Do Visual and Vestibular Inputs Compensate for Somatosensory Loss in the Perception of Spatial Orientation? Insights from a Deafferented Patient

Abstract

The present study aimed at investigating the consequences of a massive loss of somatosensory inputs on the perception of spatial orientation. The occurrence of possible compensatory processes for external (i.e., object) orientation perception and self-orientation perception was examined by manipulating visual and/or vestibular cues. To that aim, we compared perceptual responses of a deafferented patient (GL) with respect to age-matched Controls in two tasks involving gravity-related judgments. In the first task, subjects had to align a visual rod with the gravitational vertical (i.e., Subjective Visual Vertical: SVV) when facing a tilted visual frame in a classic Rod-and-Frame Test. In the second task, subjects had to report whether they felt tilted when facing different visuo-postural conditions which consisted in very slow pitch tilts of the body and/or visual surroundings away from vertical. Results showed that, much more than Controls, the deafferented patient was fully dependent on spatial cues issued from the visual frame when judging the SVV. On the other hand, the deafferented patient did not rely at all on visual cues for self-tilt detection. Moreover, the patient never reported any sensation of tilt up to 18° contrary to Controls, hence showing that she did not rely on vestibular (i.e., otoliths) signals for the detection of very slow body tilts either. Overall, this study demonstrates that a massive somatosensory deficit substantially impairs the perception of spatial orientation, and that the use of the remaining sensory inputs available to a deafferented patient differs regarding whether the judgment concerns external vs. self-orientation.

Keywords: body tilt; deafferented patient; multisensory integration; spatial orientation.

Figure 1

(A) Illustration of the portable rod-and-frame apparatus (RFT) replicated from Oltman (1968). (B) The tilting chair and the visual scene projected in the Head-Mounted Display. (C) Experimental conditions manipulated in the self-tilt detection session. Sbwd: backward rotation of the visual scene (top toward the subject) without body rotation; Bfwd: forward rotation of the body without any visual scene; BfwdS: forward body rotation with a visual scene remaining static relative to the subject; BfwdSbwd: forward body rotation with backward visual scene rotation relative to the subject.

Figure 2

Representative psychometric function defined for a Control subject in a typical trial (e.g., Bfwd condition). A non-linear regression (Probit) was applied to the raw judgments to define a threshold for self-tilt detection.

Figure 3

(A) SVV settings as a function of frame tilt in the RFT session for Controls. Each symbol represents a given subject. While SVV classic sinusoidal modulations as a function of frame tilt magnitude were observed for Controls (y = −0.0003x³ − 0.0006x² + 0.62x − 0.08; R² = 0.99), SVV estimates corresponded ~100% to the frame orientation for the deafferented patient (y = 0.98x + 0.52; R² = 1.00). (B) Mean RFT scores obtained for Controls and the deafferented patient GL. Since 0° score corresponds to extreme visual field independence and 18° score corresponds to extreme visual field dependence, this figure shows that the deafferented patient is entirely field dependent according to RFT classification. Error bars for Controls data represent 95% confidence interval. ^***p < 0.001.

Figure 4

Mean self-tilt detection thresholds as a function of experimental conditions for controls. The deafferented patient never felt any tilt up to the largest tilt angle (dashed line) across the different trials in all the conditions she was exposed to. Error bars represent 95% confidence intervals. ^*p < 0.05.