Visual vestibular interaction: vestibulo-ocular reflex suppression with head-fixed target fixation

Abstract

In order to maintain clear vision, the images on the retina must remain reasonably stable. Head movements are generally dealt with successfully by counterrotation of the eyes induced by the combined actions of the vestibulo-ocular reflex (VOR) and the opto-kinetic reflex. We have studied how, in humans, the VOR gain (VORG) is modulated to provide appropriate eye movements in two situations: 1. fixation of a stationary object of the visual space while the head moves. This requires a visuo-vestibulo-ocular reaction to induce eye movements opposite in direction, and equal in velocity to head movements, and 2. fixation of an object moving with the head. Here, the visuo-vestibulo-ocular reaction should be totally suppressed. These two situations were compared to a basic condition in which, to induce "pure" VOR, the subjects (Ss) in darkness were not allowed a visual target. Eye movements were recorded in seated Ss during constant amplitude sinusoidal and pulse-like passive rotations applied around the vertical axis. Subjects were in total darkness (DARK condition) and performing mental arithmetic. Alternatively, they were provided with a small target, either stationary with respect to earth (earth-fixed target: EFT), or moving with them (chair-fixed-target: CFT). The sinusoidal rotation experiment was used as baseline for the ensuing experiments and yielded control data in agreement with the literature. In particular, rotation in the dark showed a VORG of 0.6. With, for example, 0.8 s passive pulse rotations, typical responses in all three visual conditions were rigorously identical during the first 150 to 180 ms. They showed a delay of about 16 ms of the eye behind the head with no significant difference between passive whole-body and passive head-alone rotations. In all conditions, once the eyes had started to move, a rapid increase in eye velocity was observed during 75 to 80 ms, after which, the average VORG was 0.9 +/- 0.15. During the following 50 to 100 ms, the gain remained around 0.9 in all three conditions. Beyond 180 ms, the VORG remained around 0.9 in DARK, increased slowly towards 1 or decreased towards zero in the EFT and CFT conditions, respectively. The time-course of these later events suggests that visual tracking mechanisms came into play to reduce retinal slip through smooth pursuit. Sinusoidal rotations, extensively used in VOR studies, do not seem to be a satisfactory stimulus to rapidly and precisely characterize VOR function, particularly in pathological cases. Our data suggest that rapid transient rotations are more appropriate.

Central ocular motor disorders, including gaze palsy and nystagmus

“…The examiner should watch for corrective saccades, which indicate a disorder of the visual fixation suppression of the VOR. If the visual fixation suppression of the VOR is intact, the eye position relative to the head position does not change, but if it is not intact (which is indicated by small corrective saccades and as a rule occurs with smooth pursuit abnormalities, as these two functions use the same neural pathways) this typically indicates lesions of the cerebellum (flocculus or paraflocculus) or of cerebellar pathways [20]. Drugs, particularly anticonvulsants, sedatives and alcohol can also impair visual fixation suppression of the VOR because of their effects on the cerebellum.…”

Interaural Translational VOR: Suppression, Enhancement, and Cognitive Control

“…These studies show that the gain of the rVOR can be enhanced in trials when the target is space-fixed and diminished in trials when the target is headfixed, but exactly how this occurs is uncertain. Johnston and Sharpe (1994) and Crane and Demer (1999) found that the rVOR gain was modifiable within the first 80 ms of the response, whereas Gauthier and Vercher (1990) found no differences between responses to head-and space-fixed targets within the first 150 ms. The timing of VOR modulation is key to understanding which mechanisms might be used by the brain to modify the response.…”

“…A rotational perturbation of the head during steady-state tracking was used to investigate short-latency suppression and enhancement of the rVOR in monkeys (Lisberger 1990). The ability to suppress and enhance the rVOR depending on the location of the target of interest relative to the head also has been investigated extensively in humans (Crane and Demer 1999;Furst et al 1987;Gauthier and Vercher 1990;Huebner et al 1992;Johnston and Sharpe 1994;McKinley and Peterson 1985;Vercher and Gauthier 1990). These studies show that the gain of the rVOR can be enhanced in trials when the target is space-fixed and diminished in trials when the target is headfixed, but exactly how this occurs is uncertain.…”

Association between vestibuloocular reflex suppression during smooth movements of the head and attention deficit in progressive supranuclear palsy

“…Only trials with a predominant head rotation frequency of 0.3 to 0.4 Hz (confirmed by offline fast Fourier transformation of the head pitch record) were accepted for analysis. This bandwidth was selected to correspond to frequencies where the gain of the VOR is constant and the phase is 180° 20. The eye camera record was used to verify that the accepted trials were free from eye lid, blink artifacts, or blephrospasms.…”