Enhanced generalization and specialization of brain representations of semantic knowledge in healthy aging

Aging is often associated with a decrease in cognitive capacities. However, semantic memory appears relatively well preserved in healthy aging. Both behavioral and neuroimaging studies support the view that changes in brain networks contribute to this preservation of semantic cognition. However, lit...

Ausführliche Beschreibung

Gespeichert in:
Bibliographische Detailangaben
Veröffentlicht in:Neuropsychologia 2024-11, Vol.204, p.108999, Article 108999
Hauptverfasser: Margolles, Pedro, Soto, David
Format: Artikel
Sprache:eng
Schlagworte:
Online-Zugang:Volltext
Tags: Tag hinzufügen
Keine Tags, Fügen Sie den ersten Tag hinzu!
container_end_page
container_issue
container_start_page 108999
container_title Neuropsychologia
container_volume 204
creator Margolles, Pedro
Soto, David
description Aging is often associated with a decrease in cognitive capacities. However, semantic memory appears relatively well preserved in healthy aging. Both behavioral and neuroimaging studies support the view that changes in brain networks contribute to this preservation of semantic cognition. However, little is known about the role of healthy aging in the brain representation of semantic categories. Here we used pattern classification analyses and computational models to examine the neural representations of living and non-living word concepts. The results demonstrate that brain representations of animacy in healthy aging exhibit increased similarity across categories, even across different task contexts. This pattern of results aligns with the neural dedifferentiation hypothesis that proposes that aging is associated with decreased specificity in brain activity patterns and less efficient neural resource allocation. However, the loss in neural specificity for different categories was accompanied by increased dissimilarity of item-based conceptual representations within each category. Taken together, the age-related patterns of increased generalization and specialization in the brain representations of semantic knowledge may reflect a compensatory mechanism that enables a more efficient coding scheme characterized by both compression and sparsity, thereby helping to optimize the limited neural resources and maintain semantic processing in the healthy aging brain. •Functional MRI coupled with machine learning and computational modeling examine how aging shapes the neural representations of semantic knowledge.•Brain representations of different semantic categories exhibit increased similarity with ageing, even across different task contexts.•The loss in neural specificity for different semantic categories is accompanied by enhanced distinctiveness of examplar-based conceptual representations.•The enhanced generalization and specialization may reflect a compensatory mechanism to maintain semantic processing in aging.
doi_str_mv 10.1016/j.neuropsychologia.2024.108999
format Article
fullrecord <record><control><sourceid>proquest_cross</sourceid><recordid>TN_cdi_proquest_miscellaneous_3104038829</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><els_id>S0028393224002148</els_id><sourcerecordid>3104038829</sourcerecordid><originalsourceid>FETCH-LOGICAL-c261t-43782f2e52a15672bb2c6c8be3f50afece604d54c4ebba3fee82c9548be124ee3</originalsourceid><addsrcrecordid>eNqNkE1Lw0AQhhdRbK3-BclJvKTuZ7q5CFKqFQpe9LxsNpN0a7obd1Ol_npT6wd48jTwzjMzzIPQBcFjgkl2tRo72ATfxq1Z-sbXVo8pprxvyjzPD9CQyAlLmSD8EA0xpjJlOaMDdBLjCmPMBZXHaMBymolMsCFazdxSOwNlUoODoBv7rjvrXaJdmcQWjP2NfJUUQVuXBGgDRHDdZx53jQhr7Tprkmfn3xooa0h6cAm66ZbbRNfW1afoqNJNhLOvOkJPt7PH6TxdPNzdT28WqaEZ6VLOJpJWFATVRGQTWhTUZEYWwCqBdQUGMsxLwQ2HotCsApDU5IL3BKEcgI3Q5X5vG_zLBmKn1jYaaBrtwG-iYgRzzKSkeY9e71ETfIwBKtUGu9ZhqwhWO99qpf76Vjvfau-7X3D-dWtTrKH8Gf8W3APzPQD9x68WgorGwk64DWA6VXr731sfARafqw</addsrcrecordid><sourcetype>Aggregation Database</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>3104038829</pqid></control><display><type>article</type><title>Enhanced generalization and specialization of brain representations of semantic knowledge in healthy aging</title><source>MEDLINE</source><source>Elsevier ScienceDirect Journals</source><creator>Margolles, Pedro ; Soto, David</creator><creatorcontrib>Margolles, Pedro ; Soto, David</creatorcontrib><description>Aging is