Integrity of Neuronal Size in the Entorhinal Cortex Is a Biological Substrate of Exceptional Cognitive Aging
Average aging is associated with a gradual decline of memory capacity. SuperAgers are humans ≥80 years of age who show exceptional episodic memory at least as good as individuals 20-30 years their junior. This study investigated whether neuronal integrity in the entorhinal cortex (ERC), an area crit...
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creator | Nassif, Caren Kawles, Allegra Ayala, Ivan Minogue, Grace Gill, Nathan P Shepard, Robert A Zouridakis, Antonia Keszycki, Rachel Zhang, Hui Mao, Qinwen Flanagan, Margaret E Bigio, Eileen H Mesulam, M-Marsel Rogalski, Emily Geula, Changiz Gefen, Tamar |
description | Average aging is associated with a gradual decline of memory capacity. SuperAgers are humans ≥80 years of age who show exceptional episodic memory at least as good as individuals 20-30 years their junior. This study investigated whether neuronal integrity in the entorhinal cortex (ERC), an area critical for memory and selectively vulnerable to neurofibrillary degeneration, differentiated SuperAgers from cognitively healthy younger individuals, cognitively average peers ("Normal Elderly"), and individuals with amnestic mild cognitive impairment. Postmortem sections of the ERC were stained with cresyl violet to visualize neurons and immunostained with mouse monoclonal antibody PHF-1 to visualize neurofibrillary tangles. The cross-sectional area (i.e., size) of layer II and layer III/V ERC neurons were quantified. Two-thirds of total participants were female. Unbiased stereology was used to quantitate tangles in a subgroup of SuperAgers and Normal Elderly. Linear mixed-effect models were used to determine differences across groups. Quantitative measurements found that the soma size of layer II ERC neurons in postmortem brain specimens were significantly larger in SuperAgers compared with all groups (
< 0.05)-including younger individuals 20-30 years their junior (
< 0.005). SuperAgers had significantly fewer stereologically quantified Alzheimer's disease-related neurofibrillary tangles in layer II ERC than Normal Elderly (
< 0.05). This difference in tangle burden in layer II between SuperAgers and Normal Elderly suggests that tangle-bearing neurons may be prone to shrinkage during aging. The finding that SuperAgers show ERC layer II neurons that are substantially larger even compared with individuals 20-30 years younger is remarkable, suggesting that layer II ERC integrity is a biological substrate of exceptional memory in old age.
Average aging is associated with a gradual decline of memory. Previous research shows that an area critical for memory, the entorhinal cortex (ERC), is susceptible to the early formation of Alzheimer's disease neuropathology, even during average (or typical) trajectories of aging. The Northwestern University SuperAging Research Program studies unique individuals known as SuperAgers, individuals ≥80 years old who show exceptional memory that is at least as good as individuals 20-30 years their junior. In this study, we show that SuperAgers harbor larger, healthier neurons in the ERC compared with their cognitively average same-aged |
doi_str_mv | 10.1523/JNEUROSCI.0679-22.2022 |
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< 0.05)-including younger individuals 20-30 years their junior (
< 0.005). SuperAgers had significantly fewer stereologically quantified Alzheimer's disease-related neurofibrillary tangles in layer II ERC than Normal Elderly (
< 0.05). This difference in tangle burden in layer II between SuperAgers and Normal Elderly suggests that tangle-bearing neurons may be prone to shrinkage during aging. The finding that SuperAgers show ERC layer II neurons that are substantially larger even compared with individuals 20-30 years younger is remarkable, suggesting that layer II ERC integrity is a biological substrate of exceptional memory in old age.
