Gaze-dependent visual neurons in area V3A of monkey prestriate cortex

Abstract

Extracellular recordings from single neurons of the prestriate area V3A were carried out in awake, behaving monkeys, to test the influence of the direction of gaze on cellular activity. The responsiveness to visual stimulation of about half of the studied neurons (88/187) was influenced by the animal's direction of gaze: physically identical visual stimuli delivered to identical retinotopic positions (on the receptive field) evoked different responses, depending upon the direction of gaze. Control experiments discount the possibility that the observed phenomenon was due to changes in visual background or in depth, depending on the direction in which the animal was looking. The gaze effect modulated cell excitability with different strengths for different gaze directions. The majority of these neurons were more responsive when the animal looked contralaterally with respect to the hemisphere they were recorded from. Gaze-dependent neurons seem to be segregated in restricted cortical regions, within area V3A, without mixing with non-gaze-dependent cells of the same cortical area. The most reliable differences between V3A gaze-dependent neurons and the same type of cells previously described in area 7a (Andersen and Mountcastle, 1983) concern the small receptive field size, the laterality of gaze effect, and the lack of straight-ahead facilitated or inhibited neurons in area V3A. Since the present results show that V3A gaze-dependent neurons combine information about the position of the eye in the orbit with that of a restricted retinal locus (their receptive field), we suggest that they might directly encode spatial locations of the animal's field of view in a head frame of reference. These cells might be involved in the construction of an internal map of the visual environment in which the topographical position of the objects reflects their objective position in space instead of reflecting the retinotopic position of their images. Such an objective map of the visual world might allow the stability of visual perception despite eye movement.