Adaptive changes in vergence eye movements induced by vergence-vestibular interaction training in monkeys

Clear vision of objects moving in three-dimensional space near an observer is attained by a combination of smooth-pursuit and vergence eye movements. The two systems must interact with the vestibular system to maintain the image of the object on the fovea. Previous studies showed that training with smooth-pursuit vestibular interactions resulted in adaptive changes in the smooth-pursuit response. Although vergence and smooth-pursuit systems are thought to have separate neural substrates, recent studies indicate that the caudal parts of the frontal eye fields that receive vestibular inputs contain neurons that discharge in response to combinations of smooth-pursuit and vergence. This combination of discharge sensitivities suggests the possibility that adaptive changes may be induced in the vergence system by vestibular inputs during vergence-pursuit training. To explore this possibility, we examined the effects of training with conflicting vestibular and vergence tracking in four head-stabilized monkeys. Animals were rewarded for tracking a laser spot that moved towards or away from them at 1 Hz in phase with sinusoidal whole-body rotation (+/- 5 degrees) in the pitch plane; the spot moved closer when the monkey's nose moved downward. From the monkey's point of view, the spot moved sinusoidally 10-66 cm in front of them along the mid-sagittal plane, requiring symmetrical vergence eye movements of 4.8 degrees for each eye. Eye movements induced by equivalent spot motion at 0.3-1.0 Hz with or without chair rotation were examined before and after training for each session (0.5-1.0 h). Before training, pitch rotation alone in complete darkness did not induce vergence eye movements in any of the monkeys tested. Vergence tracking without chair rotation showed decreased gain and increased phase lag (re vergence target velocity) at frequencies above 0.5 Hz. After training, the vergence response during chair rotation with the spot showed significantly higher gains and smaller phase lags at 0.3-1.0 Hz in all monkeys. Pitch rotation alone in complete darkness induced vergence eye movements with gains (eye vergence/chair) of 0.15-0.35 after training in two monkeys. These results suggest that vestibular information can be used effectively to modify vergence tracking.