Average aging is associated with a gradual decline of memory. Previous research shows that an area critical for memory, the entorhinal cortex (ERC), is susceptible to the early formation of Alzheimer's disease neuropathology, even during average (or typical) trajectories of aging. The Northwestern University SuperAging Research Program studies unique individuals known as SuperAgers, individuals ≥80 years old who show exceptional memory that is at least as good as individuals 20-30 years their junior. In this study, we show that SuperAgers harbor larger, healthier neurons in the ERC compared with their cognitively average same-aged peers, those with amnestic mild cognitive impairment, and - remarkably - even compared with individuals 20-30 years younger. We conclude that larger ERC neurons are a biological signature of the SuperAging trajectory.</description><identifier>ISSN: 0270-6474</identifier><identifier>EISSN: 1529-2401</identifier><identifier>DOI: 10.1523/JNEUROSCI.0679-22.2022</identifier><identifier>PMID: 36180225</identifier><language>eng</language><publisher>United States: Society for Neuroscience</publisher><subject>Aged ; Aged, 80 and over ; Aging ; Alzheimer Disease - pathology ; Alzheimer's disease ; Animals ; Cognitive ability ; Cognitive Aging ; Cortex (entorhinal) ; Degeneration ; Entorhinal Cortex - pathology ; Female ; Geriatrics ; Humans ; Integrity ; Male ; Memory ; Mice ; Monoclonal antibodies ; Nervous system ; Neurodegeneration ; Neurodegenerative diseases ; Neurofibrillary tangles ; Neurofibrillary Tangles - pathology ; Neurons ; Neurons - pathology ; Neurosciences ; Older people ; Stereology ; Subgroups ; Substrates</subject><ispartof>The Journal of neuroscience, 2022-11, Vol.42 (45), p.8587-8594</ispartof><rights>Copyright © 2022 the authors.</rights><rights>Copyright Society for Neuroscience Nov 9, 2022</rights><rights>Copyright © 2022 the authors 2022</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c442t-9e51df4f32650a950f5a07b3245c217ee5d0327643c372cc1e2868d77365c0433</citedby><cites>FETCH-LOGICAL-c442t-9e51df4f32650a950f5a07b3245c217ee5d0327643c372cc1e2868d77365c0433</cites><orcidid>0000-0002-9311-3295</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/PMC9665923/pdf/$$EPDF$$P50$$Gpubmedcentral$$H</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC9665923/$$EHTML$$P50$$Gpubmedcentral$$H</linktohtml><link.rule.ids>230,314,727,780,784,885,27924,27925,53791,53793</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/36180225$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Nassif, Caren</creatorcontrib><creatorcontrib>Kawles, Allegra</creatorcontrib><creatorcontrib>Ayala, Ivan</creatorcontrib><creatorcontrib>Minogue, Grace</creatorcontrib><creatorcontrib>Gill, Nathan P</creatorcontrib><creatorcontrib>Shepard, Robert A</creatorcontrib><creatorcontrib>Zouridakis, Antonia</creatorcontrib><creatorcontrib>Keszycki, Rachel</creatorcontrib><creatorcontrib>Zhang, Hui</creatorcontrib><creatorcontrib>Mao, Qinwen</creatorcontrib><creatorcontrib>Flanagan, Margaret E</creatorcontrib><creatorcontrib>Bigio, Eileen H</creatorcontrib><creatorcontrib>Mesulam, M-Marsel</creatorcontrib><creatorcontrib>Rogalski, Emily</creatorcontrib><creatorcontrib>Geula, Changiz</creatorcontrib><creatorcontrib>Gefen, Tamar</creatorcontrib><title>Integrity of Neuronal Size in the Entorhinal Cortex Is a Biological Substrate of Exceptional Cognitive Aging</title><title>The Journal of neuroscience</title><addtitle>J Neurosci</addtitle><description>Average aging is associated with a gradual decline of memory capacity. SuperAgers are humans ≥80 years of age who show exceptional episodic memory at least as good as individuals 20-30 years their junior. This study investigated whether neuronal integrity in the entorhinal cortex (ERC), an area critical for memory and selectively vulnerable to neurofibrillary degeneration, differentiated SuperAgers from cognitively healthy younger individuals, cognitively average peers ("Normal Elderly"), and individuals with amnestic mild cognitive impairment. Postmortem sections of the ERC were stained with cresyl violet to visualize neurons and immunostained with mouse monoclonal antibody PHF-1 to visualize neurofibrillary tangles. The cross-sectional area (i.e., size) of layer II and layer III/V ERC neurons were quantified. Two-thirds of total participants were female. Unbiased stereology was used to quantitate tangles in a subgroup of SuperAgers and Normal Elderly. Linear mixed-effect models were used to determine differences across groups. Quantitative measurements found that the soma size of layer II ERC neurons in postmortem brain specimens were significantly larger in SuperAgers compared with all groups (
< 0.05)-including younger individuals 20-30 years their junior (
< 0.005). SuperAgers had significantly fewer stereologically quantified Alzheimer's disease-related neurofibrillary tangles in layer II ERC than Normal Elderly (
< 0.05). This difference in tangle burden in layer II between SuperAgers and Normal Elderly suggests that tangle-bearing neurons may be prone to shrinkage during aging. The finding that SuperAgers show ERC layer II neurons that are substantially larger even compared with individuals 20-30 years younger is remarkable, suggesting that layer II ERC integrity is a biological substrate of exceptional memory in old age.
