Dataset Information

The energetic basis for smooth human arm movements.

ABSTRACT: The central nervous system plans human reaching movements with stereotypically smooth kinematic trajectories and fairly consistent durations. Smoothness seems to be explained by accuracy as a primary movement objective, whereas duration seems to economize energy expenditure. But the current understanding of energy expenditure does not explain smoothness, so that two aspects of the same movement are governed by seemingly incompatible objectives. Here, we show that smoothness is actually economical, because humans expend more metabolic energy for jerkier motions. The proposed mechanism is an underappreciated cost proportional to the rate of muscle force production, for calcium transport to activate muscle. We experimentally tested that energy cost in humans (N = 10) performing bimanual reaches cyclically. The empirical cost was then demonstrated to predict smooth, discrete reaches, previously attributed to accuracy alone. A mechanistic, physiologically measurable, energy cost may therefore explain both smoothness and duration in terms of economy, and help resolve motor redundancy in reaching movements.

SUBMITTER: Wong JD

PROVIDER: S-EPMC8741215 | biostudies-literature | 2021 Dec

REPOSITORIES: biostudies-literature

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The energetic basis for smooth human arm movements.

Wong Jeremy D JD Cluff Tyler T Kuo Arthur D AD

eLife 20211220

The central nervous system plans human reaching movements with stereotypically smooth kinematic trajectories and fairly consistent durations. Smoothness seems to be explained by accuracy as a primary movement objective, whereas duration seems to economize energy expenditure. But the current understanding of energy expenditure does not explain smoothness, so that two aspects of the same movement are governed by seemingly incompatible objectives. Here, we show that smoothness is actually economica ...[more]

PMID: 34927584

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Project description:Human movement is generated by a dynamic interplay between the nervous system, the biomechanical structures, and the environment. To investigate this interaction, we propose a neuro-musculoskeletal model of human goal-directed arm movements. Using this model, we simulated static perturbations of the inertia and damping properties of the arm, as well as dynamic torque perturbations for one-degree-of freedom movements around the elbow joint. The controller consists of a feed-forward motor command and feedback based on muscle fiber length and contraction velocity representing short-latency (25 ms) or long-latency (50 ms) stretch reflexes as the first neuronal responses elicited by an external perturbation. To determine the open-loop control signal, we parameterized the control signal resulting in a piecewise constant stimulation over time for each muscle. Interestingly, such an intermittent open-loop signal results in a smooth movement that is close to experimental observations. So, our model can generate the unperturbed point-to-point movement solely by the feed-forward command. The feedback only contributed to the stimulation in perturbed movements. We found that the relative contribution of this feedback is small compared to the feed-forward control and that the characteristics of the musculoskeletal system create an immediate and beneficial reaction to the investigated perturbations. The novelty of these findings is (1) the reproduction of static as well as dynamic perturbation experiments in one neuro-musculoskeletal model with only one set of basic parameters. This allows to investigate the model's neuro-muscular response to the perturbations that-at least to some degree-represent stereotypical interactions with the environment; (2) the demonstration that in feed-forward driven movements the muscle characteristics generate a mechanical response with zero-time delay which helps to compensate for the perturbations; (3) that this model provides enough biomechanical detail to allow for the prediction of internal forces, including joint loads and muscle-bone contact forces which are relevant in ergonomics and for the development of assistive devices but cannot be observed in experiments.

Project description:Smooth pursuit eye movements (pursuit) are used to minimize the retinal motion of moving objects. During pursuit, the pattern of motion on the retina carries not only information about the object movement but also reafferent information about the eye movement itself. The latter arises from the retinal flow of the stationary world in the direction opposite to the eye movement. To extract the global direction of motion of the tracked object and stationary world, the visual system needs to integrate ambiguous local motion measurements (i.e., the aperture problem). Unlike the tracked object, the stationary world's global motion is entirely determined by the eye movement and thus can be approximately derived from motor commands sent to the eye (i.e., from an efference copy). Because retinal motion opposite to the eye movement is dominant during pursuit, different motion integration mechanisms might be used for retinal motion in the same direction and opposite to pursuit. To investigate motion integration during pursuit, we tested direction discrimination of a brief change in global object motion. The global motion stimulus was a circular array of small static apertures within which one-dimensional gratings moved. We found increased coherence thresholds and a qualitatively different reflexive ocular tracking for global motion opposite to pursuit. Both effects suggest reduced sampling of motion opposite to pursuit, which results in an impaired ability to extract coherence in motion signals in the reafferent direction. We suggest that anisotropic motion integration is an adaptation to asymmetric retinal motion patterns experienced during pursuit eye movements. NEW & NOTEWORTHY This study provides a new understanding of how the visual system achieves coherent perception of an object's motion while the eyes themselves are moving. The visual system integrates local motion measurements to create a coherent percept of object motion. An analysis of perceptual judgments and reflexive eye movements to a brief change in an object's global motion confirms that the visual and oculomotor systems pick fewer samples to extract global motion opposite to the eye movement.

Dataset Information

The energetic basis for smooth human arm movements.

Publications

The energetic basis for smooth human arm movements.

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