Dataset Information

Columnar processing of border ownership in primate visual cortex.

ABSTRACT: To understand a visual scene, the brain segregates figures from background by assigning borders to foreground objects. Neurons in primate visual cortex encode which object owns a border (border ownership), but the underlying circuitry is not understood. Here, we used multielectrode probes to record from border ownership-selective units in different layers in macaque visual area V4 to study the laminar organization and timing of border ownership selectivity. We find that border ownership selectivity occurs first in deep layer units, in contrast to spike latency for small stimuli in the classical receptive field. Units on the same penetration typically share the preferred side of border ownership, also across layers, similar to orientation preference. Units are often border ownership-selective for a range of border orientations, where the preferred sides of border ownership are systematically organized in visual space. Together our data reveal a columnar organization of border ownership in V4 where the earliest border ownership signals are not simply inherited from upstream areas, but computed by neurons in deep layers, and may thus be part of signals fed back to upstream cortical areas or the oculomotor system early after stimulus onset. The finding that preferred border ownership is clustered and can cover a wide range of spatially contiguous locations suggests that the asymmetric context integrated by these neurons is provided in a systematically clustered manner, possibly through corticocortical feedback and horizontal connections.

SUBMITTER: Franken TP

PROVIDER: S-EPMC8631947 | biostudies-literature |

REPOSITORIES: biostudies-literature

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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.

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Columnar processing of border ownership in primate visual cortex.

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