Sex‐dependent alterations in hippocampal connectivity are linked to cerebrovascular and amyloid pathologies in normal aging
INTRODUCTION Compared to males, females have an accelerated trajectory of cognitive decline in Alzheimer's disease (AD). The neurobiological factors underlying the more rapid cognitive decline in AD in females remain unclear. This study explored how sex‐dependent alterations in hippocampal conn...
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| Veröffentlicht in: | Alzheimer's & dementia 2024-02, Vol.20 (2), p.914-924 |
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| creator | Schweitzer, Noah Li, Jinghang Thurston, Rebecca C. Lopresti, Brian Klunk, William E. Snitz, Beth Tudorascu, Dana Cohen, Ann Kamboh, M. Ilyas Halligan‐Eddy, Edythe Iordanova, Bistra Villemagne, Victor L. Aizenstein, Howard Wu, Minjie |
| description | INTRODUCTION
Compared to males, females have an accelerated trajectory of cognitive decline in Alzheimer's disease (AD). The neurobiological factors underlying the more rapid cognitive decline in AD in females remain unclear. This study explored how sex‐dependent alterations in hippocampal connectivity over 2 years are associated with cerebrovascular and amyloid pathologies in normal aging.
METHODS
Thirty‐three females and 21 males 65 to 93 years of age with no cognitive impairment performed a face‐name associative memory functional magnetic resonance imaging (fMRI) task with a 2‐year follow‐up. We acquired baseline carbon 11‐labeled Pittsburgh compound B ([11C]PiB) positron emission tomography (PET) and T2‐weighted fluid‐attenuated inversion recovery (T2‐FLAIR) MRI to quantify amyloid β (Aβ) burden and white matter hyperintensity (WMH) volume, respectively.
RESULTS
Males had increased hippocampal‐prefrontal connectivity over 2 years, associated with greater Aβ burden. Females had increased bilateral hippocampal functional connectivity, associated with greater WMH volume.
DISCUSSION
These findings suggest sex‐dependent compensatory mechanisms in the memory network in the presence of cerebrovascular and AD pathologies and may explain the accelerated trajectory of cognitive decline in females. |
| doi_str_mv | 10.1002/alz.13503 |
| format | Article |
| fullrecord | <record><control><sourceid>proquest_pubme</sourceid><recordid>TN_cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_10916980</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><sourcerecordid>3089864325</sourcerecordid><originalsourceid>FETCH-LOGICAL-c4043-7fbf82a1a24ff1ab992432387301180b19d90e0eca3a6a53f8b247f25184b6a33</originalsourceid><addsrcrecordid>eNp1kc9qFEEQhwdRTIwefAFp8BIPm_Sf6Zmek4SgRljwEL14aWp6anY79nSP3TOrKwg-gs_ok6TNJosKnqqgPj5-xa8onjJ6wijlp-C-nTAhqbhXHDIp-ULyurm_3yt6UDxK6YrSkiomHxYHolasrip1WHy_xK-_fvzscETfoZ8IuAkjTDb4RKwnazuOwcAwgiMmeI9mshs7bQlEJM76T9iRKRCDEdsYNpDM7CAS8B2BYeuC7cgI0zq4sLJ4Y_QhDlkGK-tXj4sHPbiET27nUfHh9av35xeL5bs3b8_PlgtT0lIs6r7tFQcGvOx7Bm3T8FJwoWpBGVO0ZU3XUKRoQEAFUvSq5WXdc8lU2VYgxFHxcucd53bAzuRHIzg9RjtA3OoAVv998XatV2GjGW1Y1SiaDce3hhg-z5gmPdhk0DnwGOakuaqlkqKidUaf_4NehTn6_J8WVDWqytllpl7sKBNDShH7fRpG9e9WdW5V37Sa2Wd_xt-TdzVm4HQHfLEOt_836bPlx53yGhcrr7I</addsrcrecordid><sourcetype>Open Access Repository</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>3089864325</pqid></control><display><type>article</type><title>Sex‐dependent alterations in hippocampal connectivity are linked to cerebrovascular and amyloid pathologies in normal aging</title><source>MEDLINE</source><source>PubMed Central Open Access</source><source>Applied Social Sciences Index & Abstracts (ASSIA)</source><source>Wiley-Blackwell Open Access Titles</source><source>Wiley Online Library All Journals</source><source>PubMed Central</source><creator>Schweitzer, Noah ; Li, Jinghang ; Thurston, Rebecca C. ; Lopresti, Brian ; Klunk, William E. ; Snitz, Beth ; Tudorascu, Dana ; Cohen, Ann ; Kamboh, M. Ilyas ; Halligan‐Eddy, Edythe ; Iordanova, Bistra ; Villemagne, Victor L. ; Aizenstein, Howard ; Wu, Minjie</creator><creatorcontrib>Schweitzer, Noah ; Li, Jinghang ; Thurston, Rebecca C. ; Lopresti, Brian ; Klunk, William E. ; Snitz, Beth ; Tudorascu, Dana ; Cohen, Ann ; Kamboh, M. Ilyas ; Halligan‐Eddy, Edythe ; Iordanova, Bistra ; Villemagne, Victor L. ; Aizenstein, Howard ; Wu, Minjie</creatorcontrib><description>INTRODUCTION
