Role of vestibular signals in the caudal part of the frontal eye fields in pursuit eye movements in three-dimensional space.

For accurate visual information about objects of interest moving slowly in three-dimensional (3D) space, primates with binocular fields use both frontal smooth-pursuit (frontal-pursuit) and vergence eye movements (i.e., depth pursuit) to maintain the images of the objects precisely on the foveae of left and right eyes. Moreover, during head or whole-body movement, both frontal- and depth-pursuit systems must interact with the vestibular system to minimize slip of the retinal images that degrades image quality considerably. The caudal part of the frontal eye fields (FEF) contains many frontal-pursuit neurons. Previous studies have shown that a majority of pursuit neurons there discharge for both frontal pursuit and vergence and carry pursuit-in-3D signals. To understand how vestibular inputs interact with pursuit-in-3D signals, three different experiments that examined the nature of vestibular signals in the caudal FEF are described in this review. A majority of caudal FEF pursuit neurons responded to whole-body rotation with preferred directions similar to frontal-pursuit directions and carried frontal gaze (eye-in-space) velocity signals. They were activated in association with adaptive pursuit eye movements induced by cross-axis pursuit-vestibular interactions. During fore/aft and right/left translation in complete darkness, they were also modulated with preferred directions of many neurons similar to pursuit-preferred directions. Previous studies showed that caudal FEF pursuit neurons also receive visual signals about target motion. Taken together, these results suggest that the caudal FEF coordinates its various inputs to provide signals for accurate eye-movement-in-space commands.