often associated with a decrease in cognitive capacities. However, semantic memory appears relatively well preserved in healthy aging. Both behavioral and neuroimaging studies support the view that changes in brain networks contribute to this preservation of semantic cognition. However, little is known about the role of healthy aging in the brain representation of semantic categories. Here we used pattern classification analyses and computational models to examine the neural representations of living and non-living word concepts. The results demonstrate that brain representations of animacy in healthy aging exhibit increased similarity across categories, even across different task contexts. This pattern of results aligns with the neural dedifferentiation hypothesis that proposes that aging is associated with decreased specificity in brain activity patterns and less efficient neural resource allocation. However, the loss in neural specificity for different categories was accompanied by increased dissimilarity of item-based conceptual representations within each category. Taken together, the age-related patterns of increased generalization and specialization in the brain representations of semantic knowledge may reflect a compensatory mechanism that enables a more efficient coding scheme characterized by both compression and sparsity, thereby helping to optimize the limited neural resources and maintain semantic processing in the healthy aging brain. •Functional MRI coupled with machine learning and computational modeling examine how aging shapes the neural representations of semantic knowledge.•Brain representations of different semantic categories exhibit increased similarity with ageing, even across different task contexts.•The loss in neural specificity for different semantic categories is accompanied by enhanced distinctiveness of examplar-based conceptual representations.•The enhanced generalization and specialization may reflect a compensatory mechanism to maintain semantic processing in aging.</description><identifier>ISSN: 0028-3932</identifier><identifier>ISSN: 1873-3514</identifier><identifier>EISSN: 1873-3514</identifier><identifier>DOI: 10.1016/j.neuropsychologia.2024.108999</identifier><identifier>PMID: 39265653</identifier><language>eng</language><publisher>England: Elsevier Ltd</publisher><subject>Adult ; Aged ; Aged, 80 and over ; Aging ; Aging - physiology ; Brain - diagnostic imaging ; Brain - physiology ; Brain Mapping ; Decoding ; Female ; Generalization, Psychological - physiology ; Healthy Aging - physiology ; Healthy Aging - psychology ; Humans ; Magnetic Resonance Imaging ; Male ; Middle Aged ; MVPA ; Neural dedifferentiation ; RSA ; Semantic memory ; Semantic representation ; Semantics ; Young Adult</subject><ispartof>Neuropsychologia, 2024-11, Vol.204, p.108999, Article 108999</ispartof><rights>2024 Elsevier Ltd</rights><rights>Copyright © 2024 Elsevier Ltd. All rights reserved.</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c261t-43782f2e52a15672bb2c6c8be3f50afece604d54c4ebba3fee82c9548be124ee3</cites><orcidid>0000-0003-0205-7513</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://www.sciencedirect.com/science/article/pii/S0028393224002148$$EHTML$$P50$$Gelsevier$$H</linktohtml><link.rule.ids>314,776,780,3536,27903,27904,65309</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/39265653$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Margolles, Pedro</creatorcontrib><creatorcontrib>Soto, David</creatorcontrib><title>Enhanced generalization and specialization of brain representations of semantic knowledge in healthy aging</title><title>Neuropsychologia</title><addtitle>Neuropsychologia</addtitle><description>Aging is often associated with a decrease in cognitive capacities. However, semantic memory appears relatively well preserved in healthy aging. Both behavioral and neuroimaging studies support the view that changes in brain networks contribute to this preservation of semantic cognition. However, little is known about the role of healthy aging in the brain representation of semantic categories. Here we used pattern classification analyses and computational models to examine the neural representations of living and non-living word concepts. The results demonstrate that brain representations of animacy in healthy aging exhibit