Compared to males, females have an accelerated trajectory of cognitive decline in Alzheimer's disease (AD). The neurobiological factors underlying the more rapid cognitive decline in AD in females remain unclear. This study explored how sex‐dependent alterations in hippocampal connectivity over 2 years are associated with cerebrovascular and amyloid pathologies in normal aging.
METHODS
Thirty‐three females and 21 males 65 to 93 years of age with no cognitive impairment performed a face‐name associative memory functional magnetic resonance imaging (fMRI) task with a 2‐year follow‐up. We acquired baseline carbon 11‐labeled Pittsburgh compound B ([11C]PiB) positron emission tomography (PET) and T2‐weighted fluid‐attenuated inversion recovery (T2‐FLAIR) MRI to quantify amyloid β (Aβ) burden and white matter hyperintensity (WMH) volume, respectively.
RESULTS
Males had increased hippocampal‐prefrontal connectivity over 2 years, associated with greater Aβ burden. Females had increased bilateral hippocampal functional connectivity, associated with greater WMH volume.
DISCUSSION
These findings suggest sex‐dependent compensatory mechanisms in the memory network in the presence of cerebrovascular and AD pathologies and may explain the accelerated trajectory of cognitive decline in females.</description><identifier>ISSN: 1552-5260</identifier><identifier>ISSN: 1552-5279</identifier><identifier>EISSN: 1552-5279</identifier><identifier>DOI: 10.1002/alz.13503</identifier><identifier>PMID: 37817668</identifier><language>eng</language><publisher>United States: John Wiley & Sons, Inc</publisher><subject>Aging ; Alzheimer Disease - pathology ; Alzheimer's disease ; Amyloid ; amyloid beta ; Amyloid beta-Peptides - metabolism ; Associative memory ; Biomarkers ; Brain - pathology ; cerebral small vessel disease ; Cognition & reasoning ; Cognitive Dysfunction - pathology ; Cognitive impairment ; Female ; Females ; Functional connectivity ; Functional magnetic resonance imaging ; Gender differences ; hippocampal functional connectivity ; Hippocampus - pathology ; Humans ; Magnetic Resonance Imaging ; Male ; Males ; neural compensation ; Positron emission tomography ; sex ; Tomography ; white matter hyperintensity</subject><ispartof>Alzheimer's & dementia, 2024-02, Vol.20 (2), p.914-924</ispartof><rights>2023 The Authors. published by Wiley Periodicals LLC on behalf of Alzheimer's Association.</rights><rights>2023 The Authors. Alzheimer's & Dementia published by Wiley Periodicals LLC on behalf of Alzheimer's Association.</rights><rights>2024. This work is published under http://creativecommons.org/licenses/by-nc/4.0/ (the "License"). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c4043-7fbf82a1a24ff1ab992432387301180b19d90e0eca3a6a53f8b247f25184b6a33</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC10916980/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC10916980/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,885,1417,11561,12845,27923,27924,30998,45573,45574,46051,46475,53790,53792</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/37817668$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Schweitzer, Noah</creatorcontrib><creatorcontrib>Li, Jinghang</creatorcontrib><creatorcontrib>Thurston, Rebecca C.</creatorcontrib><creatorcontrib>Lopresti, Brian</creatorcontrib><creatorcontrib>Klunk, William E.