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Anatomical correlates of category-selective visual regions have distinctive signatures of connectivity in neonates
The ventral visual stream is shaped during development by innate proto-organization within the visual system, such as the strong input from the fovea to the fusiform face area. In adults, category-selective regions have distinct signatures of connectivity to brain regions beyond the visual system, l...
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Published in: | Developmental cognitive neuroscience 2022-12, Vol.58, p.101179, Article 101179 |
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description | The ventral visual stream is shaped during development by innate proto-organization within the visual system, such as the strong input from the fovea to the fusiform face area. In adults, category-selective regions have distinct signatures of connectivity to brain regions beyond the visual system, likely reflecting cross-modal and motoric associations. We tested if this long-range connectivity is part of the innate proto-organization, or if it develops with postnatal experience, by using diffusion-weighted imaging to characterize the connectivity of anatomical correlates of category-selective regions in neonates (N = 445), 1–9 month old infants (N = 11), and adults (N = 14). Using the HCP data we identified face- and place- selective regions and a third intermediate region with a distinct profile of selectivity. Using linear classifiers, these regions were found to have distinctive connectivity at birth, to other regions in the visual system and to those outside of it. The results support an extended proto-organization that includes long-range connectivity that shapes, and is shaped by, experience-dependent development.
•Anatomical correlates of neonate category-selective regions had mature signatures of structural connectivity.•As identified with linear discriminant classifiers, face networks developed early and experienced the least change.•Long-range connections to distal regions are part of the innate proto-organization.•Category-selective regions were identified by connectivity to the visual system, replicating past proto-organizations. |
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•Anatomical correlates of neonate category-selective regions had mature signatures of structural connectivity.•As identified with linear discriminant classifiers, face networks developed early and experienced the least change.•Long-range connections to distal regions are part of the innate proto-organization.•Category-selective regions were identified by connectivity to the visual system, replicating past proto-organizations.</description><identifier>ISSN: 1878-9293</identifier><identifier>ISSN: 1878-9307</identifier><identifier>EISSN: 1878-9307</identifier><identifier>DOI: 10.1016/j.dcn.2022.101179</identifier><identifier>PMID: 36521345</identifier><language>eng</language><publisher>Netherlands: Elsevier Ltd</publisher><subject>Adult ; Brain ; Brain Mapping ; Classification ; Diffusion Magnetic Resonance Imaging ; Diffusion MRI ; Humans ; Infant ; Infant, Newborn ; Magnetic Resonance Imaging ; Neuroimaging ; Original Research ; Tractography ; Vision</subject><ispartof>Developmental cognitive neuroscience, 2022-12, Vol.58, p.101179, Article 101179</ispartof><rights>2023 The Authors</rights><rights>Copyright © 2022. Published by Elsevier Ltd.</rights><rights>2022 Published by Elsevier Ltd. 2022</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c517t-21455b561159b3eef2c80e9d73ff1845da8a4cae9330611e51090f67e123e7073</citedby><cites>FETCH-LOGICAL-c517t-21455b561159b3eef2c80e9d73ff1845da8a4cae9330611e51090f67e123e7073</cites><orcidid>0000-0002-4303-3537</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC9768242/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.sciencedirect.com/science/article/pii/S1878929322001220$$EHTML$$P50$$Gelsevier$$Hfree_for_read</linktohtml><link.rule.ids>230,314,724,777,781,882,3536,27905,27906,45761,53772,53774</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/36521345$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Cabral, Laura</creatorcontrib><creatorcontrib>Zubiaurre-Elorza, Leire</creatorcontrib><creatorcontrib>Wild, Conor J.</creatorcontrib><creatorcontrib>Linke, Annika</creatorcontrib><creatorcontrib>Cusack, Rhodri</creatorcontrib><title>Anatomical correlates of category-selective visual regions have distinctive signatures of connectivity in neonates</title><title>Developmental cognitive neuroscience</title><addtitle>Dev Cogn Neurosci</addtitle><description>The ventral visual stream is shaped during development by innate proto-organization within the visual system, such as the strong input from the fovea to the fusiform face area. In adults, category-selective regions have distinct signatures of connectivity to brain regions beyond the visual system, likely reflecting cross-modal and motoric associations. We tested if this long-range connectivity is part of the innate proto-organization, or if it develops with postnatal experience, by using diffusion-weighted imaging to characterize the connectivity of anatomical correlates of category-selective regions in neonates (N = 445), 1–9 month old infants (N = 11), and adults (N = 14). Using the HCP data we identified face- and place- selective regions and a third intermediate region with a distinct profile of selectivity. Using linear classifiers, these regions were found to have distinctive connectivity at birth, to other regions in the visual system and to those outside of it. The results support an extended proto-organization that includes long-range connectivity that shapes, and is shaped by, experience-dependent development.
