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Analysis of spiking synchrony in visual cortex reveals distinct types of top-down modulation signals for spatial and object-based attention

The activity of a border ownership selective (BOS) neuron indicates where a foreground object is located relative to its (classical) receptive field (RF). A population of BOS neurons thus provides an important component of perceptual grouping, the organization of the visual scene into objects. In pr...

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Autores principales: Wagatsuma, Nobuhiko, Hu, Brian, von der Heydt, Rüdiger, Niebur, Ernst
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8023487/
https://www.ncbi.nlm.nih.gov/pubmed/33765007
http://dx.doi.org/10.1371/journal.pcbi.1008829
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author Wagatsuma, Nobuhiko
Hu, Brian
von der Heydt, Rüdiger
Niebur, Ernst
author_facet Wagatsuma, Nobuhiko
Hu, Brian
von der Heydt, Rüdiger
Niebur, Ernst
author_sort Wagatsuma, Nobuhiko
collection PubMed
description The activity of a border ownership selective (BOS) neuron indicates where a foreground object is located relative to its (classical) receptive field (RF). A population of BOS neurons thus provides an important component of perceptual grouping, the organization of the visual scene into objects. In previous theoretical work, it has been suggested that this grouping mechanism is implemented by a population of dedicated grouping (“G”) cells that integrate the activity of the distributed feature cells representing an object and, by feedback, modulate the same cells, thus making them border ownership selective. The feedback modulation by G cells is thought to also provide the mechanism for object-based attention. A recent modeling study showed that modulatory common feedback, implemented by synapses with N-methyl-D-aspartate (NMDA)-type glutamate receptors, accounts for the experimentally observed synchrony in spike trains of BOS neurons and the shape of cross-correlations between them, including its dependence on the attentional state. However, that study was limited to pairs of BOS neurons with consistent border ownership preferences, defined as two neurons tuned to respond to the same visual object, in which attention decreases synchrony. But attention has also been shown to increase synchrony in neurons with inconsistent border ownership selectivity. Here we extend the computational model from the previous study to fully understand these effects of attention. We postulate the existence of a second type of G-cell that represents spatial attention by modulating the activity of all BOS cells in a spatially defined area. Simulations of this model show that a combination of spatial and object-based mechanisms fully accounts for the observed pattern of synchrony between BOS neurons. Our results suggest that modulatory feedback from G-cells may underlie both spatial and object-based attention.
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spelling pubmed-80234872021-04-15 Analysis of spiking synchrony in visual cortex reveals distinct types of top-down modulation signals for spatial and object-based attention Wagatsuma, Nobuhiko Hu, Brian von der Heydt, Rüdiger Niebur, Ernst PLoS Comput Biol Research Article The activity of a border ownership selective (BOS) neuron indicates where a foreground object is located relative to its (classical) receptive field (RF). A population of BOS neurons thus provides an important component of perceptual grouping, the organization of the visual scene into objects. In previous theoretical work, it has been suggested that this grouping mechanism is implemented by a population of dedicated grouping (“G”) cells that integrate the activity of the distributed feature cells representing an object and, by feedback, modulate the same cells, thus making them border ownership selective. The feedback modulation by G cells is thought to also provide the mechanism for object-based attention. A recent modeling study showed that modulatory common feedback, implemented by synapses with N-methyl-D-aspartate (NMDA)-type glutamate receptors, accounts for the experimentally observed synchrony in spike trains of BOS neurons and the shape of cross-correlations between them, including its dependence on the attentional state. However, that study was limited to pairs of BOS neurons with consistent border ownership preferences, defined as two neurons tuned to respond to the same visual object, in which attention decreases synchrony. But attention has also been shown to increase synchrony in neurons with inconsistent border ownership selectivity. Here we extend the computational model from the previous study to fully understand these effects of attention. We postulate the existence of a second type of G-cell that represents spatial attention by modulating the activity of all BOS cells in a spatially defined area. Simulations of this model show that a combination of spatial and object-based mechanisms fully accounts for the observed pattern of synchrony between BOS neurons. Our results suggest that modulatory feedback from G-cells may underlie both spatial and object-based attention. Public Library of Science 2021-03-25 /pmc/articles/PMC8023487/ /pubmed/33765007 http://dx.doi.org/10.1371/journal.pcbi.1008829 Text en © 2021 Wagatsuma et al http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Wagatsuma, Nobuhiko
Hu, Brian
von der Heydt, Rüdiger
Niebur, Ernst
Analysis of spiking synchrony in visual cortex reveals distinct types of top-down modulation signals for spatial and object-based attention
title Analysis of spiking synchrony in visual cortex reveals distinct types of top-down modulation signals for spatial and object-based attention
title_full Analysis of spiking synchrony in visual cortex reveals distinct types of top-down modulation signals for spatial and object-based attention
title_fullStr Analysis of spiking synchrony in visual cortex reveals distinct types of top-down modulation signals for spatial and object-based attention
title_full_unstemmed Analysis of spiking synchrony in visual cortex reveals distinct types of top-down modulation signals for spatial and object-based attention
title_short Analysis of spiking synchrony in visual cortex reveals distinct types of top-down modulation signals for spatial and object-based attention
title_sort analysis of spiking synchrony in visual cortex reveals distinct types of top-down modulation signals for spatial and object-based attention
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8023487/
https://www.ncbi.nlm.nih.gov/pubmed/33765007
http://dx.doi.org/10.1371/journal.pcbi.1008829
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