Asymmetry of visuo-vestibular mechanisms contributes to reversal of optokinetic after-nystagmus

Abstract

When the visual background is moving while subject fixate a visual target, optokinetic eye movements (OKN) are suppressed and the after response, called optokinetic after nystagmus (OKAN), occurring at the stimuli offset is often inverted as compared to the situation when the OKN movements are allowed. In this study, we investigated whether this reversal of OKAN results from a perceptual or extra-retinal feedback in relation with the pursuit system and/or the vestibular indirect system. Optokinesis performance was studied in normal subjects in four experiments always using the same background motion (1) to characterize the OKN and OKAN performance elicited by the whole visual field motion while fixating or not a central visual target, (2) to investigate the 3D characteristics of the OKAN reversal by using different orientations of the visual stimulation, (3) to correlate the occurrence of an inverted OKAN with functional asymmetry of the visuo-vestibular system, by studying the effects of ocular fixation deviations and finally (4) to examine the effects of the depth plane of gaze fixation on the OKAN characteristics. In Experiments 1 and 2, we observed that the visual fixation during full-field motion induced either a dumping effect or an inversion of the OKAN response that could occur in the different planes of eye movements. The time constant was significantly increased in the inverted after-responses as compared to the not inverted ones. In Experiment 3, we found that the occurrence of an OKAN reversal after eye movement inhibition was significantly related to the presence of right/left asymmetrical OKAN responses. Moreover, the OKAN time constant was strikingly dependent on the eye fixation position during the visual stimulation and this time constant/eye position relation diverged between OKAN responses with and without inversion. Finally, Experiment 4 showed that the OKAN inversion tended to disappear when the visual target to fixate was in the near space as compared to the far space included in the background. These results argue in favor of an extraretinal influence in relation to the dynamics of the vestibulo-motor system, rather than for a perceptual influence on the inverted OKAN mechanisms. More precisely, we postulate that the reversal of OKAN could be linked to an inhibition issued from pursuit signals combined with an asymmetrical activity in the VSM vestibular complex.