Neuronal properties of pyramidal cells in lateral prefrontal cortex of the aging rhesus monkey brain are associated with performance deficits on spatial working memory but not executive function
Age-related declines in cognitive abilities occur as early as middle-age in humans and rhesus monkeys. Specifically, performance by aged individuals on tasks of executive function (EF) and working memory (WM) is characterized by greater frequency of errors, shorter memory spans, increased frequency...
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description | Age-related declines in cognitive abilities occur as early as middle-age in humans and rhesus monkeys. Specifically, performance by aged individuals on tasks of executive function (EF) and working memory (WM) is characterized by greater frequency of errors, shorter memory spans, increased frequency of perseverative responses, impaired use of feedback and reduced speed of processing. However, how aging precisely differentially impacts specific aspects of these cognitive functions and the distinct brain areas mediating cognition are not well understood. The prefrontal cortex (PFC) is known to mediate EF and WM and is an area that shows a vulnerability to age-related alterations in neuronal morphology. In the current study, we show that performance on EF and WM tasks exhibited significant changes with age, and these impairments correlate with changes in biophysical properties of layer 3 (L3) pyramidal neurons in lateral LPFC (LPFC). Specifically, there was a significant age-related increase in excitability of L3 LPFC pyramidal neurons, consistent with previous studies. Further, this age-related hyperexcitability of LPFC neurons was significantly correlated with age-related decline on a task of WM, but not an EF task. The current study characterizes age-related performance on tasks of WM and EF and provides insight into the neural substrates that may underlie changes in both WM and EF with age. |
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Specifically, performance by aged individuals on tasks of executive function (EF) and working memory (WM) is characterized by greater frequency of errors, shorter memory spans, increased frequency of perseverative responses, impaired use of feedback and reduced speed of processing. However, how aging precisely differentially impacts specific aspects of these cognitive functions and the distinct brain areas mediating cognition are not well understood. The prefrontal cortex (PFC) is known to mediate EF and WM and is an area that shows a vulnerability to age-related alterations in neuronal morphology. In the current study, we show that performance on EF and WM tasks exhibited significant changes with age, and these impairments correlate with changes in biophysical properties of layer 3 (L3) pyramidal neurons in lateral LPFC (LPFC). Specifically, there was a significant age-related increase in excitability of L3 LPFC pyramidal neurons, consistent with previous studies. Further, this age-related hyperexcitability of LPFC neurons was significantly correlated with age-related decline on a task of WM, but not an EF task. The current study characterizes age-related performance on tasks of WM and EF and provides insight into the neural substrates that may underlie changes in both WM and EF with age.</description><identifier>ISSN: 2509-2723</identifier><identifier>ISSN: 2509-2715</identifier><identifier>EISSN: 2509-2723</identifier><identifier>DOI: 10.1007/s11357-023-00798-2</identifier><identifier>PMID: 37106282</identifier><language>eng</language><publisher>Cham: Springer International Publishing</publisher><subject>Age ; Aged ; Aging ; Animals ; Biomedical and Life Sciences ; Cell Biology ; Cognitive ability ; Excitability ; Executive function ; Geriatrics/Gerontology ; Humans ; Life Sciences ; Macaca mulatta ; Memory ; Memory, Short-Term - physiology ; Molecular Medicine ; Neurons ; Original ; Original Article ; Prefrontal Cortex ; Pyramidal cells ; Pyramidal Cells - physiology ; Short term memory ; Spatial memory</subject><ispartof>GeroScience, 2023-06, Vol.45 (3), p.1317-1342</ispartof><rights>The Author(s), under exclusive licence to American Aging Association 2023. Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.</rights><rights>2023. The Author(s), under exclusive licence to American Aging Association.