Inter-limb interference during bimanual adaptation to dynamic environments

Abstract

Skillful manipulation of objects often requires the spatio-temporal coordination of both hands and, at the same time, the compensation of environmental forces. In bimanual coordination, movements of the two hands may be coupled because each hand needs to compensate the forces generated by the other hand or by an object operated by both hands (dynamic coupling), or because the two hands share the same workspace (spatial coupling). We examined how spatial coupling influences bimanual coordination, by looking at the adaptation of velocity-dependent force fields during a task in which the two hands simultaneously perform center-out reaching movements with the same initial position and the same targets, equally spaced on a circle. Subjects were randomly allocated to two groups, which differed in terms of the force fields they were exposed to: in one group (CW-CW), force fields had equal clockwise orientations in both hands; in the other group (CCW-CW), they had opposite orientations. In both groups, in randomly selected trials (catch trials) of the adaptation phase, the force fields were unexpectedly removed. Adaptation was quantified in terms of the changes of directional error for both hand trajectories. Bimanual coordination was quantified in terms of inter-limb longitudinal and sideways displacements, in force field and in catch trials. Experimental results indicate that both arms could simultaneously adapt to the two force fields. However, in the CCW-CW group, adaptation was incomplete for the movements from the central position to the more distant targets with respect to the body. In addition, in this group the left hand systematically leads in the movements toward targets on the left of the starting position, whereas the right hand leads in the movements to targets on the right. We show that these effects are due to a gradual sideways shift of the hands, so that during movements the left hand tends to consistently remain at the left of the right hand. These findings can be interpreted in terms of a neural mechanism of bimanual coordination/interaction, triggered by the force field adaptation process but largely independent from it, which opposes movements that may lead to the crossing of the hands. In conclusion, our results reveal a concurrent interplay of two task-dependent modules of motor-cognitive processing: an adaptive control module and a 'protective' module that opposes potentially 'dangerous' (or cognitively costly) bimanual interactions.

Figures

Figure 1

Two views of the experimental set-up (top panel) and layout of the eight targets (2 cm in diameter), equally spaced on a circle (20 cm in diameter). In the data analysis subset of targets are considered: ‘right’ subset (T1, T2, T8), ‘left’ subset (T4, T5, T6), ‘proximal’ subset (T6, T7, T8), ‘distal’ subset (T2, T3, T4).

Figure 2

Movement trajectories at the beginning (left) and end (right) of the force field adaptation phase, for two subjects, one in the CW-CW group (S6) and one in the CCW-CW group (S11). Lines in grey and black denote, respectively, the left and right hand. Scale bar: 2 cm.

Figure 3

A, B: Evolution of the directional error for the left (A) and right (B) hand for two subjects, one in the CW-CW group (S6, black line) and one in the CCW-CW group (S11, grey line). Positive directions denote counter-clockwise deviations. Dashed lines indicate catch trials, solid lines indicate force field trials. C, D: Learning indexes for each subjects in the two groups (CW-CW: black; CCW-CW: grey), for the left (C) and right hand (D). Error bars indicate ± SE.

Figure 4

Polar plots of the directional error (average over subjects), as a function of the movement direction, for both hands (left, right) and both groups (CW-CW: black lines; CCW-CW: gray lines). The circle corresponds to null directional error. Positive errors are plotted outside the circle and correspond to counter-clockwise deviations. The radius of the circle is equivalent to a deviation of 20 deg. In the familiarization phase, the errors shown are absolute. In the other phases, the errors at the end of the familiarization phase have been subtracted from the total errors (see text).

Figure 5

Comparison among movements to ‘proximal’ targets (black) and ‘distal’ targets (grey) during the adaptation phase (average over all subjects). A: forward (center-out) movements; B: backward (return) movements. Error bars indicate ± SE. C, D: temporal evolution of the directional errors (CCW-CW group) in the left (C) and right hand (D). Dashed lines indicate catch trials, solid lines indicate force field trials.

Figure 6

A, B: Evolution of the inter-limb sideways displacement over epochs, for the CW-CW group (A) and CCW-CW group (B), averaged over all target directions. C, D: the different behavior of movements to ‘proximal’ targets (black lines) or ‘distal’ targets (grey lines). Catch trials are indicated by dashed lines.

Figure 7

Analysis of longitudinal inter-limb coordination. A, B, C (top): Polar plots of the longitudinal distance between hands, as a function of the movement direction, for familiarization (A), adaptation (B) and wash-out phases (C). Black and grey lines indicate, respectively, the CW-CW and the CCW-CW groups. The circle (radius: 2 cm) indicates zero longitudinal displacement. The points outside the circle denote positive displacement (i.e. the right hand leads the left hand). D, E (middle): Evolution over epochs of the longitudinal distance between hands, for the CW-CW (D) and the CCW-CW group (E), for targets in the left hemi-space (grey lines) and the right hemi-space (black lines). F, G (bottom): time course of the hand speed and the longitudinal component of the inter-hand hand distance at the end of the adaptation phase, for a movement to target T5 (LEFT) or to target T1 (RIGHT), for a representative subject of the CW-CW group (F) and a representative subject of the CCW-CW group (G). Left hand: grey lines; right hand: black lines; dashed lines: catch trials.