Distributed network flows generate localized category selectivity in human visual cortex
A central goal of neuroscience is to understand how function-relevant brain activations are generated. Here we test the hypothesis that function-relevant brain activations are generated primarily by distributed network flows. We focused on visual processing in human cortex, given the long-standing l...
Gespeichert in:
Veröffentlicht in: | PLoS computational biology 2024-10, Vol.20 (10), p.e1012507 |
---|---|
Hauptverfasser: | , , , , , |
Format: | Artikel |
Sprache: | eng |
Schlagworte: | |
Online-Zugang: | Volltext |
Tags: |
Tag hinzufügen
Keine Tags, Fügen Sie den ersten Tag hinzu!
|
container_end_page | |
---|---|
container_issue | 10 |
container_start_page | e1012507 |
container_title | PLoS computational biology |
container_volume | 20 |
creator | Cocuzza, Carrisa V Sanchez-Romero, Ruben Ito, Takuya Mill, Ravi D Keane, Brian P Cole, Michael W |
description | A central goal of neuroscience is to understand how function-relevant brain activations are generated. Here we test the hypothesis that function-relevant brain activations are generated primarily by distributed network flows. We focused on visual processing in human cortex, given the long-standing literature supporting the functional relevance of brain activations in visual cortex regions exhibiting visual category selectivity. We began by using fMRI data from N = 352 human participants to identify category-specific responses in visual cortex for images of faces, places, body parts, and tools. We then systematically tested the hypothesis that distributed network flows can generate these localized visual category selective responses. This was accomplished using a recently developed approach for simulating - in a highly empirically constrained manner - the generation of task-evoked brain activations by modeling activity flowing over intrinsic brain connections. We next tested refinements to our hypothesis, focusing on how stimulus-driven network interactions initialized in V1 generate downstream visual category selectivity. We found evidence that network flows directly from V1 were sufficient for generating visual category selectivity, but that additional, globally distributed (whole-cortex) network flows increased category selectivity further. Using null network architectures we also found that each region's unique intrinsic "connectivity fingerprint" was key to the generation of category selectivity. These results generalized across regions associated with all four visual categories tested (bodies, faces, places, and tools), and provide evidence that the human brain's intrinsic network organization plays a prominent role in the generation of functionally relevant, localized responses. |
doi_str_mv | 10.1371/journal.pcbi.1012507 |
format | Article |
fullrecord | <record><control><sourceid>gale_proqu</sourceid><recordid>TN_cdi_proquest_miscellaneous_3119721909</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><galeid>A815030030</galeid><sourcerecordid>A815030030</sourcerecordid><originalsourceid>FETCH-LOGICAL-c367t-6ce1969a5dee8bd3d4ae3e0c02e9883eb07c396ca4074da8dc40357fb17250e73</originalsourceid><addsrcrecordid>eNqVkk9PGzEQxS0EgpD2GyBkqZdySGrHu-v1MQqlRYpA6h-pN8vrnQ0G7zrY3kD66esoARGpF-SDx6Pfs_RmHkJnlIwp4_TLvet9p-x4qSszpoROcsIP0IDmORtxlpeHb-oTdBrCPSGpFMUxOmEiY4WYiAH6c2lC9KbqI9S4g_jk_ANurHsKeAEdeBUBW6eVNX8ToNNz4fwaB7Cgo1mZuMamw3d9qzq8MqFXFmvnIzx_QEeNsgE-7u4h-n319dfs-2h---16Np2PNCt4HBUaqCiEymuAsqpZnSlgQDSZgChLBhXhmolCq4zwrFZlrbPkgjcV5ckwcDZEn7f_Lr177CFE2ZqgwVrVgeuDZJQKPqGCiIR-2qILZUGarnHRK73B5bSkOWFpQCRR4_9Q6dTQGu06aEzq7wku9gSJSf7jQvUhyOufP97B3uyz2ZbV3oXgoZFLb1rl15ISuYmA3EVAbiIgdxFIsvPdQPqqhfpV9LJz9g_Prq6u</addsrcrecordid><sourcetype>Aggregation Database</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>3119721909</pqid></control><display><type>article</type><title>Distributed network flows generate localized category selectivity in human visual cortex</title><source>MEDLINE</source><source>DOAJ Directory of Open Access Journals</source><source>Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals</source><source>Public Library of Science (PLoS)</source><source>PubMed Central</source><creator>Cocuzza, Carrisa V ; Sanchez-Romero, Ruben ; Ito, Takuya ; Mill, Ravi D ; Keane, Brian P ; Cole, Michael W</creator><contributor>Kay, Kendrick</contributor><creatorcontrib>Cocuzza, Carrisa V ; Sanchez-Romero, Ruben ; Ito, Takuya ; Mill, Ravi D ; Keane, Brian P ; Cole, Michael W ; Kay, Kendrick</creatorcontrib><description>A central goal of neuroscience is to understand how function-relevant brain activations are generated. Here we test the hypothesis that function-relevant brain activations are generated primarily by distributed network flows. We focused on visual processing in human cortex, given the long-standing literature supporting the functional relevance of brain activations in visual cortex regions exhibiting visual category selectivity. We began by using fMRI data from N = 352 human participants to identify category-specific responses in visual cortex for images of faces, places, body parts, and tools. We then systematically tested the hypothesis that distributed network flows can generate these localized visual category selective responses. This was accomplished using a recently developed approach for simulating - in a highly empirically constrained manner - the generation of task-evoked brain activations by modeling activity flowing over intrinsic brain connections. We next tested refinements to our hypothesis, focusing on how stimulus-driven network interactions initialized in V1 generate downstream visual category selectivity. We found evidence that network flows directly from V1 were sufficient for generating visual category selectivity, but that additional, globally distributed (whole-cortex) network flows increased category selectivity further. Using null network architectures we also found that each region's unique intrinsic "connectivity fingerprint" was key to the generation of category selectivity. These results generalized across regions associated with all four visual categories tested (bodies, faces, places, and tools), and provide evidence that the human brain's intrinsic network organization plays a prominent role in the generation of functionally relevant, localized responses.</description><identifier>ISSN: 1553-7358</identifier><identifier>ISSN: 1553-734X</identifier><identifier>EISSN: 1553-7358</identifier><identifier>DOI: 10.1371/journal.pcbi.1012507</identifier><identifier>PMID: 39436929</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Adult ; Brain Mapping - methods ; Computational Biology ; Female ; Humans ; Magnetic Resonance Imaging ; Male ; Models, Neurological ; Nerve Net - physiology ; Neural circuitry ; Photic Stimulation ; Visual cortex ; Visual Cortex - physiology ; Visual Perception - physiology ; Young Adult</subject><ispartof>PLoS computational biology, 2024-10, Vol.20 (10), p.e1012507</ispartof><rights>Copyright: © 2024 Cocuzza et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.</rights><rights>COPYRIGHT 2024 Public Library of Science</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c367t-6ce1969a5dee8bd3d4ae3e0c02e9883eb07c396ca4074da8dc40357fb17250e73</cites><orcidid>0000-0002-2060-4608 ; 0000-0001-5117-2433</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>314,780,784,864,2928,27924,27925</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/39436929$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Kay, Kendrick</contributor><creatorcontrib>Cocuzza, Carrisa V</creatorcontrib><creatorcontrib>Sanchez-Romero, Ruben</creatorcontrib><creatorcontrib>Ito, Takuya</creatorcontrib><creatorcontrib>Mill, Ravi D</creatorcontrib><creatorcontrib>Keane, Brian P</creatorcontrib><creatorcontrib>Cole, Michael W</creatorcontrib><title>Distributed network flows generate localized category selectivity in human visual cortex</title><title>PLoS computational biology</title><addtitle>PLoS Comput Biol</addtitle><description>A central goal of neuroscience is to understand how function-relevant brain activations are generated. Here we test the hypothesis that function-relevant brain activations are generated primarily by distributed network flows. We focused on visual processing in human cortex, given the long-standing literature supporting the functional relevance of brain activations in visual cortex regions exhibiting visual category selectivity. We began by using fMRI data from N = 352 human participants to identify category-specific responses in visual cortex for images of