Rapid Visuomotor Corrective Responses during Transport of Hand-Held Objects Incorporate Novel Object Dynamics

Abstract

Numerous studies have shown that people are adept at learning novel object dynamics, linking applied force and motion, when performing reaching movements with hand-held objects. Here we investigated whether the control of rapid corrective arm responses, elicited in response to visual perturbations, has access to such newly acquired knowledge of object dynamics. Participants first learned to make reaching movements while grasping an object subjected to complex load forces that depended on the distance and angle of the hand from the start position. During a subsequent test phase, we examined grip and load force coordination during corrective arm movements elicited (within ∼150 ms) in response to viewed sudden lateral shifts (1.5 cm) in target or object position. We hypothesized that, if knowledge of object dynamics is incorporated in the control of the corrective responses, grip force changes would anticipate the unusual load force changes associated with the corrective arm movements so as to support grasp stability. Indeed, we found that the participants generated grip force adjustments tightly coupled, both spatially and temporally, to the load force changes associated with the arm movement corrections. We submit that recently learned novel object dynamics are effectively integrated into sensorimotor control policies that support rapid visually driven arm corrective actions during transport of hand held objects. Significance statement: Previous studies have demonstrated that the motor system can learn, and make use of, internal models of object dynamics to generate feedforward motor commands. However, it is not known whether such internal models are incorporated into rapid, automatic arm movement corrections that compensate for errors that arise during movement. Here we demonstrate, for the first time, that internal models of novel object dynamics are integrated into rapid corrective arm movements made in response to visuomotor perturbations that, importantly, do not directly perturb the object.

Keywords: internal model; motor learning; object manipulation; reaching; visuomotor control.

Figure 1.

Apparatus and experimental design. A, Drawing of the experimental setup (for details, see text). B, Configuration of the start position, occluder, and the 10 training targets. Red force vectors, within the red shaded region, indicate the position-dependent force field applied to the grasped object. C, Configuration for the experimental trials with targets at −10° and 5° and the same force field as shown in B (illustrated with fewer red arrows). Shown only for the 5° target, but also present for the −10° target, are the cursor jumps (filled colored circles) and target jumps (open colored circles). Red and blue circles represent perturbations requiring a rightward and leftward movement response, respectively. D, Average object paths toward the 10 training targets for a single participant, with trajectories aligned to the time at which the cursor emerged from the occluder. Shaded regions represent ±1 SD orthogonal to the target direction. E, F, Average object paths for each target and perturbation type for the same participant as in D. Red and blue traces represent perturbation trials requiring a rightward and leftward movement, respectively. Gray traces represent unperturbed trials (with the same unperturbed trials shown in E and F. G, Procedure for calculating arm movement response latency, relative to the time of the perturbation (t = 0), illustrated for a single participant and target jumps involving the 10° target. We first determined when the p value from a running t test comparing the average object velocity perpendicular to the vector from the start position to the target for right (red trace) and left (blue trace) target jumps dropped <0.001 (vertical gray dash-dotted line), and then backtracked to the first minima in the rate of change of the p value (vertical black dashed line) .

Figure 2.

Object velocity profiles for each target and perturbation type for a single participant. A–D, Average perpendicular velocity profiles, with trials aligned in time to the perturbation (t = 0), for unperturbed trials (gray) and perturbed trials requiring a leftward (blue) or rightward (red) correction. Positive indicates rightward relative to the movement direction. Dashed blue, red, and gray vertical lines indicate the times at which the blue and gray, red and gray, and blue and red velocity profiles differed, respectively (see Materials and Methods), with these times included as color-coded text. Solid blue, red, and gray vertical lines indicate the mean times the participant reached the target for each trial type. B, Dash-dotted red and blue vertical lines indicate, for perturbations requiring right and left responses, respectively, the difference between the peak average velocity in perturbation trials and the average velocity in unperturbed trials. Before averaging, profiles were aligned to perturbation onset, or the corresponding time in unperturbed trials (dash-dotted lines). The heights of the shaded regions represent ±1 SD. E–H, Corresponding plots for velocity in the same direction as the vector connecting the start position and target.

Figure 3.

Grip and load force profiles for each target and perturbation type for a single participant. A–D, Average grip force profiles for unperturbed trials (gray) and perturbed trials requiring a leftward (blue) or rightward (red) correction. Dashed blue, red, and gray vertical lines, shown for the right target only, indicate the response latencies obtained by comparing the leftward and baseline, rightward and baseline, and leftward and rightward responses, respectively. Solid blue, red, and gray vertical lines indicate the mean times the participant reached the target for each trial type. Before averaging, profiles were aligned to perturbation onset, or the corresponding time in unperturbed trials (t = 0). The heights of the shaded regions represent ±1 SD. E–H, Corresponding plots for load force.

Figure 4.

Grip force and movement response latencies. A–C, Average response latencies, based on participant means, for grip force, load force, and perpendicular velocity for trials involving the right target. Colored bars represent the three latency measures calculated by comparing leftward response and unperturbed trials (blue), rightward and leftward response trials (gray), and rightward response and unperturbed trials (red). Error bars indicate ±1 SE. C, Circles represent the movement response latencies for the left target. D, Grip force response latency versus movement response latency, where the latter was computed from the average of the load force and perpendicular velocity latencies. Each circle represents a single participant, and all three latencies are based on averaging the three latency measures. Open and filled circles represent latencies for the cursor and target jump trials, respectively. Dashed line indicates the unity line. Solid line indicates the regression slope computed using all points.

Figure 5.

Coordination of grip and load force. A, B, Average grip force (GF) plotted against average load force (LF) for movements to the right target involving either cursor (A) or target (B) jumps. Average force based on participant means. Blue and red traces represent trials requiring rightward and leftward movement corrections, respectively. Gray traces represent unperturbed trials. Open squares represent the average point at which the perturbation occurred. Open circles represent the average point at which participants reached the target. C, D, Grip and load forces, averaged over the 50 ms before reaching the target, as a function of the arc length of the target position relative to −5°. Each circle represented an average based on participant means. Blue and red circles represent perturbation trials requiring leftward and rightward responses, respectively. Gray circles represent unperturbed trials. Black circles represent training trials. Error bars indicate ±1 SE.