Enhanced crosslimb transfer of force-field learning for dynamics that are identical in extrinsic and joint-based coordinates for both limbs

Abstract

Humans are able to adapt their motor commands to make accurate movements in novel sensorimotor environments, such as when wielding tools that alter limb dynamics. However, it is unclear to what extent sensorimotor representations, obtained through experience with one limb, are available to the opposite, untrained limb and in which form they are available. Here, we compared crosslimb transfer of force-field compensation after participants adapted to a velocity-dependent curl field, oriented either in the sagittal or the transverse plane. Due to the mirror symmetry of the limbs, the force field had identical effects for both limbs in joint and extrinsic coordinates in the sagittal plane but conflicting joint-based effects in the transverse plane. The degree of force-field compensation exhibited by the opposite arm in probe trials immediately after initial learning was significantly greater after sagittal (26 ± 5%) than transverse plane adaptation (9 ± 4%; P < 0.001), irrespective of whether participants learned initially with the left or the right arm or via abrupt or gradual exposure to the force field. Thus transfer was impaired when the orientation of imposed dynamics conflicted in intrinsic coordinates for the two limbs. The data reveal that neural representations of novel dynamics are only partially available to the opposite limb, since transfer is incomplete even when force-field perturbation is spatially compatible for the two limbs, according to both intrinsic and extrinsic coordinates.

Keywords: coordinate frame; interlimb transfer; motor learning; sensorimotor adaptation.

Fig. 1.

Schematic illustrations of the experimental setup. A and B: transverse and sagittal plane reaching conditions, respectively. C and D: the orientation of joint torques imposed upon the left and right arms by a given curl force field defined in extrinsic coordinates for the transverse and sagittal plane-reaching conditions, respectively. The joint torques are identical for both limbs during sagittal reaching but differ for transverse reaching. E: the time course of each experiment and the composition of the various experimental phases. Force-field trials, blue; null field trials, black; channel trials, green. Only 15 of the 60 channel trials completed are shown per phase (initial learning and transfer) for clarity.

Fig. 2.

Average time-series plots of channel forces divided by peak hand speed for each trial for sagittal (A) and transverse (B) groups. Error bars show 95% confidence intervals. Trials were aligned according to the time of peak hand speed and averaged from 600 ms before to 600 ms after the time of peak speed. The blue boxes show both the time window (width) around peak hand speed used to measure force-field compensation (±70 ms) and the force magnitude (height) required to compensate perfectly the imposed field (i.e., 13 N·m⁻¹·s) at peak hand speed (i.e., ∼0.7 m/s). Thus the unit of the ordinate of each plot is the percentage of the force required to compensate the imposed field at peak hand speed. Scale is specified by the height of the blue box as 100%. The first and last block of initial learning and transfer phases is shown, as well as the probe trials conducted just before the transfer phase for the “untrained” hand. LR, left to right; RL, right to left.

Fig. 3.

Force-field compensation. Averages and 95% confidence intervals for average percentage force-field compensation at peak hand speed ±70 ms in each condition for sagittal (A) and transverse (B) plane reaching. The 3 points plotted between initial learning- and transfer-phase data show average probe-trial forces. C: average and 95% confidence intervals for percentage transfer after opposite-limb adaptation for all 6 conditions. Lines join initial learning- and transfer-phase data for each condition. D: averages and 95% confidence intervals for percentage force-field compensation produced in the first initial learning and transfer blocks for all 6 conditions. E: averages and 95% confidence intervals for percentage force-field compensation produced in the last initial learning and transfer blocks for all 6 conditions. *P < 0.05, statistically significant main effects for transfer or force-field compensation between sagittal and transverse planes of movement.

Fig. 4.

Kinematic analysis. Averages and 95% confidence intervals for peak perpendicular errors from a straight line path from the origin to the target for sagittal (A) and transverse (B) conditions.

Fig. 5.

Summary plots for kinematic errors. A: averages and 95% confidence intervals for peak perpendicular errors in the first initial learning- and transfer-phase blocks for each condition. Lines join initial learning- and transfer-phase data for each condition. B: averages and 95% confidence intervals for perpendicular error at the time of peak hand speed in the first initial learning and transfer blocks for all 6 conditions. Averages and 95% confidence intervals for peak perpendicular errors in the first (C) and last (D) blocks of the washout phases of the experiment. *P < 0.05, statistically significant main effects between sagittal and transverse planes of movement or pairwise contrasts between initial learning and transfer phase performance within a group.