Average aging is associated with a gradual decline of memory. Previous research shows that an area critical for memory, the entorhinal cortex (ERC), is susceptible to the early formation of Alzheimer's disease neuropathology, even during average (or typical) trajectories of aging. The Northwestern University SuperAging Research Program studies unique individuals known as SuperAgers, individuals ≥80 years old who show exceptional memory that is at least as good as individuals 20-30 years their junior. In this study, we show that SuperAgers harbor larger, healthier neurons in the ERC compared with their cognitively average same-aged peers, those with amnestic mild cognitive impairment, and - remarkably - even compared with individuals 20-30 years younger. We conclude that larger ERC neurons are a biological signature of the SuperAging trajectory.</description><subject>Aged</subject><subject>Aged, 80 and over</subject><subject>Aging</subject><subject>Alzheimer Disease - pathology</subject><subject>Alzheimer's disease</subject><subject>Animals</subject><subject>Cognitive ability</subject><subject>Cognitive Aging</subject><subject>Cortex (entorhinal)</subject><subject>Degeneration</subject><subject>Entorhinal Cortex - pathology</subject><subject>Female</subject><subject>Geriatrics</subject><subject>Humans</subject><subject>Integrity</subject><subject>Male</subject><subject>Memory</subject><subject>Mice</subject><subject>Monoclonal antibodies</subject><subject>Nervous system</subject><subject>Neurodegeneration</subject><subject>Neurodegenerative diseases</subject><subject>Neurofibrillary tangles</subject><subject>Neurofibrillary Tangles - pathology</subject><subject>Neurons</subject><subject>Neurons - pathology</subject><subject>Neurosciences</subject><subject>Older people</subject><subject>Stereology</subject><subject>Subgroups</subject><subject>Substrates</subject><issn>0270-6474</issn><issn>1529-2401</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2022</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNpdkU9vEzEQxS0EomnhK1SWuHDZYI__ZS9IJQo0VdVKlJ6tjTO7cbVZB9tbtXx6dkkb0Z5GM_Obpzd6hJxyNuUKxJeLq8Xtz-ub-XLKtCkLgCkwgDdkMmyHVjL-lkwYGFZoaeQROU7pjjFmGDfvyZHQfDbgakLaZZexiT4_0lDTK-xj6KqW3vg_SH1H8wbposshbvw4noeY8YEuE63oNx_a0Hg30v0q5VhlHDUWDw532Yc933Q--3ukZ43vmg_kXV21CT8-1RNy-33xa35eXF7_WM7PLgsnJeSiRMXXtawFaMWqUrFaVcysBEjlgBtEtWYCjJbCCQPOcYSZnq2NEVo5JoU4IV_3urt-tcW1w25w19pd9NsqPtpQefty0_mNbcK9LbVWJYwCn58EYvjdY8p265PDtq06DH2yYIBJmLFSD-inV-hd6OPw_EgJBYrDP0d6T7kYUopYH8xwZsdA7SFQOwZqAewY6HB4-v8rh7PnBMVfFjOdDA</recordid><startdate>20221109</startdate><enddate>20221109</enddate><creator>Nassif, Caren</creator><creator>Kawles, Allegra</creator><creator>Ayala, Ivan</creator><creator>Minogue, Grace</creator><creator>Gill, Nathan P</creator><creator>Shepard, Robert A</creator><creator>Zouridakis, Antonia</creator><creator>Keszycki, Rachel</creator><creator>Zhang, Hui</creator><creator>Mao, Qinwen</creator><creator>Flanagan, Margaret E</creator><creator>Bigio, Eileen H</creator><creator>Mesulam, M-Marsel</creator><creator>Rogalski, Emily</creator><creator>Geula, Changiz</creator><creator>Gefen, Tamar</creator><general>Society for Neuroscience</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>7QR</scope><scope>7TK</scope><scope>7U7</scope><scope>7U9</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>H94</scope><scope>P64</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0002-9311-3295</orcidid></search><sort><creationdate>20221109</creationdate><title>Integrity