increased similarity across categories, even across different task contexts. This pattern of results aligns with the neural dedifferentiation hypothesis that proposes that aging is associated with decreased specificity in brain activity patterns and less efficient neural resource allocation. However, the loss in neural specificity for different categories was accompanied by increased dissimilarity of item-based conceptual representations within each category. Taken together, the age-related patterns of increased generalization and specialization in the brain representations of semantic knowledge may reflect a compensatory mechanism that enables a more efficient coding scheme characterized by both compression and sparsity, thereby helping to optimize the limited neural resources and maintain semantic processing in the healthy aging brain. •Functional MRI coupled with machine learning and computational modeling examine how aging shapes the neural representations of semantic knowledge.•Brain representations of different semantic categories exhibit increased similarity with ageing, even across different task contexts.•The loss in neural specificity for different semantic categories is accompanied by enhanced distinctiveness of examplar-based conceptual representations.•The enhanced generalization and specialization may reflect a compensatory mechanism to maintain semantic processing in aging.</description><subject>Adult</subject><subject>Aged</subject><subject>Aged, 80 and over</subject><subject>Aging</subject><subject>Aging - physiology</subject><subject>Brain - diagnostic imaging</subject><subject>Brain - physiology</subject><subject>Brain Mapping</subject><subject>Decoding</subject><subject>Female</subject><subject>Generalization, Psychological - physiology</subject><subject>Healthy Aging - physiology</subject><subject>Healthy Aging - psychology</subject><subject>Humans</subject><subject>Magnetic Resonance Imaging</subject><subject>Male</subject><subject>Middle Aged</subject><subject>MVPA</subject><subject>Neural dedifferentiation</subject><subject>RSA</subject><subject>Semantic memory</subject><subject>Semantic representation</subject><subject>Semantics</subject><subject>Young Adult</subject><issn>0028-3932</issn><issn>1873-3514</issn><issn>1873-3514</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqNkE1Lw0AQhhdRbK3-BclJvKTuZ7q5CFKqFQpe9LxsNpN0a7obd1Ol_npT6wd48jTwzjMzzIPQBcFjgkl2tRo72ATfxq1Z-sbXVo8pprxvyjzPD9CQyAlLmSD8EA0xpjJlOaMDdBLjCmPMBZXHaMBymolMsCFazdxSOwNlUoODoBv7rjvrXaJdmcQWjP2NfJUUQVuXBGgDRHDdZx53jQhr7Tprkmfn3xooa0h6cAm66ZbbRNfW1afoqNJNhLOvOkJPt7PH6TxdPNzdT28WqaEZ6VLOJpJWFATVRGQTWhTUZEYWwCqBdQUGMsxLwQ2HotCsApDU5IL3BKEcgI3Q5X5vG_zLBmKn1jYaaBrtwG-iYgRzzKSkeY9e71ETfIwBKtUGu9ZhqwhWO99qpf76Vjvfau-7X3D-dWtTrKH8Gf8W3APzPQD9x68WgorGwk64DWA6VXr731sfARafqw</recordid><startdate>20241105</startdate><enddate>20241105</enddate><creator>Margolles, Pedro</creator><creator>Soto, David</creator><general>Elsevier Ltd</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>7X8</scope><orcidid>https://orcid.org/0000-0003-0205-7513</orcidid></search><sort><creationdate>20241105</creationdate><title>Enhanced generalization and specialization of brain representations of semantic knowledge in healthy aging</title><author>Margolles, Pedro ; Soto, David</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c261t-43782f2e52a15672bb2c6c8be3f50afece604d54c4ebba3fee82c9548be124ee3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2024</creationdate><topic>Adult</topic><topic>Aged</topic><topic>Aged, 80 and over</topic><topic>Aging</topic><topic>Aging - physiology</topic><topic>Brain - diagnostic imaging</topic><topic>Brain - physiology</topic><topic>Brain Mapping</topic><topic>Decoding</topic><topic>Female</topic><topic>Generalization, Psychological - physiology</topic><topic>Healthy Aging - physiology</topic><topic>Healthy Aging - psychology</topic><topic>Humans</topic><topic>Magnetic Resonance Imaging</topic><topic>Male</topic><topic>Middle Aged</topic><topic>MVPA</topic><topic>Neural dedifferentiation</topic><topic>RSA</topic><topic>Semantic memory</topic><topic>Semantic representation</topic><topic>Semantics</topic><topic>Young