A trade-off between kinematic and dynamic control of bimanual reaching in virtual reality

Abstract

Bimanual coordination is an essential component of human movement. Cooperative bimanual reaching tasks are widely used to assess the optimal control of goal-directed reaching. However, little is known about the neuromuscular mechanisms governing these tasks. Twelve healthy, right-handed participants performed a bimanual reaching task in a three-dimensional virtual reality environment. They controlled a shared cursor, located at the midpoint between the hands, and reached targets located at 80% of full arm extension. Following a baseline of normal reaches, we placed a wrist weight on one arm and measured the change in coordination. Relative contribution (RC) was computed as the displacement of the right hand divided by the sum of displacements of both hands. We used surface electromyography placed over the anterior deltoid and biceps brachii to compute muscle contribution (MC) from root mean squared muscle activity data. We found RC was no different than 50% during baseline, indicating participants reached equal displacements when no weights were applied. Participants systematically altered limb coordination in response to altered limb dynamics. RC increased by 0.91% and MC decreased by 5.3% relative to baseline when the weight was applied to the left arm; RC decreased by 0.94% and MC increased by 6.3% when the weight was applied to the right arm. Participants adopted an optimal control strategy that attempted to minimize both kinematic and muscular asymmetries between limbs. What emerged was a trade-off between these two parameters, and we propose this trade-off as a potential neuromuscular mechanism of cooperative bimanual reaching.NEW & NOTEWORTHY This study is the first to propose a trade-off between kinematic and dynamic control parameters governing goal-directed reaching. We propose a straightforward tool to assess this trade-off without the need for computational modeling. The technologies and techniques developed in this study are discussed in the context of upper extremity rehabilitation.

Keywords: bimanual coordination; electromyography; goal-directed reaching; optimal control; virtual reality.

Graphical abstract

Figure 1.

Experimental design. A: schematic of testing setup. Targets were located at shoulder and eye level at 80% of full arm extension. Each of the six targets appeared with equal frequency within each block. B: exemplar task sequence of within-subjects, repeated-measure design. Both experimental factors, initial limb weighting (left vs. right wrist) and load level (30% vs. 60%), were counterbalanced across blocks and days.

Figure 2.

Hand displacement (A) and deltoid muscle activity (B) throughout movement extent. Data from all 16 reaches within a block (LH weighted and RH weighted) to the midline, eye-level target were averaged for one 31-yr-old male participant who responded strongly to limb weighting. Displacement data from lap-to-target were resampled to 100 samples before averaging. RMS muscle activity values from lap-to-lap were computed using 50 nonoverlapping windows on resampled data before averaging (5000 samples/trial). Thick lines represent the mean; clouds represent SE. LH, left hand; RH, right hand; RMS, root mean square.

Figure 3.

Relative contribution and muscle contribution block-timeseries. Top: relative contribution (RC) of the right hand relative to the left during the first baseline (red), left-hand weighted (green), and right-hand weighted (blue) conditions. Each data point represents the mean and standard error of 6 consecutive trials (bins) throughout each testing block. RC did not change over time, indicating participants were not fatigued by weight application, nor did they adapt to the altered limb dynamics. However, placing the wrist weight on one arm increased the contribution of the contralateral limb. In addition, this altered coordination pattern was enhanced by increasing the mass of the wrist weight. Bottom: the change in muscle contribution (ΔMC) relative to the first baseline (red) increased in the weighted limb compared with the nonweighted limb in both the biceps brachii and anterior deltoid muscles. Like RC, ΔMC did not change over time within each block but was systematically altered by the wrist weights. For both muscle pairs, MC increased in the weighted arm compared with the nonweighted arm in a dose-response fashion, but this response was greater in the biceps compared with the deltoid. Study population comprised 12, right-handed young adults (age: 23.6 ± 4.3 yr, 5 female). LH, left hand; RH, right hand.

Figure 4.

The change in relative contribution (ΔRC) of the right hand relative to the first baseline block. Values above zero indicate an increase in the displacement of the right hand compared with the left hand. Participants increased the use of their nonweighted limb compared with their weighted limb (F_1,11 = 42.6, P = 4.3e-05, ges = 0.56). When we placed a wrist weight on the left hand, increasing the mass of the weight from 30% to 60% of arm torque increased RC of the right hand by an additional 0.8% (t_18.4= 2.5, P < 0.022, d = 0.76). Here, we show a systematic change in bimanual coordination in response to altered limb dynamics. Study population comprised 12, right-handed young adults (age: 23.6 ± 4.3 yr, 5 female). LH, left hand; RH, right hand.

Figure 5.

The change in muscle contribution of the right limb (ΔMC) relative to the left compared with the first baseline block. Values greater than zero indicate increased muscle activity in the right muscle (biceps or deltoid) compared with the left muscle. Muscle activity in the weighted limb was higher than in the nonweighted limb (F_1,8 = 143.0, P = 2.2e-06, ges = 0.53), regardless of load and muscle pair. When the wrist weight was placed on the left arm, increasing the load from 30% to 60% increased muscle activity in the left arm by an additional 5.6% (t_9.96= 2.5, P = 0.03, d = 0.79). Here, we show that placing a wrist weight on one arm produces an asymmetry in activity in the muscles controlling the upper extremities. Study population comprised 12, right-handed young adults (age: 23.6 ± 4.3 yr, 5 female). LH, left hand; RH, right hand.

Figure 6.

The average change in relative contribution and the average change in muscle contribution is plotted for each participant in both the LH weighted and RH weighted blocks. Each participant contributes two points, which are connected by a solid black line. The average of slopes for the bicep (top) was −0.13 (95% CI: [−0.24, −0.02]), and the average of slopes for the deltoid (bottom) was −0.35 (95% CI: [−0.88, −0.03]). These negative slopes and the clustering of LH weighted points in the 2nd quadrant and RH weighted points in the 4th quadrant indicate that a tradeoff emerges between kinematic and dynamic control of reaching during our shared cursor task. Study population comprised 12, right-handed young adults (age: 23.6 ± 4.3 yr, 5 female). LH, left hand; RH, right hand.