•Anatomical correlates of neonate category-selective regions had mature signatures of structural connectivity.•As identified with linear discriminant classifiers, face networks developed early and experienced the least change.•Long-range connections to distal regions are part of the innate proto-organization.•Category-selective regions were identified by connectivity to the visual system, replicating past proto-organizations.</description><subject>Adult</subject><subject>Brain</subject><subject>Brain Mapping</subject><subject>Classification</subject><subject>Diffusion Magnetic Resonance Imaging</subject><subject>Diffusion MRI</subject><subject>Humans</subject><subject>Infant</subject><subject>Infant, Newborn</subject><subject>Magnetic Resonance Imaging</subject><subject>Neuroimaging</subject><subject>Original Research</subject><subject>Tractography</subject><subject>Vision</subject><issn>1878-9293</issn><issn>1878-9307</issn><issn>1878-9307</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2022</creationdate><recordtype>article</recordtype><sourceid>DOA</sourceid><recordid>eNp9kUtv3CAUhVHVqonS_IBuKi-78ZSHMUaVKkVRH5EiddOuEYaLw8gDKeCR5t-XiSdRsgkb4N5zP9A5CH0keEMw6b9sN9aEDcWUHu9EyDfonAxiaCXD4u3jmUp2hi5z3uK6mOxpR9-jM9ZzSljHz1G6CrrEnTd6bkxMCWZdIDfRNaYeppgObYYZTPF7aPY-L1WXYPIx5OZO15r1ufiw9rOfKm1JJ0AM4WHQl0PjQxMghiP8A3rn9Jzh8rRfoL8_vv-5_tXe_v55c3112xpORGkp6TgfeU8IlyMDcNQMGKQVzDkydNzqQXdGg2QMVxFwgiV2vQBCGQgs2AW6Wbk26q26T36n00FF7dVDIaZJ6VS8mUGNHBsuBHZCkK7DTFvcS9ButI4wKl1lfVtZ98u4A2sglKTnF9CXneDv1BT3Sop-qJ5XwOcTIMV_C-Sidj4bmGddbVmyooJzLtiAuyolq9SkmHMC9_QMweoYvdqqGr06Rq_W6OvMp-f_e5p4DLoKvq4CqI7vPSSVjYdgwPpUQ6qW-Ffw_wHlYME5</recordid><startdate>20221201</startdate><enddate>20221201</enddate><creator>Cabral, Laura</creator><creator>Zubiaurre-Elorza, Leire</creator><creator>Wild, Conor J.</creator><creator>Linke, Annika</creator><creator>Cusack, Rhodri</creator><general>Elsevier Ltd</general><general>Elsevier</general><scope>6I.</scope><scope>AAFTH</scope><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>7X8</scope><scope>5PM</scope><scope>DOA</scope><orcidid>https://orcid.org/0000-0002-4303-3537</orcidid></search><sort><creationdate>20221201</creationdate><title>Anatomical correlates of category-selective visual regions have distinctive signatures of connectivity in neonates</title><author>Cabral, Laura ; Zubiaurre-Elorza, Leire ; Wild, Conor J. ; Linke, Annika ; Cusack, Rhodri</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c517t-21455b561159b3eef2c80e9d73ff1845da8a4cae9330611e51090f67e123e7073</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2022</creationdate><topic>Adult</topic><topic>Brain</topic><topic>Brain Mapping</topic><topic>Classification</topic><topic>Diffusion Magnetic Resonance Imaging</topic><topic>Diffusion MRI</topic><topic>Humans</topic><topic>Infant</topic><topic>Infant, Newborn</topic><topic>Magnetic Resonance Imaging</topic><topic>Neuroimaging</topic><topic>Original Research</topic><topic>Tractography</topic><topic>Vision</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Cabral, Laura</creatorcontrib><creatorcontrib>Zubiaurre-Elorza, Leire</creatorcontrib><creatorcontrib>Wild, Conor J.</creatorcontrib><creatorcontrib>Linke, Annika</creatorcontrib><creatorcontrib>Cusack, Rhodri</creatorcontrib><collection>ScienceDirect Open Access Titles</collection><collection>Elsevier:ScienceDirect:Open Access</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>Developmental cognitive neuroscience</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Cabral, Laura</au><au>Zubiaurre-Elorza, Leire</au><au>Wild, Conor J.</au><au>Linke, Annika</au><au>Cusack, Rhodri</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Anatomical correlates of category-selective visual regions have distinctive signatures of connectivity in neonates</atitle><jtitle>Developmental cognitive neuroscience</jtitle><addtitle>Dev Cogn Neurosci</addtitle><date>2022-12-01</date><risdate>2022</risdate><volume>58</volume><spage>101179</spage><pages>101179-</pages><artnum>101179</artnum><issn>1878-9293</issn><issn>1878-9307</issn><eissn>1878-9307</eissn><abstract>The ventral visual stream is shaped during development by innate proto-organization within the visual system, such as the strong input from the fovea to the fusiform face area. In adults, category-selective regions have distinct signatures of connectivity to brain regions beyond the visual system, likely reflecting cross-modal and motoric associations. We tested if this long-range connectivity is part of the innate proto-organization, or if it develops with postnatal experience, by using diffusion-weighted imaging to characterize the connectivity of anatomical correlates of category-selective regions in neonates (N = 445), 1–9 month old infants (N = 11), and adults (N = 14). Using the HCP data we identified face- and place- selective regions and a third intermediate region with a distinct profile of selectivity. Using linear classifiers, these regions were found to have distinctive connectivity at birth, to other regions in the visual system and to those outside of it. The results support an extended proto-organization that includes long-range connectivity that shapes, and is shaped by, experience-dependent development.
•Anatomical correlates of neonate category-selective regions had mature signatures of structural connectivity.•As identified with linear discriminant classifiers, face networks developed early and experienced the least change.•Long-range connections to distal regions are part of the innate proto-organization.•Category-selective regions were identified by connectivity to the visual system, replicating past proto-organizations.</abstract><cop>Netherlands</cop><pub>Elsevier Ltd</pub><pmid>36521345</pmid><doi>10.1016/j.dcn.2022.101179</doi><orcidid>https://orcid.org/0000-0002-4303-3537</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Adult Brain Brain Mapping Classification Diffusion Magnetic Resonance Imaging Diffusion MRI Humans Infant Infant, Newborn Magnetic Resonance Imaging Neuroimaging Original Research Tractography Vision |
title | Anatomical correlates of category-selective visual regions have distinctive signatures of connectivity in neonates |
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