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c475t-dc118d9ec360a7809c5178d727e7ff402e21281248291f1f11ac068468570e5f3</citedby><cites>FETCH-LOGICAL-c475t-dc118d9ec360a7809c5178d727e7ff402e21281248291f1f11ac068468570e5f3</cites><orcidid>0000-0003-3869-3837</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/PMC10400510/pdf/$$EPDF$$P50$$Gpubmedcentral$$H</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC10400510/$$EHTML$$P50$$Gpubmedcentral$$H</linktohtml><link.rule.ids>230,315,729,782,786,887,27931,27932,41495,42564,51326,53798,53800</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/37106282$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Moore, Tara L.</creatorcontrib><creatorcontrib>Medalla, Maria</creatorcontrib><creatorcontrib>Ibañez, Sara</creatorcontrib><creatorcontrib>Wimmer, Klaus</creatorcontrib><creatorcontrib>Mojica, Chromewell A.</creatorcontrib><creatorcontrib>Killiany, Ronald J.</creatorcontrib><creatorcontrib>Moss, Mark B.</creatorcontrib><creatorcontrib>Luebke, Jennifer I.</creatorcontrib><creatorcontrib>Rosene, Douglas L.</creatorcontrib><title>Neuronal properties of pyramidal cells in lateral prefrontal cortex of the aging rhesus monkey brain are associated with performance deficits on spatial working memory but not executive function</title><title>GeroScience</title><addtitle>GeroScience</addtitle><addtitle>Geroscience</addtitle><description>Age-related declines in cognitive abilities occur as early as middle-age in humans and rhesus monkeys. 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The current study characterizes age-related performance on tasks of WM and EF and provides insight into the neural substrates that may underlie changes in both WM and EF with age.</description><subject>Age</subject><subject>Aged</subject><subject>Aging</subject><subject>Animals</subject><subject>Biomedical and Life Sciences</subject><subject>Cell Biology</subject><subject>Cognitive ability</subject><subject>Excitability</subject><subject>Executive function</subject><subject>Geriatrics/Gerontology</subject><subject>Humans</subject><subject>Life Sciences</subject><subject>Macaca mulatta</subject><subject>Memory</subject><subject>Memory, Short-Term - physiology</subject><subject>Molecular Medicine</subject><subject>Neurons</subject><subject>Original</subject><subject>Original Article</subject><subject>Prefrontal Cortex</subject><subject>Pyramidal cells</subject><subject>Pyramidal Cells - physiology</subject><subject>Short term memory</subject><subject>Spatial memory</subject><issn>2509-2723</issn><issn>2509-2715</issn><issn>2509-2723</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2023</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp9ks1u1TAQhSMEolXpC7BAltiwCYydHzsrhCpokSrYwNpyncm9bhM72E7b-3o8GZPeUgoLZEtOPN-csT2nKF5yeMsB5LvEedXIEkRV0m-nSvGkOBQNdKWQonr66PugOE7pEgC4bNsK4HlxUEkOrVDisPj5BZcYvBnZHMOMMTtMLAxs3kUzuZ72LY5jYs6z0WSMdyAOlJLXWIgZb1c-b5GZjfMbFreYlsSm4K9wxy6ioVQTKZpSsI40enbj8pZRsSHEyXiLrMfBWZepsmdpNtmR9k2IV6vehFOIJLRk5kNmeIt2ye4a2bB4m13wL4pngxkTHt-vR8X3Tx-_nZyV519PP598OC9tLZtc9pZz1XdoqxaMVNDZhkvVSyFRDkMNAgUXiotaiY4PNLix0Kq6VY0EbIbqqHi_152Xiwl7iz7Tc-g5usnEnQ7G6b8j3m31JlxrDjVAw4EU3twrxPBjwZT15NL6vsZjWJIWijrJBZcr-vof9DIskfq0UnXTVh1NosSesjGkRH15OA0HvdpE722iySb6ziZaUNKrx_d4SPltCgKqPZAo5DcY_9T-j-wvJjjNPw</recordid><startdate>20230601</startdate><enddate>20230601</enddate><creator>Moore, Tara L.</creator><creator>Medalla, Maria</creator><creator>Ibañez, Sara</creator><creator>Wimmer, Klaus</creator><creator>Mojica, Chromewell A.</creator><creator>Killiany, Ronald J.</creator><creator>Moss, Mark B.</creator><creator>Luebke, Jennifer I.</creator><creator>Rosene, Douglas L.</creator><general>Springer International Publishing</general><general>Springer Nature B.V</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>7QG</scope><scope>7T5</scope><scope>7TK</scope><scope>7TM</scope><scope>H94</scope><scope>K9.</scope><scope>NAPCQ</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0003-3869-3837</orcidid></search><sort><creationdate>20230601</creationdate><title>Neuronal properties of pyramidal cells in lateral prefrontal cortex of the aging rhesus monkey brain are associated with performance deficits on spatial working memory but not executive function</title><author>Moore, Tara L. ; 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subjects | Age Aged Aging Animals Biomedical and Life Sciences Cell Biology Cognitive ability Excitability Executive function Geriatrics/Gerontology Humans Life Sciences Macaca mulatta Memory Memory, Short-Term - physiology Molecular Medicine Neurons Original Original Article Prefrontal Cortex Pyramidal cells Pyramidal Cells - physiology Short term memory Spatial memory |
title | Neuronal properties of pyramidal cells in lateral prefrontal cortex of the aging rhesus monkey brain are associated with performance deficits on spatial working memory but not executive function |
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