Perturbing reach elicits anticipatory responses in transport and grasp

Abstract

Introduction: The purpose of this study was to investigate whether the anticipation of a mechanical perturbation applied to the arm during a reach-to-grasp movement elicits anticipatory adjustments in the reach and grasp components. Additionally, we aimed to evaluate whether anticipatory adjustments in the upper limb might be global or specific to the direction of the perturbation.

Methods: Thirteen healthy participants performed reach-to-grasp with perturbations randomly applied to their dominant limb. Participants were presented with three types of trials: unperturbed (control), trials perturbed in a predictable manner (either Up or Down), or perturbed in a partially predictable manner (knowledge about the perturbation but not its specific direction). EMG activity of 16 muscles, as well as the kinematics of wrist, thumb, and index finger, were acquired and analyzed.

Results and discussion: When the perturbation was expected, EMG activity of the triceps and pectoralis major muscles significantly increased about 50 - 200 ms before the perturbation onset. Peak acceleration of the reach was significantly higher and occurred earlier relative to control trials. Similar adjustments were observed in the grasp kinematics, reflected as significantly shorter time to peak aperture velocity and acceleration, as well as in increased activity of flexor and extensor digitorum 100-200 ms before perturbation onset. In summary, our data demonstrate that knowledge of an upcoming perturbation of reach during reach-to-grasp action triggers anticipatory adjustments not only in the muscles controlling the reach component, but also in those controlling grasp. Furthermore, our data revealed that the preparatory activations were generalized, rather than direction specific.

Keywords: anticipatory adjustments; feedforward control; perturbation; prehension; reach and grasp coordination.

FIGURE 1

Experimental setup (A), and schematic representation of the experimental conditions (B). B1: “NON-PERTURB” cues indicated the absence of any perturbation. B2: Full information that indicated both the presence, and the direction, of the perturbation. B3: Partial information indicating that there would be a perturbation without specifying the direction. The perturbation component vectors are indicated as gray (when direction was unknown) or colored arrows (when the direction was provided, blue indicates perturbation up and yellow perturbation down). The actual force vector was a resultant vector in either the upward-back or downward-back diagonals.

FIGURE 2

Experimental design. UD, unpredictable direction, PD, predictable direction.

FIGURE 3

Schematic representation of the order of events and timing of three phases (in blue): up to –200 ms before movement onset—Movement Preparation phase (MP), between movement onset and perturbation - Anticipatory Postural Adjustments phase (APA), and up to 200 ms after perturbation - Compensatory Postural Adjustments phase (CPA). Numbers from 1 to 4 indicate the 50 ms epochs in which integrated muscle activity was calculated. For example, APA4 indicates that the iEMG was calculated in last 50ms (150–200 ms) before the onset of the perturbation. RT, reaction time; MT, movement time.

FIGURE 4

Mean trajectories of transport (wrist marker) across participants are shown under unperturbed conditions (control) as well as under mechanical perturbation with predictable and unpredictable directions. The circle marker indicates the moment in the movement when the perturbation was applied. UD, unpredictable direction; PD, predictable direction.

FIGURE 5

Mean peaks and time to peaks for aperture velocity, aperture acceleration and transport acceleration. Standard deviations showed as error bars. Significant differences between control and perturbed conditions were marked as *. Significant differences between directions of perturbations were marked as #.

FIGURE 6

The heatmaps show mean iEMG across all participants in 50 ms time epochs (see Methods) in muscles associated with transport (panel A) and grasp (panel B) components. Each heatmap was normalized to maximum iEMG across all experimental conditions within a given muscle, therefore 1 indicate maximum, and 0 minimum iEMG of a given muscle (yellow and blue color on heatmap, respectively). For example, the activity of EDC muscle (panel B) was the smallest in MP1 phase in all experimental conditions, and the highest in CPA2 phase in PD-down condition. MO, movement onset; P, perturbation; MP, movement preparation; APA, anticipatory postural adjustments; CPA, compensatory postural adjustments.

FIGURE 7

The mean EMG traces across all participants for the triceps brachii (TB), pectoralis major (PEC), flexor digitorum superficialis (FDS), extensor digitorum communis (EDC). The black solid line corresponds to the control condition, whereas the colored lines represent perturbed conditions. MO, movement onset; P, perturbation; UD, unpredictable direction; PD, predictable direction.