Scaling of compensatory eye movements during translations: virtual versus real depth

Abstract

Vestibulo-ocular reflexes are the fastest compensatory reflex systems. One of these is the translational vestibulo-ocular reflex (TVOR) which stabilizes the gaze at a given fixation point during whole body translations. For a proper response of the TVOR the eyes have to counter rotate in the head with a velocity that is inversely scaled to viewing distance of the target. It is generally assumed that scaling of the TVOR is automatically coupled to vergence angle at the brainstem level. However, different lines of evidence also argue that in humans scaling of the TVOR also depends on a mechanism that pre-sets gain on a priori knowledge of target distance. To discriminate between these two possibilities we used a real target paradigm with vergence angle coupled to distance and a virtual target paradigm with vergence angle dissociated from target distance. We compared TVOR responses in six subjects who underwent lateral sinusoidal whole-body translations at 1 and 2 Hz. Real targets varied between distance of 50 and 22.4 cm in front of the subjects, whereas the virtual targets consisting of a green and red light emitting diode (LED) were physically located at 50 cm from the subject. Red and green LED's were dichoptically viewed. By shifting the red LED relative to the green LED we created a range of virtual viewing distances where vergence angle changed but the ideal kinematic eye velocity was always the same. Eye velocity data recorded with virtual targets were compared to eye velocity data recorded with real targets. We also used flashing targets (flash frequency 1 Hz, duration 5 ms). During the real, continuous visible targets condition scaling of compensatory eye velocity with vergence angle was nearly perfect. During viewing of virtual targets, and with flashed targets compensatory eye velocity only weakly correlated to vergence angle, indicating that vergence angle is only partially coupled to compensatory eye velocity during translation. Our data suggest that in humans vergence angle as a measure of target distance estimation has only limited use for automatic TVOR scaling.

Figure 1

The two real and virtual target paradigms. Panel A shows the real targets that were located at 5 distances from the subject. Panel B shows the ‘virtual targets’; six optic fibre tips (top circles): one green fibre on the left (filled circle) and five red fibres on the right (open circles). These are seen through red and green filters (bottom bars): the left eye could only see the red fibres; the right eye only the green fibre. Only two fibres were switched on at the same time: the green one and one of the red ones. The distance to the intersections of the lines of sight of both eyes (striped circles) was defined as virtual target distance. The target distances of the virtual targets in B matched those of the real targets in A. Note that for the furthest virtual target, the green and red fibre are located at approximately the same position. This target therefore resembles a real target.

Figure 2

Example (subject 2) of platform position (upper panel), and eye movements (lower four panels) recorded with the search coil system, under the four different target conditions: real continuous, virtual continuous, real flashed and virtual flashed. Upper traces in each panel represent left eye positions, the lower traces right eye positions. Dashed vertical lines indicate the moments in time at which the flashes occurred. Upward deflections: rightward horizontal eye movements.

Figure 3

Gaze versus vergence angle during whole-body translations at 2 Hz. In this plot vergence angle is plotted on the y-axis (zero vergence at top), whereas the gaze positions of the left (blue) and right (red) eyes are plotted on the X-axis. The panel shows that for real targets (upper panel) there is an increase in gaze amplitude and vergence angle as a function of vergence. Gaze trajectories become larger for near viewing distances, consistent with the geometrical requirement for keeping the eyes on target during the linear translations. The lower panel of figure 3 shows as an example a gaze vergence plot of eye movements in response to the targets at all presented virtual distances. For any virtual distance, the gaze amplitude of the right and left eye remained the same regardless of the vergence angle required to fuse the virtual target by shifting the left eye (blue traces) to the right

Figure 4

Peak eye velocity as a function of vergence angle during 1 and 2 Hz sinusoidal translations (left and right panels respectively). The solid line in each panel shows the expected eye velocity for the continuously viewed real target condition. The slope of this line, 4.92 °/s per degree of vergence represents the expected ideal relationship between eye velocity and vergence angle. The dashed line is the expected eye velocity for the virtual target condition. Data from individual subjects are indicated with different colours. Squares: real targets, Circles: virtual targets. Upper panels: continuously lit targets, Lower panels: strobed targets.

Figure 5

Smooth pursuit gain as function of sinusoidal stimulation frequency and viewing distance . Frequency range was between 0.25 and 2.0 Hz. Viewing distance varied between 189 and 26 cm. Smooth pursuit gain decreases as a function of frequency is not modulated by target distance or vergence angle.