Gaze direction controls response gain in primary visual-cortex neurons

Abstract

To localize objects in space, the brain needs to combine information about the position of the stimulus on the retinae with information about the location of the eyes in their orbits. Interaction between these two types of information occurs in several cortical areas, but the role of the primary visual cortex (area V1) in this process has remained unclear. Here we show that, for half the cells recorded in area V1 of behaving monkeys, the classically described visual responses are strongly modulated by gaze direction. Specifically, we find that selectivity for horizontal retinal disparity-the difference in the position of a stimulus on each retina which relates to relative object distance-and for stimulus orientation may be present at a given gaze direction, but be absent or poorly expressed at another direction. Shifts in preferred disparity also occurred in several neurons. These neural changes were most often present at the beginning of the visual response, suggesting a feedforward gain control by eye position signals. Cortical neural processes for encoding information about the three-dimensional position of a stimulus in space therefore start as early as area V1.

Short-Term Synaptic Depression Causes a Non-Monotonic Response to Correlated Stimuli

“…Systems showing selective neural response and gain modulation, which abound in visual areas and in parietal cortex (Salinas and Thier, 2000), are candidates in which this effect may occur. It is known that V1 cells receive, apart from visual information from the retina, a signal encoding the position of the eyes that modulates their gain (Trotter and Celebrini, 1999). It is plausible that this signal, which gates the flow of retinal information at the LGN (Lal and Friedlander, 1989), could control the degree of synchrony of geniculate cells [which can be very high (Alonso et al, 1996)].…”

Eye position effects in macaque area V4

“…area V1 [9,10]. Different substructures within area V1 feed into different parts of the visual cortical system, i.e.…”

“…Interestingly, eye position effects are not only found in higher dorsal stream areas, but also at the very ®rst stage of visual cortical processing [9,10] as well as in premotor cortex [11,12] and the supplementary eye ®eld [13]. As a general rule valid in all mentioned areas, eye position effects occur at the single cell level but are balanced out at the population level, i.e.…”

Spatiotopic coding and remapping in humans

“…Electrophysiological studies have shown that neurons in specific areas of associative visual cortex, including V6 [3] and ventral intraparietal area (VIP) [4], show the spatiotopic selectivity that we would expect to exist, with spatial tuning in real-world coordinates, invariant of gaze. Indeed, even primary cortex V1 is modulated to some extent by gaze [5], particularly the peripheral representation [6]. What about humans?…”