The influence of target sensory modality on motor planning may reflect errors in sensori-motor transformations

Abstract

Multi-sensory integration studies have shown that combining heterogeneous signals can optimize motor performance by reducing errors inherent to any single modality. However, it has also been suggested that errors could arise from erroneous transformations between heterogeneous coordinate systems. Here we investigated the effect of visuo-proprioceptive integration on the control of multi-joint arm movements by manipulating target modality. When the target was visual, movement control required the integration of visual target signals with proprioceptive signals about limb configuration. In contrast, when the target was the unseen fingertip, movement control relied solely on proprioceptive signals since visual feedback of hand position was precluded. We hypothesized that a faulty integration of visual target signals with proprioceptive arm signals would result in a less accurate planning of visually-targeted movements with respect to proprioceptively-targeted movements. Different inter-joint coordinations patterns were tested by varying starting hand position. Results showed larger initial trajectory deviations from target direction for visually-targeted movements involving substantial shoulder and elbow motions. Inverse dynamic analysis revealed that these deviations were associated with less efficient intersegmental coordination. The control of visually-targeted movements thus appeared sub-optimal compared to proprioceptively-targeted movements when considering theoretical models of motor planning assuming kinematic or dynamic optimizations. Additional experiments further highlighted the effect of target position, and visual feedback of starting hand position, on motor planning for proprioceptively- and visually-targeted movements. Our findings suggest that the integration of heterogeneous sensory signals related to hand and target positions introduces errors in motor planning.

Figure 1

(A) Experimental set-up. (B) Target position was constant while starting hand position varied. Part of the projection screen is omitted here for illustration. Subjects could not see their arm. Subjects could only see the target and the starting position in visual target conditions. Visual feedback of the moving limb was not available.

Figure 2

(A) Top view of representative unseen arm movements toward the proprioceptive and visual target from two starting positions, for the same subject. Although target position remained constant throughout the experiment, movements from the two starting positions are presented in two distinct panels for the sake of clarity (B) Bar plot of averaged initial movement direction (with respect to target direction) as a function of experimental conditions. Negative values represent counterclockwise deviations. Error bars represent standard errors. The asterisk indicates a significant difference at post-hoc analysis.

Figure 3

Kinematic and dynamic differences of movements from distinct starting positions (A) Bar plot of elbow excursion. (B) Bar plot of shoulder excursion, which was greater for movements starting from start position 2. (C) Bar plot of interaction torque, which was greater for movements starting from start position 2 (F_{1, 6}=48.0; P<0.001).

Figure 4

Arm movements made from starting position 2. (A) Representative hand paths. (B) Representative joint displacements profiles corresponding to the hand path shown in A. (C) Corresponding shoulder joint torque patterns. (D) Corresponding elbow joint torque patterns: in the left panel, net torque and interaction torques are almost undistinguishable from movement onset to peak acceleration.

Figure 5

(A) Bar plot of the time course of the elbow extension to shoulder flexion ratio. Error bars represent standard errors. (B) Visually- and proprioceptively-targeted movements in joint space. (C) Bar plot of the peak elbow muscle torque between movement onset and peak acceleration. Error bars represent standard errors. Elbow muscle torque contributes to elbow flexion when reaching for the visual target, while the task requires elbow extension. The asterisk indicates a significant difference at post-hoc analysis.

Figure 6

(A) Top view of representative unseen arm movements toward the visual targets. (B) Top view of representative unseen arm movements toward the proprioceptive targets. (C) Averaged initial movement direction’s variability as a function of experimental conditions.