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Sensory Agreement Guides Kinetic Energy Optimization of Arm Movements during Object Manipulation.

ABSTRACT: The laws of physics establish the energetic efficiency of our movements. In some cases, like locomotion, the mechanics of the body dominate in determining the energetically optimal course of action. In other tasks, such as manipulation, energetic costs depend critically upon the variable properties of objects in the environment. Can the brain identify and follow energy-optimal motions when these motions require moving along unfamiliar trajectories? What feedback information is required for such optimal behavior to occur? To answer these questions, we asked participants to move their dominant hand between different positions while holding a virtual mechanical system with complex dynamics (a planar double pendulum). In this task, trajectories of minimum kinetic energy were along curvilinear paths. Our findings demonstrate that participants were capable of finding the energy-optimal paths, but only when provided with veridical visual and haptic information pertaining to the object, lacking which the trajectories were executed along rectilinear paths.

SUBMITTER: Farshchiansadegh A

PROVIDER: S-EPMC4818082 | biostudies-literature | 2016 Apr

REPOSITORIES: biostudies-literature

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Sensory Agreement Guides Kinetic Energy Optimization of Arm Movements during Object Manipulation.

Farshchiansadegh Ali A Melendez-Calderon Alejandro A Ranganathan Rajiv R Murphey Todd D TD Mussa-Ivaldi Ferdinando A FA

PLoS computational biology 20160401 4

The laws of physics establish the energetic efficiency of our movements. In some cases, like locomotion, the mechanics of the body dominate in determining the energetically optimal course of action. In other tasks, such as manipulation, energetic costs depend critically upon the variable properties of objects in the environment. Can the brain identify and follow energy-optimal motions when these motions require moving along unfamiliar trajectories? What feedback information is required for such ...[more]

PMID: 27035587

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Project description:During manipulation, object slipping is prevented by modulating the grip force (GF) in synchrony with motion-related inertial forces, i.e., load force (LF). However, due to conduction delays of the sensory system, GF must be modulated in advance based on predictions of LF changes. It has been proposed that such predictive force control relies on internal representations, i.e., internal models, of the relation between the dynamic of the environment and movement kinematics. Somatosensory and visual feedback plays a primary role in building these internal representations. For instance, it has been shown that manipulation-dependent somatosensory signals contribute to building internal representations of gravity in normal and altered gravitational contexts. Furthermore, delaying the timing of visual feedback of object displacement has been shown to affect GF. Here, we explored whether and the extent to which spatial features of visual feedback movement, such as motion direction, may contribute to GF control. If this were the case, a spatial mismatch between actual (somatosensory) and visual feedback of object motion would elicit changes in GF modulation. We tested this hypothesis by asking participants to generate vertical object movements while visual feedback of object position was congruent (0° rotation) or incongruent (180° or 90°) with the actual object displacement. The role of vision on GF control was quantified by the temporal shift of GF modulation as a function of visual feedback orientation and actual object motion direction. GF control was affected by visual feedback when this was incongruent in the vertical (180°), but not horizontal dimension. Importantly, 180° visual feedback rotation delayed and anticipated GF modulation during upward and downward actual movements, respectively. Our findings suggest that during manipulation, spatial features of visual feedback motion are used to predict upcoming LF changes. Furthermore, the present study provides evidence that an internal model of gravity contributes to GF control by influencing sensory reweighting processes during object manipulation.

Project description:We explored in 75 s long trials the effects of visually induced self-rotation and displacement (SR&D) on the horizontally extended right arm of standing subjects (N = 12). A "tool condition" was included in which subjects held a long rod. The extent of arm movement was contingent on whether the arm was extended out Freely or Pointing at a briefly proprioceptively specified target position. The results were nearly identical when subjects held the rod. Subjects in the Free conditions showed significant unintentional arm deviations, averaging 55° in the direction opposite the induced illusory self-motion. Deviations in the Pointing conditions were on average a fifth of those in the Free condition. Deviations of head and torso positions also occurred in all conditions. Total arm and head deviations were the sum of deviations of the arm and head with respect to the torso and deviations of the torso with respect to space. Pointing subjects were able to detect and correct for arm and head deviations with respect to the torso but not for the arm and head deviations with respect to space due to deviations of the torso. In all conditions, arm, head, and torso deviations began before subjects experienced SR&D. We relate our findings to being an extension of the manual following response (MFR) mechanism to influence passive arm control and arm target maintenance as well. Visual-vestibular convergence at vestibular nuclei cells and multiple cortical movement related areas can explain our results, MFR results, and classical Pass Pointing. We distinguish two Phases in the induction of SR&D. In Phase 1, the visual stimulation period prior to SR&D onset, the arm, head, and torso deviations are first apparent, circa < 1 s after stimulus begins. They are augmented at the onset of Phase 2 that starts when SR&D is first sensed. In Phase 2, reaching movements first show curved paths that are compensatory for the Coriolis forces that would be generated on the reaching arm were subjects actually physically rotating. These movement deviations are in the opposite direction to the MFR and the arm, head, and torso deviations reported here. Our results have implications for vehicle control in environments that can induce illusory self motion and displacement.

Dataset Information

Sensory Agreement Guides Kinetic Energy Optimization of Arm Movements during Object Manipulation.

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Sensory Agreement Guides Kinetic Energy Optimization of Arm Movements during Object Manipulation.

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