Interaction between visual and vestibular signals for the control of rapid eye movements.

Abstract

To investigate interactions between voluntary and reflexive eye movements, five subjects were asked to make pro- or anti-saccades to various oblique locations cued by a head-fixed flash while being rotated sinusoidally in yaw (0.17 Hz; 73 degrees /s peak velocity) in complete darkness. Eye movements were recorded with the coil technique. In the pro-saccade task, targeting responses showed clear compensation for the intervening nystagmus, but there was a marked increase in horizontal scatter. Most quick phases directed into the hemifield opposite to the flash (away trials) were suppressed from ~100 ms onward. By contrast, quick phases directed into the hemifield of the flash (toward trials) continued virtually unabated until visually triggered saccades began to appear. From 80 ms onward, these vestibularly triggered movements showed signs of metrical modification by the visual signal. In the anti-saccade experiments, suppression of quick phases away from the flash was just as strong as in the pro-saccade experiments, and error rates in these trials were almost as low as in stationary control conditions. Suppression of quick phases directed toward the flash was a new phenomenon that emerged only in anti-saccade experiments. Since this inhibition had a late onset and was only partial, error rates in anti-saccade toward trials were very high. At short latencies, both components of most rapid eye movements were wrongly directed toward the flash. This was followed by a stage with frequent incongruent responses in which unsuppressed quick phases provoked an incorrect horizontal movement, whereas the vertical component showed a correct anti-saccade response. At still longer latencies, most responses were correct in both components. The visual modification of short-latency responses in both tasks showed that rapid eye movements could not simply be classified as either voluntary or reflexive, but suggested that signals underlying each class could merge into a compromise response. That vestibular rotation during the anti-saccade task may cause a wrongly directed horizontal component resembling a quick phase, combined with a vertical component expressing a correct anti-saccade signal, reveals a remarkable independence at the component level. These observations suggest that voluntary and involuntary movements can be programmed in parallel. This behavior is explained most parsimoniously by assuming that the two signals converge at a component-coding stage of the system, rather than at a vectorial coding stage.