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...
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Veröffentlicht in: | Neuropsychologia 2024-11, Vol.204, p.108999, Article 108999 |
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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 |
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•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> |
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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 |
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