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Recurrent connectivity supports higher-level visual and semantic object representations in the brain

Visual object recognition has been traditionally conceptualised as a predominantly feedforward process through the ventral visual pathway. While feedforward artificial neural networks (ANNs) can achieve human-level classification on some image-labelling tasks, it’s unclear whether computational mode...

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Autores principales: von Seth, Jacqueline, Nicholls, Victoria I., Tyler, Lorraine K., Clarke, Alex
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10682037/
https://www.ncbi.nlm.nih.gov/pubmed/38012301
http://dx.doi.org/10.1038/s42003-023-05565-9
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author von Seth, Jacqueline
Nicholls, Victoria I.
Tyler, Lorraine K.
Clarke, Alex
author_facet von Seth, Jacqueline
Nicholls, Victoria I.
Tyler, Lorraine K.
Clarke, Alex
author_sort von Seth, Jacqueline
collection PubMed
description Visual object recognition has been traditionally conceptualised as a predominantly feedforward process through the ventral visual pathway. While feedforward artificial neural networks (ANNs) can achieve human-level classification on some image-labelling tasks, it’s unclear whether computational models of vision alone can accurately capture the evolving spatiotemporal neural dynamics. Here, we probe these dynamics using a combination of representational similarity and connectivity analyses of fMRI and MEG data recorded during the recognition of familiar, unambiguous objects. Modelling the visual and semantic properties of our stimuli using an artificial neural network as well as a semantic feature model, we find that unique aspects of the neural architecture and connectivity dynamics relate to visual and semantic object properties. Critically, we show that recurrent processing between the anterior and posterior ventral temporal cortex relates to higher-level visual properties prior to semantic object properties, in addition to semantic-related feedback from the frontal lobe to the ventral temporal lobe between 250 and 500 ms after stimulus onset. These results demonstrate the distinct contributions made by semantic object properties in explaining neural activity and connectivity, highlighting it as a core part of object recognition not fully accounted for by current biologically inspired neural networks.
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spelling pubmed-106820372023-11-30 Recurrent connectivity supports higher-level visual and semantic object representations in the brain von Seth, Jacqueline Nicholls, Victoria I. Tyler, Lorraine K. Clarke, Alex Commun Biol Article Visual object recognition has been traditionally conceptualised as a predominantly feedforward process through the ventral visual pathway. While feedforward artificial neural networks (ANNs) can achieve human-level classification on some image-labelling tasks, it’s unclear whether computational models of vision alone can accurately capture the evolving spatiotemporal neural dynamics. Here, we probe these dynamics using a combination of representational similarity and connectivity analyses of fMRI and MEG data recorded during the recognition of familiar, unambiguous objects. Modelling the visual and semantic properties of our stimuli using an artificial neural network as well as a semantic feature model, we find that unique aspects of the neural architecture and connectivity dynamics relate to visual and semantic object properties. Critically, we show that recurrent processing between the anterior and posterior ventral temporal cortex relates to higher-level visual properties prior to semantic object properties, in addition to semantic-related feedback from the frontal lobe to the ventral temporal lobe between 250 and 500 ms after stimulus onset. These results demonstrate the distinct contributions made by semantic object properties in explaining neural activity and connectivity, highlighting it as a core part of object recognition not fully accounted for by current biologically inspired neural networks. Nature Publishing Group UK 2023-11-27 /pmc/articles/PMC10682037/ /pubmed/38012301 http://dx.doi.org/10.1038/s42003-023-05565-9 Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
von Seth, Jacqueline
Nicholls, Victoria I.
Tyler, Lorraine K.
Clarke, Alex
Recurrent connectivity supports higher-level visual and semantic object representations in the brain
title Recurrent connectivity supports higher-level visual and semantic object representations in the brain
title_full Recurrent connectivity supports higher-level visual and semantic object representations in the brain
title_fullStr Recurrent connectivity supports higher-level visual and semantic object representations in the brain
title_full_unstemmed Recurrent connectivity supports higher-level visual and semantic object representations in the brain
title_short Recurrent connectivity supports higher-level visual and semantic object representations in the brain
title_sort recurrent connectivity supports higher-level visual and semantic object representations in the brain
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10682037/
https://www.ncbi.nlm.nih.gov/pubmed/38012301
http://dx.doi.org/10.1038/s42003-023-05565-9
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