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A Unifying Principle for the Functional Organization of Visual Cortex

A key feature of many cortical systems is functional organization: the arrangement of neurons with specific functional properties in characteristic spatial patterns across the cortical surface. However, the principles underlying the emergence and utility of functional organization are poorly underst...

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Autores principales: Margalit, Eshed, Lee, Hyodong, Finzi, Dawn, DiCarlo, James J., Grill-Spector, Kalanit, Yamins, Daniel L. K.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Cold Spring Harbor Laboratory 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10245753/
https://www.ncbi.nlm.nih.gov/pubmed/37292946
http://dx.doi.org/10.1101/2023.05.18.541361
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author Margalit, Eshed
Lee, Hyodong
Finzi, Dawn
DiCarlo, James J.
Grill-Spector, Kalanit
Yamins, Daniel L. K.
author_facet Margalit, Eshed
Lee, Hyodong
Finzi, Dawn
DiCarlo, James J.
Grill-Spector, Kalanit
Yamins, Daniel L. K.
author_sort Margalit, Eshed
collection PubMed
description A key feature of many cortical systems is functional organization: the arrangement of neurons with specific functional properties in characteristic spatial patterns across the cortical surface. However, the principles underlying the emergence and utility of functional organization are poorly understood. Here we develop the Topographic Deep Artificial Neural Network (TDANN), the first unified model to accurately predict the functional organization of multiple cortical areas in the primate visual system. We analyze the key factors responsible for the TDANN’s success and find that it strikes a balance between two specific objectives: achieving a task-general sensory representation that is self-supervised, and maximizing the smoothness of responses across the cortical sheet according to a metric that scales relative to cortical surface area. In turn, the representations learned by the TDANN are lower dimensional and more brain-like than those in models that lack a spatial smoothness constraint. Finally, we provide evidence that the TDANN’s functional organization balances performance with inter-area connection length, and use the resulting models for a proof-of-principle optimization of cortical prosthetic design. Our results thus offer a unified principle for understanding functional organization and a novel view of the functional role of the visual system in particular.
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spelling pubmed-102457532023-06-08 A Unifying Principle for the Functional Organization of Visual Cortex Margalit, Eshed Lee, Hyodong Finzi, Dawn DiCarlo, James J. Grill-Spector, Kalanit Yamins, Daniel L. K. bioRxiv Article A key feature of many cortical systems is functional organization: the arrangement of neurons with specific functional properties in characteristic spatial patterns across the cortical surface. However, the principles underlying the emergence and utility of functional organization are poorly understood. Here we develop the Topographic Deep Artificial Neural Network (TDANN), the first unified model to accurately predict the functional organization of multiple cortical areas in the primate visual system. We analyze the key factors responsible for the TDANN’s success and find that it strikes a balance between two specific objectives: achieving a task-general sensory representation that is self-supervised, and maximizing the smoothness of responses across the cortical sheet according to a metric that scales relative to cortical surface area. In turn, the representations learned by the TDANN are lower dimensional and more brain-like than those in models that lack a spatial smoothness constraint. Finally, we provide evidence that the TDANN’s functional organization balances performance with inter-area connection length, and use the resulting models for a proof-of-principle optimization of cortical prosthetic design. Our results thus offer a unified principle for understanding functional organization and a novel view of the functional role of the visual system in particular. Cold Spring Harbor Laboratory 2023-05-18 /pmc/articles/PMC10245753/ /pubmed/37292946 http://dx.doi.org/10.1101/2023.05.18.541361 Text en https://creativecommons.org/licenses/by-nc-nd/4.0/This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License (https://creativecommons.org/licenses/by-nc-nd/4.0/) , which allows reusers to copy and distribute the material in any medium or format in unadapted form only, for noncommercial purposes only, and only so long as attribution is given to the creator.
spellingShingle Article
Margalit, Eshed
Lee, Hyodong
Finzi, Dawn
DiCarlo, James J.
Grill-Spector, Kalanit
Yamins, Daniel L. K.
A Unifying Principle for the Functional Organization of Visual Cortex
title A Unifying Principle for the Functional Organization of Visual Cortex
title_full A Unifying Principle for the Functional Organization of Visual Cortex
title_fullStr A Unifying Principle for the Functional Organization of Visual Cortex
title_full_unstemmed A Unifying Principle for the Functional Organization of Visual Cortex
title_short A Unifying Principle for the Functional Organization of Visual Cortex
title_sort unifying principle for the functional organization of visual cortex
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10245753/
https://www.ncbi.nlm.nih.gov/pubmed/37292946
http://dx.doi.org/10.1101/2023.05.18.541361
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