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Disinhibitory circuit mediated by connections from vasoactive intestinal polypeptide to somatostatin interneurons underlies the paradoxical decrease in spike synchrony with increased border ownership selective neuron firing rate

The activity of border ownership selective (BOS) neurons in intermediate-level visual areas indicates which side of a contour owns a border relative to its classical receptive field and provides a fundamental component of figure-ground segregation. A physiological study reported that selective atten...

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Autores principales: Wagatsuma, Nobuhiko, Shimomura, Haruka, Nobukawa, Sou
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9672816/
https://www.ncbi.nlm.nih.gov/pubmed/36405781
http://dx.doi.org/10.3389/fncom.2022.988715
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author Wagatsuma, Nobuhiko
Shimomura, Haruka
Nobukawa, Sou
author_facet Wagatsuma, Nobuhiko
Shimomura, Haruka
Nobukawa, Sou
author_sort Wagatsuma, Nobuhiko
collection PubMed
description The activity of border ownership selective (BOS) neurons in intermediate-level visual areas indicates which side of a contour owns a border relative to its classical receptive field and provides a fundamental component of figure-ground segregation. A physiological study reported that selective attention facilitates the activity of BOS neurons with a consistent border ownership preference, defined as two neurons tuned to respond to the same visual object. However, spike synchrony between this pair is significantly suppressed by selective attention. These neurophysiological findings are derived from a biologically-plausible microcircuit model consisting of spiking neurons including two subtypes of inhibitory interneurons, somatostatin (SOM) and vasoactive intestinal polypeptide (VIP) interneurons, and excitatory BOS model neurons. In our proposed model, BOS neurons and SOM interneurons cooperate and interact with each other. VIP interneurons not only suppress SOM interneuron responses but also are activated by feedback signals mediating selective attention, which leads to disinhibition of BOS neurons when they are directing selective attention toward an object. Our results suggest that disinhibition arising from the synaptic connections from VIP to SOM interneurons plays a critical role in attentional modulation of neurons in intermediate-level visual areas.
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spelling pubmed-96728162022-11-19 Disinhibitory circuit mediated by connections from vasoactive intestinal polypeptide to somatostatin interneurons underlies the paradoxical decrease in spike synchrony with increased border ownership selective neuron firing rate Wagatsuma, Nobuhiko Shimomura, Haruka Nobukawa, Sou Front Comput Neurosci Neuroscience The activity of border ownership selective (BOS) neurons in intermediate-level visual areas indicates which side of a contour owns a border relative to its classical receptive field and provides a fundamental component of figure-ground segregation. A physiological study reported that selective attention facilitates the activity of BOS neurons with a consistent border ownership preference, defined as two neurons tuned to respond to the same visual object. However, spike synchrony between this pair is significantly suppressed by selective attention. These neurophysiological findings are derived from a biologically-plausible microcircuit model consisting of spiking neurons including two subtypes of inhibitory interneurons, somatostatin (SOM) and vasoactive intestinal polypeptide (VIP) interneurons, and excitatory BOS model neurons. In our proposed model, BOS neurons and SOM interneurons cooperate and interact with each other. VIP interneurons not only suppress SOM interneuron responses but also are activated by feedback signals mediating selective attention, which leads to disinhibition of BOS neurons when they are directing selective attention toward an object. Our results suggest that disinhibition arising from the synaptic connections from VIP to SOM interneurons plays a critical role in attentional modulation of neurons in intermediate-level visual areas. Frontiers Media S.A. 2022-11-04 /pmc/articles/PMC9672816/ /pubmed/36405781 http://dx.doi.org/10.3389/fncom.2022.988715 Text en Copyright © 2022 Wagatsuma, Shimomura and Nobukawa. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Neuroscience
Wagatsuma, Nobuhiko
Shimomura, Haruka
Nobukawa, Sou
Disinhibitory circuit mediated by connections from vasoactive intestinal polypeptide to somatostatin interneurons underlies the paradoxical decrease in spike synchrony with increased border ownership selective neuron firing rate
title Disinhibitory circuit mediated by connections from vasoactive intestinal polypeptide to somatostatin interneurons underlies the paradoxical decrease in spike synchrony with increased border ownership selective neuron firing rate
title_full Disinhibitory circuit mediated by connections from vasoactive intestinal polypeptide to somatostatin interneurons underlies the paradoxical decrease in spike synchrony with increased border ownership selective neuron firing rate
title_fullStr Disinhibitory circuit mediated by connections from vasoactive intestinal polypeptide to somatostatin interneurons underlies the paradoxical decrease in spike synchrony with increased border ownership selective neuron firing rate
title_full_unstemmed Disinhibitory circuit mediated by connections from vasoactive intestinal polypeptide to somatostatin interneurons underlies the paradoxical decrease in spike synchrony with increased border ownership selective neuron firing rate
title_short Disinhibitory circuit mediated by connections from vasoactive intestinal polypeptide to somatostatin interneurons underlies the paradoxical decrease in spike synchrony with increased border ownership selective neuron firing rate
title_sort disinhibitory circuit mediated by connections from vasoactive intestinal polypeptide to somatostatin interneurons underlies the paradoxical decrease in spike synchrony with increased border ownership selective neuron firing rate
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9672816/
https://www.ncbi.nlm.nih.gov/pubmed/36405781
http://dx.doi.org/10.3389/fncom.2022.988715
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