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The manifold structure of limb coordination in walking Drosophila.

ABSTRACT: Terrestrial locomotion requires animals to coordinate their limb movements to efficiently traverse their environment. While previous studies in hexapods have reported that limb coordination patterns can vary substantially, the structure of this variability is not yet well understood. Here, we characterized the symmetric and asymmetric components of variation in walking kinematics in the genetic model organism Drosophila. We found that Drosophila use a single continuum of coordination patterns without evidence for preferred configurations. Spontaneous symmetric variability was associated with modulation of a single control parameter-stance duration-while asymmetric variability consisted of small, limb-specific modulations along multiple dimensions of the underlying symmetric pattern. Commands that modulated walking speed, originating from artificial neural activation or from the visual system, evoked modulations consistent with spontaneous behavior. Our findings suggest that Drosophila employ a low-dimensional control architecture, which provides a framework for understanding the neural circuits that regulate hexapod legged locomotion.

SUBMITTER: DeAngelis BD

PROVIDER: S-EPMC6598772 | biostudies-literature | 2019 Jun

REPOSITORIES: biostudies-literature

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The manifold structure of limb coordination in walking Drosophila.

DeAngelis Brian D BD Zavatone-Veth Jacob A JA Clark Damon A DA

eLife 20190628

Terrestrial locomotion requires animals to coordinate their limb movements to efficiently traverse their environment. While previous studies in hexapods have reported that limb coordination patterns can vary substantially, the structure of this variability is not yet well understood. Here, we characterized the symmetric and asymmetric components of variation in walking kinematics in the genetic model organism Drosophila. We found that Drosophila use a single continuum of coordinati ...[more]

PMID: 31250807

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Project description:Lower-limb intersegmental coordination is a complex component of human walking. Aging may result in impairments of motor control and coordination contributing to the decline in mobility inducing loss of autonomy. Investigating intersegmental coordination could therefore provide insights into age-related changes in neuromuscular control of gait. However, it is unknown whether the age-related declines in gait performance relates to intersegmental coordination. The aim of this study was to evaluate the impact of aging on the coordination of lower limb kinematics and kinetics during walking at a conformable speed. We then assessed the body kinematics and kinetics from gait analyses of 84 volunteers from 25 to 85 years old when walking was performed at their self-selected speeds. Principal Component Analysis (PCA) was used to assess lower-limb intersegmental coordination and to evaluate the planar covariation of the Shank-Thigh and Foot-Shank segments. Ankle and knee stiffness were also estimated. Age-related effects on planar covariation parameters was evaluated using multiple linear regressions (i.e., without a priori age group determination) adjusted to normalized self-selected gait velocity. Colinearity between parameters was assessed using a variation inflation factor (VIF) and those with a VIF < 5 were entered in the analysis. Normalized gait velocity significantly decreased with aging (r = -0.24; P = 0.028). Planar covariation of inter-segmental coordination was consistent across age (99.3 ± 0.24% of explained variance of PCA). Significant relationships were found between age and intersegmental foot-shank coordination, range of motion of the ankle, maximal power of the knee, and the ankle. Lower-limb coordination was modified with age, particularly the coordination between foot, and shank. Such modifications may influence the ankle motion and thus, ankle power. This observation may explain the decrease in the ankle plantar flexor strength mainly reported in the literature. We therefore hypothesize that this modification of coordination constitutes a neuromuscular adaptation of gait control accompanying a loss of ankle strength and amplitude by increasing the knee power in order to maintain gait efficiency. We propose that foot-shank coordination might represent a valid outcome measure to estimate the efficacy of rehabilitative strategies and to evaluate their efficiency in restoring lower-limb synergies during walking.

Dataset Information

The manifold structure of limb coordination in walking Drosophila.

Publications

The manifold structure of limb coordination in walking <i>Drosophila</i>.

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