of Neuronal Size in the Entorhinal Cortex Is a Biological Substrate of Exceptional Cognitive Aging</title><author>Nassif, Caren ; Kawles, Allegra ; Ayala, Ivan ; Minogue, Grace ; Gill, Nathan P ; Shepard, Robert A ; Zouridakis, Antonia ; Keszycki, Rachel ; Zhang, Hui ; Mao, Qinwen ; Flanagan, Margaret E ; Bigio, Eileen H ; Mesulam, M-Marsel ; Rogalski, Emily ; Geula, Changiz ; Gefen, Tamar</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c442t-9e51df4f32650a950f5a07b3245c217ee5d0327643c372cc1e2868d77365c0433</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2022</creationdate><topic>Aged</topic><topic>Aged, 80 and over</topic><topic>Aging</topic><topic>Alzheimer Disease - pathology</topic><topic>Alzheimer's disease</topic><topic>Animals</topic><topic>Cognitive ability</topic><topic>Cognitive Aging</topic><topic>Cortex (entorhinal)</topic><topic>Degeneration</topic><topic>Entorhinal Cortex - pathology</topic><topic>Female</topic><topic>Geriatrics</topic><topic>Humans</topic><topic>Integrity</topic><topic>Male</topic><topic>Memory</topic><topic>Mice</topic><topic>Monoclonal antibodies</topic><topic>Nervous system</topic><topic>Neurodegeneration</topic><topic>Neurodegenerative diseases</topic><topic>Neurofibrillary tangles</topic><topic>Neurofibrillary Tangles - pathology</topic><topic>Neurons</topic><topic>Neurons - pathology</topic><topic>Neurosciences</topic><topic>Older people</topic><topic>Stereology</topic><topic>Subgroups</topic><topic>Substrates</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Nassif, Caren</creatorcontrib><creatorcontrib>Kawles, Allegra</creatorcontrib><creatorcontrib>Ayala, Ivan</creatorcontrib><creatorcontrib>Minogue, Grace</creatorcontrib><creatorcontrib>Gill, Nathan P</creatorcontrib><creatorcontrib>Shepard, Robert A</creatorcontrib><creatorcontrib>Zouridakis, Antonia</creatorcontrib><creatorcontrib>Keszycki, Rachel</creatorcontrib><creatorcontrib>Zhang, Hui</creatorcontrib><creatorcontrib>Mao, Qinwen</creatorcontrib><creatorcontrib>Flanagan, Margaret E</creatorcontrib><creatorcontrib>Bigio, Eileen H</creatorcontrib><creatorcontrib>Mesulam, M-Marsel</creatorcontrib><creatorcontrib>Rogalski, Emily</creatorcontrib><creatorcontrib>Geula, Changiz</creatorcontrib><creatorcontrib>Gefen, Tamar</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Animal Behavior Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>Toxicology Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Engineering Research Database</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>The Journal of neuroscience</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Nassif, Caren</au><au>Kawles, Allegra</au><au>Ayala, Ivan</au><au>Minogue, Grace</au><au>Gill, Nathan P</au><au>Shepard, Robert A</au><au>Zouridakis, Antonia</au><au>Keszycki, Rachel</au><au>Zhang, Hui</au><au>Mao, Qinwen</au><au>Flanagan, Margaret E</au><au>Bigio, Eileen H</au><au>Mesulam, M-Marsel</au><au>Rogalski, Emily</au><au>Geula, Changiz</au><au>Gefen, Tamar</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Integrity of Neuronal Size in the Entorhinal Cortex Is a Biological Substrate of Exceptional Cognitive Aging</atitle><jtitle>The Journal of neuroscience</jtitle><addtitle>J Neurosci</addtitle><date>2022-11-09</date><risdate>2022</risdate><volume>42</volume><issue>45</issue><spage>8587</spage><epage>8594</epage><pages>8587-8594</pages><issn>0270-6474</issn><eissn>1529-2401</eissn><abstract>Average aging is associated with a gradual decline of memory capacity. SuperAgers are