</creatorcontrib><creatorcontrib>Snitz, Beth</creatorcontrib><creatorcontrib>Tudorascu, Dana</creatorcontrib><creatorcontrib>Cohen, Ann</creatorcontrib><creatorcontrib>Kamboh, M. Ilyas</creatorcontrib><creatorcontrib>Halligan‐Eddy, Edythe</creatorcontrib><creatorcontrib>Iordanova, Bistra</creatorcontrib><creatorcontrib>Villemagne, Victor L.</creatorcontrib><creatorcontrib>Aizenstein, Howard</creatorcontrib><creatorcontrib>Wu, Minjie</creatorcontrib><title>Sex‐dependent alterations in hippocampal connectivity are linked to cerebrovascular and amyloid pathologies in normal aging</title><title>Alzheimer's & dementia</title><addtitle>Alzheimers Dement</addtitle><description>INTRODUCTION
Compared to males, females have an accelerated trajectory of cognitive decline in Alzheimer's disease (AD). The neurobiological factors underlying the more rapid cognitive decline in AD in females remain unclear. This study explored how sex‐dependent alterations in hippocampal connectivity over 2 years are associated with cerebrovascular and amyloid pathologies in normal aging.
METHODS
Thirty‐three females and 21 males 65 to 93 years of age with no cognitive impairment performed a face‐name associative memory functional magnetic resonance imaging (fMRI) task with a 2‐year follow‐up. We acquired baseline carbon 11‐labeled Pittsburgh compound B ([11C]PiB) positron emission tomography (PET) and T2‐weighted fluid‐attenuated inversion recovery (T2‐FLAIR) MRI to quantify amyloid β (Aβ) burden and white matter hyperintensity (WMH) volume, respectively.
RESULTS
Males had increased hippocampal‐prefrontal connectivity over 2 years, associated with greater Aβ burden. Females had increased bilateral hippocampal functional connectivity, associated with greater WMH volume.
DISCUSSION
These findings suggest sex‐dependent compensatory mechanisms in the memory network in the presence of cerebrovascular and AD pathologies and may explain the accelerated trajectory of cognitive decline in females.</description><subject>Aging</subject><subject>Alzheimer Disease - pathology</subject><subject>Alzheimer's disease</subject><subject>Amyloid</subject><subject>amyloid beta</subject><subject>Amyloid beta-Peptides - metabolism</subject><subject>Associative memory</subject><subject>Biomarkers</subject><subject>Brain - pathology</subject><subject>cerebral small vessel disease</subject><subject>Cognition & reasoning</subject><subject>Cognitive Dysfunction - pathology</subject><subject>Cognitive impairment</subject><subject>Female</subject><subject>Females</subject><subject>Functional connectivity</subject><subject>Functional magnetic resonance imaging</subject><subject>Gender differences</subject><subject>hippocampal functional connectivity</subject><subject>Hippocampus - pathology</subject><subject>Humans</subject><subject>Magnetic Resonance Imaging</subject><subject>Male</subject><subject>Males</subject><subject>neural compensation</subject><subject>Positron emission tomography</subject><subject>sex</subject><subject>Tomography</subject><subject>white matter hyperintensity</subject><issn>1552-5260</issn><issn>1552-5279</issn><issn>1552-5279</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><sourceid>24P</sourceid><sourceid>WIN</sourceid><sourceid>EIF</sourceid><sourceid>7QJ</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><recordid>eNp1kc9qFEEQhwdRTIwefAFp8BIPm_Sf6Zmek4SgRljwEL14aWp6anY79nSP3TOrKwg-gs_ok6TNJosKnqqgPj5-xa8onjJ6wijlp-C-nTAhqbhXHDIp-ULyurm_3yt6UDxK6YrSkiomHxYHolasrip1WHy_xK-_fvzscETfoZ8IuAkjTDb4RKwnazuOwcAwgiMmeI9mshs7bQlEJM76T9iRKRCDEdsYNpDM7CAS8B2BYeuC7cgI0zq4sLJ4Y_QhDlkGK-tXj4sHPbiET27nUfHh9av35xeL5bs3b8_PlgtT0lIs6r7tFQcGvOx7Bm3T8FJwoWpBGVO0ZU3XUKRoQEAFUvSq5WXdc8lU2VYgxFHxcucd53bAzuRHIzg9RjtA3OoAVv998XatV2GjGW1Y1SiaDce3hhg-z5gmPdhk0DnwGOakuaqlkqKidUaf_4NehTn6_J8WVDWqytllpl7sKBNDShH7fRpG9e9WdW5V37Sa2Wd_xt-TdzVm4HQHfLEOt_836bPlx53yGhcrr7I</recordid><startdate>202402</startdate><enddate>202402</enddate><creator>Schweitzer, Noah</creator><creator>Li, Jinghang</creator><creator>Thurston, Rebecca C.