Columnar processing of border ownership in primate visual cortex.

Tom P Franken,John H Reynolds

doi:10.7554/elife.72573

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.

Highlights

One of the deepest and most enduring mysteries of visual perception is how the brain constructs an internal model of the ever-changing world that falls before our eyes
We evaluated the latency of spikes evoked by small ring stimuli in the classical receptive field (cRF). For these responses we find, in contrast to border ownership selectivity, that the latency is shorter in the granular layer compared to the deep layers and superficial layers (Figure 3; latency defined as crossing of the functions with a threshold value a third of the way from baseline to peak)
To test whether orientation preference in V4 is shared in clusters that extend vertically across layers, we determined orientation tuning for the units in our sample from responses to luminance contrast edges centered on the cRF

Summary

Introduction

One of the deepest and most enduring mysteries of visual perception is how the brain constructs an internal model of the ever-changing world that falls before our eyes. Electrodes were used to record neural activity in the upper, middle and lower layers of the visual cortex of two rhesus monkeys as they were presented with a set of abstract scenes composed of simple shapes on a background This revealed that cells signaling border ownership in deep layers of the cortex did so before the signals appeared in the middle layer. Franken and Reynolds found that the circuits of the primate brain that compute border ownership occur as columns, in which cells in deep layers signal border ownership first, suggesting that border ownership relies on feedback from more specialized areas. Another possibility is that border ownership selectivity rather represents a surface signal (Grossberg, 2015), and may be less strictly tied to border orientation and orientation tuning We addressed these questions using laminar multielectrode probes to record from border ownership-selective units in macaque area V4 across layers. We examined the relationship between border ownership preference and border orientation preference

Results

Discussion

Materials and methods

Funding Funder