Interaction of retinal, eye position, vestibular and neck proprioceptive information

Abstract

Perceptual updating of the location of visual targets in after intervening eye, head or trunk movements requires an interaction between several affer- ent signals (visual, oculomotor efference copy, vestibu- lar, proprioceptive). The nature of the interaction is still a matter of debate. To address this problem, we present- ed subjects (n=6) in the dark with a target (light spot) at various horizontal eccentricities (up to ±20°) relative to the initially determined subjective straight-ahead direc- tion (SSA). After a memory period of 12 s in complete darkness, the target reappeared at a random position and subjects were to reproduce its previous location in using a remote control. For both the presentation and the reproduction of the target's location, subjects either kept their gaze in the SSA (retinal viewing condition) or fix- ated the eccentric target (visuo-oculomotor). Three ex- perimental series were performed: A, visual-only se- ries: reproduction of the target's location in was found to be close to ideal, independently of viewing con- dition; estimation curves (reproduced vs presented posi- tions) showed intercepts ≈0° and slopes ≈1; B, visual- vestibular series: during the memory period, subjects were horizontally rotated to the right or left by 10° or 18° at 0.8-Hz or 0.1-Hz dominant frequency. Following the 0.8-Hz body rotation, reproduction was close to ide- al, while at 0.1 Hz it was partially shifted along with the body, in line with the known vestibular high-pass charac- teristics. Additionally, eccentricity of target presentation reduced the slopes of the estimation curves (less than 1); C, visual-vestibular-neck series: a shift toward the trunk also occurred after low-frequency neck stimulation (trunk rotated about stationary head). When vestibular and neck stimuli were combined (independent head and trunk rotations), their effects summed linearly, such that the errors cancelled each other during head rotation on the stationary trunk. Variability of responses was always lowest for targets presented at SSA, irrespective of inter- vening eye, head or trunk rotations. We conclude that: (1) subjects referenced space to pre-rotatory SSA and that the memory trace of the target's location in was not altered during the memory period; and that (2) they used internal estimates of eye, head and trunk dis- placements with respect to to match current target position with the memory trace during reproduction; these estimates would be obtained by inverting the phys- ical coordinate transformations produced by these dis- placements. We present a model which is able to de- scribe these operations and whose predictions closely parallel the experimental results. In this model the esti- mate of head rotation in is not obtained directly from the vestibular head-in-space signal, but from a ves- tibular estimate of the kinematic state of the body sup- port.