</creator><creator>Lopresti, Brian</creator><creator>Klunk, William E.</creator><creator>Snitz, Beth</creator><creator>Tudorascu, Dana</creator><creator>Cohen, Ann</creator><creator>Kamboh, M. Ilyas</creator><creator>Halligan‐Eddy, Edythe</creator><creator>Iordanova, Bistra</creator><creator>Villemagne, Victor L.</creator><creator>Aizenstein, Howard</creator><creator>Wu, Minjie</creator><general>John Wiley & Sons, Inc</general><general>John Wiley and Sons Inc</general><scope>24P</scope><scope>WIN</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>3V.</scope><scope>7QJ</scope><scope>7RV</scope><scope>7X7</scope><scope>7XB</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BENPR</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>K9-</scope><scope>K9.</scope><scope>KB0</scope><scope>M0R</scope><scope>M0S</scope><scope>NAPCQ</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>PSYQQ</scope><scope>7X8</scope><scope>5PM</scope></search><sort><creationdate>202402</creationdate><title>Sex‐dependent alterations in hippocampal connectivity are linked to cerebrovascular and amyloid pathologies in normal aging</title><author>Schweitzer, Noah ; Li, Jinghang ; Thurston, Rebecca C. ; Lopresti, Brian ; Klunk, William E. ; Snitz, Beth ; Tudorascu, Dana ; Cohen, Ann ; Kamboh, M. Ilyas ; Halligan‐Eddy, Edythe ; Iordanova, Bistra ; Villemagne, Victor L. ; Aizenstein, Howard ; Wu, Minjie</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c4043-7fbf82a1a24ff1ab992432387301180b19d90e0eca3a6a53f8b247f25184b6a33</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2024</creationdate><topic>Aging</topic><topic>Alzheimer Disease - pathology</topic><topic>Alzheimer's disease</topic><topic>Amyloid</topic><topic>amyloid beta</topic><topic>Amyloid beta-Peptides - metabolism</topic><topic>Associative memory</topic><topic>Biomarkers</topic><topic>Brain - pathology</topic><topic>cerebral small vessel disease</topic><topic>Cognition & reasoning</topic><topic>Cognitive Dysfunction - pathology</topic><topic>Cognitive impairment</topic><topic>Female</topic><topic>Females</topic><topic>Functional connectivity</topic><topic>Functional magnetic resonance imaging</topic><topic>Gender differences</topic><topic>hippocampal functional connectivity</topic><topic>Hippocampus - pathology</topic><topic>Humans</topic><topic>Magnetic Resonance Imaging</topic><topic>Male</topic><topic>Males</topic><topic>neural compensation</topic><topic>Positron emission tomography</topic><topic>sex</topic><topic>Tomography</topic><topic>white matter hyperintensity</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Schweitzer, Noah</creatorcontrib><creatorcontrib>Li, Jinghang</creatorcontrib><creatorcontrib>Thurston, Rebecca C.</creatorcontrib><creatorcontrib>Lopresti, Brian</creatorcontrib><creatorcontrib>Klunk, William E.</creatorcontrib><creatorcontrib>Snitz, Beth</creatorcontrib><creatorcontrib>Tudorascu, Dana</creatorcontrib><creatorcontrib>Cohen, Ann</creatorcontrib><creatorcontrib>Kamboh, M. Ilyas</creatorcontrib><creatorcontrib>Halligan‐Eddy, Edythe</creatorcontrib><creatorcontrib>Iordanova, Bistra</creatorcontrib><creatorcontrib>Villemagne, Victor L.</creatorcontrib><creatorcontrib>Aizenstein, Howard</creatorcontrib><creatorcontrib>Wu, Minjie</creatorcontrib><collection>Wiley-Blackwell Open Access Titles</collection><collection>Wiley Free Content</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>ProQuest Central (Corporate)</collection><collection>Applied Social Sciences Index & Abstracts (ASSIA)</collection><collection>Nursing & Allied Health Database</collection><collection>Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>ProQuest Central (Alumni Edition)</collection><collection>ProQuest Central UK/Ireland</collection><collection>ProQuest Central