The endless visuomotor calibration of reach-to-grasp actions

Abstract

It is reasonable to assume that when we grasp an object we carry out the movement based only on the currently available sensory information. Unfortunately, our senses are often prone to err. Here, we show that the visuomotor system exploits the mismatch between the predicted and sensory outcomes of the immediately preceding action (sensory prediction error) to attain a degree of robustness against the fallibility of our perceptual processes. Participants performed reach-to-grasp movements toward objects presented at eye level at various distances. Grip aperture was affected by the object distance, even though both visual feedback of the hand and haptic feedback were provided. Crucially, grip aperture as well as the trajectory of the hand were systematically influenced also by the immediately preceding action. These results are well predicted by a model that modifies an internal state of the visuomotor system by adjusting the visuomotor mapping based on the sensory prediction errors. In sum, the visuomotor system appears to be in a constant fine-tuning process which makes the generation and control of grasping movements more resistant to interferences caused by our perceptual errors.

Figure 1

Shape from stereopsis. (a) Two objects of the same size r are placed at two distances (d_N and d_F). (b) Due to wrong encoding of distance from ocular vergence, the close object is perceived farther and deeper and the far object is perceived closer and shallower. (b) A linear function of negative slope (s_d) that represents the relationship between depth estimates and object distance.

Figure 2

Distance effects on grip aperture. (a) Grip aperture (GA) as a function of the object’s distance at the current trial (dark blue lines). (b) Grip aperture (GA) as a function of the object’s distance at the previous trial (light green lines). Grasping was performed along the object’s depth axis (Experiment 1, continuous lines) or along the object’s oblique axis (Experiment 2, dashed lines). Separate panels represent the grip aperture when the hand was at different points of the movement path (the more negative values correspond to points of the movement path that are further away from the object). Error bars represent the standard error of the mean.

Figure 3

Current and previous distance effects on the grip aperture. Slope profiles representing the current distance effect (dark blue line) and the previous distance effect (light green line) on the grip aperture along the movement path when grasping along the depth axis (a) and along the oblique axis (b). The bands represent the 95% confidence interval of the slope parameters.

Figure 4

Relationship between individual current and previous distance effects on grip aperture. (a) Individual data from Experiment 1 (grasping along the object’s depth axis). (b) Individual data from Experiment 2 (grasping along the object’s oblique axis). Solid lines show the linear regression fits.

Figure 5

Previous distance effects on the hand position. Slope profiles representing the previous distance effect on the hand position along the movement path when grasping along the depth axis (a) and along the oblique axis (b). The bands represent the 95% confidence interval of the slope parameters.

Figure 6

Methods. (a) The three-dimensional structure of the stimulus can be observed by cross-fusing the two images stereoscopically. (b) Grasping along the depth axis (left image) and along the oblique axis (right image). Participants never had full vision of the hand, only visual feedback about the fingertips was provided (red dots). (c) A de Bruijn graph for n = 2 and a four-character alphabet composed of the characters A, B, C, and D which represent the four object’s distances. Following the numbered edges in order from 1 to 16 traces an Eulerian cycle AD, DD, DC, CC, CA, AB, BC, CD, DB, BB, BD, DA, AA, AC, CB, BA. By appending the first element to the tail and by taking the first character of each of these elements we obtain the de Bruijn sequence ADDCCABCDBBDAACBA without repetitions. (d) An example of a 145-long de Bruijn sequence with the repetition factor set to r = 3. Each of the two-character elements is repeated 9 times. (e) The green lines represent the thumb and index digit trajectories when grasping the sphere along the depth axis. The purple line represents the last 250 mm of the movement path of the midpoint between the fingertip positions. The values above the purple line show the distances from movement end along the path. The projection of the purple line (arrow) on the sagittal axis (dashed line) represents the hand position at a given point of the movement path. The dotted lines connect the thumb and index digit when both were at the same point of the movement path. The length of the dotted lines thus corresponds to the grip aperture.