Dataset Information

A Stable Visual World in Primate Primary Visual Cortex.

ABSTRACT: Humans and other primates rely on eye movements to explore visual scenes and to track moving objects. As a result, the image that is projected onto the retina-and propagated throughout the visual cortical hierarchy-is almost constantly changing and makes little sense without taking into account the momentary direction of gaze. How is this achieved in the visual system? Here, we show that in primary visual cortex (V1), the earliest stage of cortical vision, neural representations carry an embedded "eye tracker" that signals the direction of gaze associated with each image. Using chronically implanted multi-electrode arrays, we recorded the activity of neurons in area V1 of macaque monkeys during tasks requiring fast (exploratory) and slow (pursuit) eye movements. Neurons were stimulated with flickering, full-field luminance noise at all times. As in previous studies, we observed neurons that were sensitive to gaze direction during fixation, despite comparable stimulation of their receptive fields. We trained a decoder to translate neural activity into metric estimates of gaze direction. This decoded signal tracked the eye accurately not only during fixation but also during fast and slow eye movements. After a fast eye movement, the eye-position signal arrived in V1 at approximately the same time at which the new visual information arrived from the retina. Using simulations, we show that this V1 eye-position signal could be used to take into account the sensory consequences of eye movements and map the fleeting positions of objects on the retina onto their stable position in the world.

SUBMITTER: Morris AP

PROVIDER: S-EPMC6519108 | biostudies-literature | 2019 May

REPOSITORIES: biostudies-literature

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A Stable Visual World in Primate Primary Visual Cortex.

Morris Adam P AP Krekelberg Bart B

Current biology : CB 20190425 9

Humans and other primates rely on eye movements to explore visual scenes and to track moving objects. As a result, the image that is projected onto the retina-and propagated throughout the visual cortical hierarchy-is almost constantly changing and makes little sense without taking into account the momentary direction of gaze. How is this achieved in the visual system? Here, we show that in primary visual cortex (V1), the earliest stage of cortical vision, neural representations carry an embedde ...[more]

PMID: 31031112

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Project description:Our perception of how objects are laid out in visual scenes is remarkably stable, despite rapid shifts in the patterns of light that fall on the retina with each saccade. One mechanism that may help establish perceptual stability is border ownership assignment. Studies in macaque area V2 have identified border ownership neurons that signal which side of a border belongs to a foreground surface. This signal persists for hundreds of milliseconds after border ownership has been rendered ambiguous by deleting the stimulus features that distinguish foreground from background. Remarkably, this signal survives eye movements: border ownership neurons also exhibit border ownership signals de novo when an eye movement places the newly ambiguous border within their receptive field. The grouping cell hypothesis proposes the existence of hypothetical grouping cells in a downstream brain area. These cells would compute persistent proto-object representations and therefore have the properties to endow cells in upstream brain areas with selectivity for border ownership. Such grouping cells have been predicted to show a centripetal and persistent pattern of preferred side of ownership for a border placed parallel to the perimeter of their classical receptive field, and such a centripetal ownership preference pattern should also occur de novo in these same cells if an ambiguous border lands in their receptive field after a saccade. It is unknown if grouping cells exist. Here we used laminar multielectrodes in area V4 - the main source of feedback to V2 - of behaving macaques to determine whether such grouping cells exist. Consistent with the model prediction we find a substantial population of neurons with these properties, in all laminar compartments, and they exhibit a response latency that is short enough to act as the source that endows neurons in V2 with selectivity for border ownership. While grouping cell activity provides information about the location of foreground surfaces, these neurons are, counterintuitively, not as strongly tuned for luminance contrast polarity, a feature of those surfaces, as are border ownership cells. Our data suggest a division of labor in which these newly discovered grouping cells provide spatiotemporal continuity of segmented surfaces whereas border ownership cells link this location information with surface features such as luminance contrast.

Dataset Information

A Stable Visual World in Primate Primary Visual Cortex.

Publications

A Stable Visual World in Primate Primary Visual Cortex.

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