faces, places, body parts, and tools. We then systematically tested the hypothesis that distributed network flows can generate these localized visual category selective responses. This was accomplished using a recently developed approach for simulating - in a highly empirically constrained manner - the generation of task-evoked brain activations by modeling activity flowing over intrinsic brain connections. We next tested refinements to our hypothesis, focusing on how stimulus-driven network interactions initialized in V1 generate downstream visual category selectivity. We found evidence that network flows directly from V1 were sufficient for generating visual category selectivity, but that additional, globally distributed (whole-cortex) network flows increased category selectivity further. Using null network architectures we also found that each region's unique intrinsic "connectivity fingerprint" was key to the generation of category selectivity. These results generalized across regions associated with all four visual categories tested (bodies, faces, places, and tools), and provide evidence that the human brain's intrinsic network organization plays a prominent role in the generation of functionally relevant, localized responses.</description><subject>Adult</subject><subject>Brain Mapping - methods</subject><subject>Computational Biology</subject><subject>Female</subject><subject>Humans</subject><subject>Magnetic Resonance Imaging</subject><subject>Male</subject><subject>Models, Neurological</subject><subject>Nerve Net - physiology</subject><subject>Neural circuitry</subject><subject>Photic Stimulation</subject><subject>Visual cortex</subject><subject>Visual Cortex - physiology</subject><subject>Visual Perception - physiology</subject><subject>Young Adult</subject><issn>1553-7358</issn><issn>1553-734X</issn><issn>1553-7358</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqVkk9PGzEQxS0EgpD2GyBkqZdySGrHu-v1MQqlRYpA6h-pN8vrnQ0G7zrY3kD66esoARGpF-SDx6Pfs_RmHkJnlIwp4_TLvet9p-x4qSszpoROcsIP0IDmORtxlpeHb-oTdBrCPSGpFMUxOmEiY4WYiAH6c2lC9KbqI9S4g_jk_ANurHsKeAEdeBUBW6eVNX8ToNNz4fwaB7Cgo1mZuMamw3d9qzq8MqFXFmvnIzx_QEeNsgE-7u4h-n319dfs-2h---16Np2PNCt4HBUaqCiEymuAsqpZnSlgQDSZgChLBhXhmolCq4zwrFZlrbPkgjcV5ckwcDZEn7f_Lr177CFE2ZqgwVrVgeuDZJQKPqGCiIR-2qILZUGarnHRK73B5bSkOWFpQCRR4_9Q6dTQGu06aEzq7wku9gSJSf7jQvUhyOufP97B3uyz2ZbV3oXgoZFLb1rl15ISuYmA3EVAbiIgdxFIsvPdQPqqhfpV9LJz9g_Prq6u</recordid><startdate>20241022</startdate><enddate>20241022</enddate><creator>Cocuzza, Carrisa V</creator><creator>Sanchez-Romero, Ruben</creator><creator>Ito, Takuya</creator><creator>Mill, Ravi D</creator><creator>Keane, Brian P</creator><creator>Cole, Michael W</creator><general>Public Library of Science</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>ISN</scope><scope>ISR</scope><scope>7X8</scope><orcidid>https://orcid.org/0000-0002-2060-4608</orcidid><orcidid>https://orcid.org/0000-0001-5117-2433</orcidid></search><sort><creationdate>20241022</creationdate><title>Distributed network flows generate localized category selectivity in human visual cortex</title><author>Cocuzza, Carrisa V ; Sanchez-Romero, Ruben ; Ito, Takuya ; Mill, Ravi D ; Keane, Brian P ; Cole, Michael W</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c367t-6ce1969a5dee8bd3d4ae3e0c02e9883eb07c396ca4074da8dc40357fb17250e73</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2024</creationdate><topic>Adult</topic><topic>Brain Mapping - methods</topic><topic>Computational Biology</topic><topic>Female</topic><topic>Humans</topic><topic>Magnetic Resonance Imaging</topic><topic>Male</topic><topic>Models, Neurological</topic><topic>Nerve Net - physiology</topic><topic>Neural circuitry</topic><topic>Photic Stimulation</topic><topic>Visual cortex</topic><topic>Visual Cortex - physiology</topic><topic>Visual Perception - physiology</topic><topic>Young Adult</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Cocuzza, Carrisa V</creatorcontrib><creatorcontrib>Sanchez-Romero, Ruben</creatorcontrib><creatorcontrib>Ito, Takuya</creatorcontrib><creatorcontrib>Mill, Ravi D</creatorcontrib><creatorcontrib>Keane, Brian P</creatorcontrib><creatorcontrib>Cole, Michael W</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Gale In Context: Canada</collection><collection>Gale In Context: Science</collection><collection>MEDLINE - Academic</collection><jtitle>PLoS computational biology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Cocuzza, Carrisa V</au><au>Sanchez-Romero, Ruben</au><au>Ito, Takuya</au><au>Mill, Ravi D</au><au>Keane, Brian P</au><au>Cole, Michael W</au><au>Kay, Kendrick</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Distributed network flows generate localized category selectivity in human visual cortex</atitle><jtitle>PLoS computational biology</jtitle><addtitle>PLoS Comput Biol</addtitle><date>2024-10-22</date><risdate>2024</risdate><volume>20</volume><issue>10</issue><spage>e1012507</spage><pages>e1012507-</pages><issn>1553-7358</issn><issn>1553-734X</issn><eissn>1553-7358</eissn><abstract>A central goal of neuroscience is to understand how function-relevant brain activations are generated. Here we test the hypothesis that function-relevant brain activations are generated primarily by distributed network flows. We focused on visual processing in human cortex, given the long-standing literature supporting the functional relevance of brain activations in visual cortex regions exhibiting visual category selectivity. We began by using fMRI data from N = 352 human participants to identify category-specific responses in visual cortex for images of faces, places, body parts, and tools. We then systematically tested the hypothesis that distributed network flows can generate these localized visual category selective responses. This was accomplished using a recently developed approach for simulating - in a highly empirically constrained manner - the generation of task-evoked brain activations by modeling activity flowing over intrinsic brain connections. We next tested refinements to our hypothesis, focusing on how stimulus-driven network interactions initialized in V1 generate downstream visual category selectivity. We found evidence that network flows directly from V1 were sufficient for generating visual category selectivity, but that additional, globally distributed (whole-cortex) network flows increased category selectivity further. Using null network architectures we also found that each region's unique intrinsic "connectivity fingerprint" was key to the generation of category selectivity. These results generalized across regions associated with all four visual categories tested (bodies, faces, places, and tools), and provide evidence that the human brain's intrinsic network organization plays a prominent role in the generation of functionally relevant, localized responses.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>39436929</pmid><doi>10.1371/journal.pcbi.1012507</doi><tpages>e1012507</tpages><orcidid>https://orcid.org/0000-0002-2060-4608</orcidid><orcidid>https://orcid.org/0000-0001-5117-2433</orcidid><oa>free_for_read</oa></addata></record> |
fulltext | fulltext |
identifier | ISSN: 1553-7358 |
ispartof | PLoS computational biology, 2024-10, Vol.20 (10), p.e1012507 |
issn | 1553-7358 1553-734X 1553-7358 |
language | eng |
recordid | cdi_proquest_miscellaneous_3119721909 |
source | MEDLINE; DOAJ Directory of Open Access Journals; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; Public Library of Science (PLoS); PubMed Central |
subjects | Adult Brain Mapping - methods Computational Biology Female Humans Magnetic Resonance Imaging Male Models, Neurological Nerve Net - physiology Neural circuitry Photic Stimulation Visual cortex Visual Cortex - physiology Visual Perception - physiology Young Adult |
title | Distributed network flows generate localized category selectivity in human visual cortex |
url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-01-04T16%3A36%3A21IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-gale_proqu&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Distributed%20network%20flows%20generate%20localized%20category%20selectivity%20in%20human%20visual%20cortex&rft.jtitle=PLoS%20computational%20biology&rft.au=Cocuzza,%20Carrisa%20V&rft.date=2024-10-22&rft.volume=20&rft.issue=10&rft.spage=e1012507&rft.pages=e1012507-&rft.issn=1553-7358&rft.eissn=1553-7358&rft_id=info:doi/10.1371/journal.pcbi.1012507&rft_dat=%3Cgale_proqu%3EA815030030%3C/gale_proqu%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=3119721909&rft_id=info:pmid/39436929&rft_galeid=A815030030&rfr_iscdi=true |