Essentials</collection><collection>ProQuest Central</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central Korea</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>Consumer Health Database (Alumni Edition)</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Nursing & Allied Health Database (Alumni Edition)</collection><collection>Consumer Health Database</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>Nursing & Allied Health Premium</collection><collection>Publicly Available Content Database</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>ProQuest Central China</collection><collection>ProQuest One Psychology</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Alzheimer's & dementia</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Schweitzer, Noah</au><au>Li, Jinghang</au><au>Thurston, Rebecca C.</au><au>Lopresti, Brian</au><au>Klunk, William E.</au><au>Snitz, Beth</au><au>Tudorascu, Dana</au><au>Cohen, Ann</au><au>Kamboh, M. Ilyas</au><au>Halligan‐Eddy, Edythe</au><au>Iordanova, Bistra</au><au>Villemagne, Victor L.</au><au>Aizenstein, Howard</au><au>Wu, Minjie</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Sex‐dependent alterations in hippocampal connectivity are linked to cerebrovascular and amyloid pathologies in normal aging</atitle><jtitle>Alzheimer's & dementia</jtitle><addtitle>Alzheimers Dement</addtitle><date>2024-02</date><risdate>2024</risdate><volume>20</volume><issue>2</issue><spage>914</spage><epage>924</epage><pages>914-924</pages><issn>1552-5260</issn><issn>1552-5279</issn><eissn>1552-5279</eissn><abstract>INTRODUCTION
Compared to males, females have an accelerated trajectory of cognitive decline in Alzheimer's disease (AD). The neurobiological factors underlying the more rapid cognitive decline in AD in females remain unclear. This study explored how sex‐dependent alterations in hippocampal connectivity over 2 years are associated with cerebrovascular and amyloid pathologies in normal aging.
METHODS
Thirty‐three females and 21 males 65 to 93 years of age with no cognitive impairment performed a face‐name associative memory functional magnetic resonance imaging (fMRI) task with a 2‐year follow‐up. We acquired baseline carbon 11‐labeled Pittsburgh compound B ([11C]PiB) positron emission tomography (PET) and T2‐weighted fluid‐attenuated inversion recovery (T2‐FLAIR) MRI to quantify amyloid β (Aβ) burden and white matter hyperintensity (WMH) volume, respectively.
RESULTS
Males had increased hippocampal‐prefrontal connectivity over 2 years, associated with greater Aβ burden. Females had increased bilateral hippocampal functional connectivity, associated with greater WMH volume.
DISCUSSION
These findings suggest sex‐dependent compensatory mechanisms in the memory network in the presence of cerebrovascular and AD pathologies and may explain the accelerated trajectory of cognitive decline in females.</abstract><cop>United States</cop><pub>John Wiley & Sons, Inc</pub><pmid>37817668</pmid><doi>10.1002/alz.13503</doi><tpages>11</tpages><oa>free_for_read</oa></addata></record> |
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| subjects | Aging Alzheimer Disease - pathology Alzheimer's disease Amyloid amyloid beta Amyloid beta-Peptides - metabolism Associative memory Biomarkers Brain - pathology cerebral small vessel disease Cognition & reasoning Cognitive Dysfunction - pathology Cognitive impairment Female Females Functional connectivity Functional magnetic resonance imaging Gender differences hippocampal functional connectivity Hippocampus - pathology Humans Magnetic Resonance Imaging Male Males neural compensation Positron emission tomography sex Tomography white matter hyperintensity |
| title | Sex‐dependent alterations in hippocampal connectivity are linked to cerebrovascular and amyloid pathologies in normal aging |
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