Human manual control precision depends on vestibular sensory precision and gravitational magnitude

Abstract

Precise motion control is critical to human survival on Earth and in space. Motion sensation is inherently imprecise, and the functional implications of this imprecision are not well understood. We studied a "vestibular" manual control task in which subjects attempted to keep themselves upright with a rotational hand controller (i.e., joystick) to null out pseudorandom, roll-tilt motion disturbances of their chair in the dark. Our first objective was to study the relationship between intersubject differences in manual control performance and sensory precision, determined by measuring vestibular perceptual thresholds. Our second objective was to examine the influence of altered gravity on manual control performance. Subjects performed the manual control task while supine during short-radius centrifugation, with roll tilts occurring relative to centripetal accelerations of 0.5, 1.0, and 1.33 G_C (1 G_C = 9.81 m/s²). Roll-tilt vestibular precision was quantified with roll-tilt vestibular direction-recognition perceptual thresholds, the minimum movement that one can reliably distinguish as leftward vs. rightward. A significant intersubject correlation was found between manual control performance (defined as the standard deviation of chair tilt) and thresholds, consistent with sensory imprecision negatively affecting functional precision. Furthermore, compared with 1.0 G_C manual control was more precise in 1.33 G_C (-18.3%, P = 0.005) and less precise in 0.5 G_C (+39.6%, P < 0.001). The decrement in manual control performance observed in 0.5 G_C and in subjects with high thresholds suggests potential risk factors for piloting and locomotion, both on Earth and during human exploration missions to the moon (0.16 G) and Mars (0.38 G). NEW & NOTEWORTHY The functional implications of imprecise motion sensation are not well understood. We found a significant correlation between subjects' vestibular perceptual thresholds and performance in a manual control task (using a joystick to keep their chair upright), consistent with sensory imprecision negatively affecting functional precision. Furthermore, using an altered-gravity centrifuge configuration, we found that manual control precision was improved in "hypergravity" and degraded in "hypogravity." These results have potential relevance for postural control, aviation, and spaceflight.

Keywords: human; manual control; otoliths; psychophysics; semicircular canals; thresholds; vestibular perceptual threshold.

Fig. 1.

Diagram of the experimental setup, with the chair positioned such that the subject’s head is 0.68 m from the center of rotation, the joystick is mounted in front of the subject’s chest, and the roll-tilt axis is centered at the level of the subject’s vestibular system. GIF, gravitoinertial force.

Fig. 2.

A: pseudorandom sum-of-sines roll-tilt disturbance profile (gray) and centrifuge chair position (black) for 1 trial of 1 subject. B: subject joystick deflection angle used for controlling chair orientation in a rate-control-attitude mode. The dynamics of subject inputs to the joystick were similar to those recently reported (Vimal et al. 2016).

Fig. 3.

Characterization of an example motion for a 0.2-Hz roll-tilt stimulus in the threshold task. A, acceleration; f, frequency; T, period.

Fig. 4.

Manual control position variability metric as a function of threshold for each subject in 0.5 G_C (centripetal acceleration), 1.0 G_C, and 1.33 G_C. Individual subjects are displayed with unique symbols.

Fig. 5.

A: manual control position variability metric (PVM) in 1.0 G_C (centripetal acceleration) and 1.33 G_C (subexperiment 1). Individual subjects are displayed in gray with unique symbols corresponding to Fig. 4. The intersubject mean is plotted in black, with error bars indicating 95% confidence intervals. B: manual control PVM in 1.0 G_C and 0.5 G_C (subexperiment 2).