Specific excitatory connectivity for feature integration in mouse primary visual cortex.

Local excitatory connections in mouse primary visual cortex (V1) are stronger and more prevalent between neurons that share similar functional response features. However, the details of how functional rules for local connectivity shape neuronal responses in V1 remain unknown. We hypothesised that co...

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Main Authors: Dylan R Muir, Patricia Molina-Luna, Morgane M Roth, Fritjof Helmchen, Björn M Kampa
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2017-12-01
Series:PLoS Computational Biology
Online Access:http://europepmc.org/articles/PMC5746254?pdf=render
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author Dylan R Muir
Patricia Molina-Luna
Morgane M Roth
Fritjof Helmchen
Björn M Kampa
author_facet Dylan R Muir
Patricia Molina-Luna
Morgane M Roth
Fritjof Helmchen
Björn M Kampa
author_sort Dylan R Muir
collection DOAJ
description Local excitatory connections in mouse primary visual cortex (V1) are stronger and more prevalent between neurons that share similar functional response features. However, the details of how functional rules for local connectivity shape neuronal responses in V1 remain unknown. We hypothesised that complex responses to visual stimuli may arise as a consequence of rules for selective excitatory connectivity within the local network in the superficial layers of mouse V1. In mouse V1 many neurons respond to overlapping grating stimuli (plaid stimuli) with highly selective and facilitatory responses, which are not simply predicted by responses to single gratings presented alone. This complexity is surprising, since excitatory neurons in V1 are considered to be mainly tuned to single preferred orientations. Here we examined the consequences for visual processing of two alternative connectivity schemes: in the first case, local connections are aligned with visual properties inherited from feedforward input (a 'like-to-like' scheme specifically connecting neurons that share similar preferred orientations); in the second case, local connections group neurons into excitatory subnetworks that combine and amplify multiple feedforward visual properties (a 'feature binding' scheme). By comparing predictions from large scale computational models with in vivo recordings of visual representations in mouse V1, we found that responses to plaid stimuli were best explained by assuming feature binding connectivity. Unlike under the like-to-like scheme, selective amplification within feature-binding excitatory subnetworks replicated experimentally observed facilitatory responses to plaid stimuli; explained selective plaid responses not predicted by grating selectivity; and was consistent with broad anatomical selectivity observed in mouse V1. Our results show that visual feature binding can occur through local recurrent mechanisms without requiring feedforward convergence, and that such a mechanism is consistent with visual responses and cortical anatomy in mouse V1.
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spelling doaj.art-b11040467d66497e891165b7df4b81112022-12-22T00:02:50ZengPublic Library of Science (PLoS)PLoS Computational Biology1553-734X1553-73582017-12-011312e100588810.1371/journal.pcbi.1005888Specific excitatory connectivity for feature integration in mouse primary visual cortex.Dylan R MuirPatricia Molina-LunaMorgane M RothFritjof HelmchenBjörn M KampaLocal excitatory connections in mouse primary visual cortex (V1) are stronger and more prevalent between neurons that share similar functional response features. However, the details of how functional rules for local connectivity shape neuronal responses in V1 remain unknown. We hypothesised that complex responses to visual stimuli may arise as a consequence of rules for selective excitatory connectivity within the local network in the superficial layers of mouse V1. In mouse V1 many neurons respond to overlapping grating stimuli (plaid stimuli) with highly selective and facilitatory responses, which are not simply predicted by responses to single gratings presented alone. This complexity is surprising, since excitatory neurons in V1 are considered to be mainly tuned to single preferred orientations. Here we examined the consequences for visual processing of two alternative connectivity schemes: in the first case, local connections are aligned with visual properties inherited from feedforward input (a 'like-to-like' scheme specifically connecting neurons that share similar preferred orientations); in the second case, local connections group neurons into excitatory subnetworks that combine and amplify multiple feedforward visual properties (a 'feature binding' scheme). By comparing predictions from large scale computational models with in vivo recordings of visual representations in mouse V1, we found that responses to plaid stimuli were best explained by assuming feature binding connectivity. Unlike under the like-to-like scheme, selective amplification within feature-binding excitatory subnetworks replicated experimentally observed facilitatory responses to plaid stimuli; explained selective plaid responses not predicted by grating selectivity; and was consistent with broad anatomical selectivity observed in mouse V1. Our results show that visual feature binding can occur through local recurrent mechanisms without requiring feedforward convergence, and that such a mechanism is consistent with visual responses and cortical anatomy in mouse V1.http://europepmc.org/articles/PMC5746254?pdf=render
spellingShingle Dylan R Muir
Patricia Molina-Luna
Morgane M Roth
Fritjof Helmchen
Björn M Kampa
Specific excitatory connectivity for feature integration in mouse primary visual cortex.
PLoS Computational Biology
title Specific excitatory connectivity for feature integration in mouse primary visual cortex.
title_full Specific excitatory connectivity for feature integration in mouse primary visual cortex.
title_fullStr Specific excitatory connectivity for feature integration in mouse primary visual cortex.
title_full_unstemmed Specific excitatory connectivity for feature integration in mouse primary visual cortex.
title_short Specific excitatory connectivity for feature integration in mouse primary visual cortex.
title_sort specific excitatory connectivity for feature integration in mouse primary visual cortex
url http://europepmc.org/articles/PMC5746254?pdf=render
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AT fritjofhelmchen specificexcitatoryconnectivityforfeatureintegrationinmouseprimaryvisualcortex
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