Adult</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Margolles, Pedro</creatorcontrib><creatorcontrib>Soto, David</creatorcontrib><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><jtitle>Neuropsychologia</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Margolles, Pedro</au><au>Soto, David</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Enhanced generalization and specialization of brain representations of semantic knowledge in healthy aging</atitle><jtitle>Neuropsychologia</jtitle><addtitle>Neuropsychologia</addtitle><date>2024-11-05</date><risdate>2024</risdate><volume>204</volume><spage>108999</spage><pages>108999-</pages><artnum>108999</artnum><issn>0028-3932</issn><issn>1873-3514</issn><eissn>1873-3514</eissn><abstract>Aging is often associated with a decrease in cognitive capacities. However, semantic memory appears relatively well preserved in healthy aging. Both behavioral and neuroimaging studies support the view that changes in brain networks contribute to this preservation of semantic cognition. However, little is known about the role of healthy aging in the brain representation of semantic categories. Here we used pattern classification analyses and computational models to examine the neural representations of living and non-living word concepts. The results demonstrate that brain representations of animacy in healthy aging exhibit increased similarity across categories, even across different task contexts. This pattern of results aligns with the neural dedifferentiation hypothesis that proposes that aging is associated with decreased specificity in brain activity patterns and less efficient neural resource allocation. However, the loss in neural specificity for different categories was accompanied by increased dissimilarity of item-based conceptual representations within each category. Taken together, the age-related patterns of increased generalization and specialization in the brain representations of semantic knowledge may reflect a compensatory mechanism that enables a more efficient coding scheme characterized by both compression and sparsity, thereby helping to optimize the limited neural resources and maintain semantic processing in the healthy aging brain. •Functional MRI coupled with machine learning and computational modeling examine how aging shapes the neural representations of semantic knowledge.•Brain representations of different semantic categories exhibit increased similarity with ageing, even across different task contexts.•The loss in neural specificity for different semantic categories is accompanied by enhanced distinctiveness of examplar-based conceptual representations.•The enhanced generalization and specialization may reflect a compensatory mechanism to maintain semantic processing in aging.</abstract><cop>England</cop><pub>Elsevier Ltd</pub><pmid>39265653</pmid><doi>10.1016/j.neuropsychologia.2024.108999</doi><orcidid>https://orcid.org/0000-0003-0205-7513</orcidid></addata></record>
fulltext fulltext
identifier ISSN: 0028-3932
ispartof Neuropsychologia, 2024-11, Vol.204, p.108999, Article 108999
issn 0028-3932
1873-3514
1873-3514
language eng
recordid cdi_proquest_miscellaneous_3104038829
source MEDLINE; Elsevier ScienceDirect Journals
subjects Adult
Aged
Aged, 80 and over
Aging
Aging - physiology
Brain - diagnostic imaging
Brain - physiology
Brain Mapping
Decoding
Female
Generalization, Psychological - physiology
Healthy Aging - physiology
Healthy Aging - psychology
Humans
Magnetic Resonance Imaging
Male
Middle Aged
MVPA
Neural dedifferentiation
RSA
Semantic memory
Semantic representation
Semantics
Young Adult
title Enhanced generalization and specialization of brain representations of semantic knowledge in healthy aging
url https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-01-25T02%3A28%3A59IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-proquest_cross&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Enhanced%20generalization%20and%20specialization%20of%20brain%20representations%20of%20semantic%20knowledge%20in%20healthy%20aging&rft.jtitle=Neuropsychologia&rft.au=Margolles,%20Pedro&rft.date=2024-11-05&rft.volume=204&rft.spage=108999&rft.pages=108999-&rft.artnum=108999&rft.issn=0028-3932&rft.eissn=1873-3514&rft_id=info:doi/10.1016/j.neuropsychologia.2024.108999&rft_dat=%3Cproquest_cross%3E3104038829%3C/proquest_cross%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=3104038829&rft_id=info:pmid/39265653&rft_els_id=S0028393224002148&rfr_iscdi=true