humans ≥80 years of age who show exceptional episodic memory at least as good as individuals 20-30 years their junior. This study investigated whether neuronal integrity in the entorhinal cortex (ERC), an area critical for memory and selectively vulnerable to neurofibrillary degeneration, differentiated SuperAgers from cognitively healthy younger individuals, cognitively average peers ("Normal Elderly"), and individuals with amnestic mild cognitive impairment. Postmortem sections of the ERC were stained with cresyl violet to visualize neurons and immunostained with mouse monoclonal antibody PHF-1 to visualize neurofibrillary tangles. The cross-sectional area (i.e., size) of layer II and layer III/V ERC neurons were quantified. Two-thirds of total participants were female. Unbiased stereology was used to quantitate tangles in a subgroup of SuperAgers and Normal Elderly. Linear mixed-effect models were used to determine differences across groups. Quantitative measurements found that the soma size of layer II ERC neurons in postmortem brain specimens were significantly larger in SuperAgers compared with all groups (
< 0.05)-including younger individuals 20-30 years their junior (
< 0.005). SuperAgers had significantly fewer stereologically quantified Alzheimer's disease-related neurofibrillary tangles in layer II ERC than Normal Elderly (
< 0.05). This difference in tangle burden in layer II between SuperAgers and Normal Elderly suggests that tangle-bearing neurons may be prone to shrinkage during aging. The finding that SuperAgers show ERC layer II neurons that are substantially larger even compared with individuals 20-30 years younger is remarkable, suggesting that layer II ERC integrity is a biological substrate of exceptional memory in old age.
Average aging is associated with a gradual decline of memory. Previous research shows that an area critical for memory, the entorhinal cortex (ERC), is susceptible to the early formation of Alzheimer's disease neuropathology, even during average (or typical) trajectories of aging. The Northwestern University SuperAging Research Program studies unique individuals known as SuperAgers, individuals ≥80 years old who show exceptional memory that is at least as good as individuals 20-30 years their junior. In this study, we show that SuperAgers harbor larger, healthier neurons in the ERC compared with their cognitively average same-aged peers, those with amnestic mild cognitive impairment, and - remarkably - even compared with individuals 20-30 years younger. We conclude that larger ERC neurons are a biological signature of the SuperAging trajectory.</abstract><cop>United States</cop><pub>Society for Neuroscience</pub><pmid>36180225</pmid><doi>10.1523/JNEUROSCI.0679-22.2022</doi><tpages>8</tpages><orcidid>https://orcid.org/0000-0002-9311-3295</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Aged Aged, 80 and over Aging Alzheimer Disease - pathology Alzheimer's disease Animals Cognitive ability Cognitive Aging Cortex (entorhinal) Degeneration Entorhinal Cortex - pathology Female Geriatrics Humans Integrity Male Memory Mice Monoclonal antibodies Nervous system Neurodegeneration Neurodegenerative diseases Neurofibrillary tangles Neurofibrillary Tangles - pathology Neurons Neurons - pathology Neurosciences Older people Stereology Subgroups Substrates |
title | Integrity of Neuronal Size in the Entorhinal Cortex Is a Biological Substrate of Exceptional Cognitive Aging |
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