nor limb kinematics was affected by the inhibition of knee sensory afferents. This perturbation also did not affect the correlations between VM and VL, suggesting that the regulation of patellofemoral joint loading is mediated by different mechanisms. However, inhibition of knee sensory afferents caused a significant reduction in the correlation between vastus intermedius (VI) and both VM and VL across, but not within, strides. Knee joint sensory afferents may therefore modulate the coordination between the vasti muscles but only at coarse time scales. Injuries compromising joint afferents might result in altered muscle coordination, potentially leading to persistent internal joint stresses and strains. NEW & NOTEWORTHY Sensory afferents originating from knee joint receptors provide the nervous system with information about the internal state of the joint. In this study, we show that these sensory signals are used to modulate the covariations among the activity of a subset of vasti muscles across strides of locomotion. Sport-related injuries that damage joint receptors may therefore compromise these mechanisms of muscle coordination, potentially leading to persistent internal joint stresses and strains.more » « less
- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1152/jn.00152.2021
