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Time separating spatial memories does not influence their integration in humans
Humans can navigate through similar environments-like grocery stores-by integrating across their memories to extract commonalities or by differentiating between each to find idiosyncratic locations. Here, we investigate one factor that might impact whether two related spatial memories are integrated...
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Published in: | PloS one 2023-08, Vol.18 (8), p.e0289649-e0289649 |
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description | Humans can navigate through similar environments-like grocery stores-by integrating across their memories to extract commonalities or by differentiating between each to find idiosyncratic locations. Here, we investigate one factor that might impact whether two related spatial memories are integrated or differentiated: Namely, the temporal delay between experiences. Rodents have been shown to integrate memories more often when they are formed within 6 hours of each other. To test if this effect influences how humans spontaneously integrate spatial memories, we had 131 participants search for rewards in two similar virtual environments. We separated these learning experiences by either 30 minutes, 3 hours, or 27 hours. Memory integration was assessed three days later. Participants were able to integrate and simultaneously differentiate related memories across experiences. However, neither memory integration nor differentiation was modulated by temporal delay, in contrast to previous work. We further showed that both the levels of initial memory reactivation during the second experience and memory generalization to novel environments were comparable across conditions. Moreover, perseveration toward the initial reward locations during the second experience was related positively to integration and negatively to differentiation-but again, these associations did not vary by delay. Our findings identify important boundary conditions on the translation of rodent memory mechanisms to humans, motivating more research to characterize how even fundamental memory mechanisms are conserved and diverge across species. |
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Here, we investigate one factor that might impact whether two related spatial memories are integrated or differentiated: Namely, the temporal delay between experiences. Rodents have been shown to integrate memories more often when they are formed within 6 hours of each other. To test if this effect influences how humans spontaneously integrate spatial memories, we had 131 participants search for rewards in two similar virtual environments. We separated these learning experiences by either 30 minutes, 3 hours, or 27 hours. Memory integration was assessed three days later. Participants were able to integrate and simultaneously differentiate related memories across experiences. However, neither memory integration nor differentiation was modulated by temporal delay, in contrast to previous work. We further showed that both the levels of initial memory reactivation during the second experience and memory generalization to novel environments were comparable across conditions. Moreover, perseveration toward the initial reward locations during the second experience was related positively to integration and negatively to differentiation-but again, these associations did not vary by delay. Our findings identify important boundary conditions on the translation of rodent memory mechanisms to humans, motivating more research to characterize how even fundamental memory mechanisms are conserved and diverge across species.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0289649</identifier><identifier>PMID: 37561677</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Analysis ; Biology and Life Sciences ; Boundary conditions ; Delay ; Differentiation ; Endangered & extinct species ; Evaluation ; Generalization, Psychological - physiology ; Geospatial data ; Grocery industry ; Humans ; Integration ; Medicine and Health Sciences ; Memory ; Reward ; Rodents ; Social Sciences ; Spatial Memory ; Supermarkets ; Virtual environments ; Wildlife conservation</subject><ispartof>PloS one, 2023-08, Vol.18 (8), p.e0289649-e0289649</ispartof><rights>Copyright: © 2023 Fang et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.</rights><rights>COPYRIGHT 2023 Public Library of Science</rights><rights>2023 Fang et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>2023 Fang et al 2023 Fang et al</rights><rights>2023 Fang et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. 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-c576t-89d373aca46d27e0b952d7577eac883fe5f1496fc6d0454922fea436f74a8c73</cites><orcidid>0000-0001-9208-7155</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.proquest.com/docview/2848826684/fulltextPDF?pq-origsite=primo$$EPDF$$P50$$Gproquest$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.proquest.com/docview/2848826684?pq-origsite=primo$$EHTML$$P50$$Gproquest$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,885,25753,27924,27925,37012,37013,38516,43895,44590,53791,53793,74412,75126</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/37561677$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>King, Bradley R.</contributor><creatorcontrib>Fang, Xiaoping</creatorcontrib><creatorcontrib>Alsbury-Nealy, Benjamin</creatorcontrib><creatorcontrib>Wang, Ying</creatorcontrib><creatorcontrib>Frankland, Paul W</creatorcontrib><creatorcontrib>Josselyn, Sheena A</creatorcontrib><creatorcontrib>Schlichting, Margaret L</creatorcontrib><creatorcontrib>Duncan, Katherine D</creatorcontrib><title>Time separating spatial memories does not influence their integration in humans</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>Humans can navigate through similar environments-like grocery stores-by integrating across their memories to extract commonalities or by differentiating between each to find idiosyncratic locations. 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Moreover, perseveration toward the initial reward locations during the second experience was related positively to integration and negatively to differentiation-but again, these associations did not vary by delay. Our findings identify important boundary conditions on the translation of rodent memory mechanisms to humans, motivating more research to characterize how even fundamental memory mechanisms are conserved and diverge across species.</description><subject>Analysis</subject><subject>Biology and Life Sciences</subject><subject>Boundary conditions</subject><subject>Delay</subject><subject>Differentiation</subject><subject>Endangered & extinct species</subject><subject>Evaluation</subject><subject>Generalization, Psychological - physiology</subject><subject>Geospatial data</subject><subject>Grocery industry</subject><subject>Humans</subject><subject>Integration</subject><subject>Medicine and Health Sciences</subject><subject>Memory</subject><subject>Reward</subject><subject>Rodents</subject><subject>Social Sciences</subject><subject>Spatial Memory</subject><subject>Supermarkets</subject><subject>Virtual environments</subject><subject>Wildlife conservation</subject><issn>1932-6203</issn><issn>1932-6203</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2023</creationdate><recordtype>article</recordtype><sourceid>COVID</sourceid><sourceid>PIMPY</sourceid><recordid>eNqNkt9r1TAUx4sobk7_A9GCMPThXtMkTdKnMYY_BoMLevE1ZOlpm5EmNWlF__ulrhu3sgcJ5Jwkn-854ZyTZa8LtC0ILz7e-Ck4ZbeDd7BFWFSMVk-y46IieMMwIk8P_KPsRYw3CJVEMPY8OyK8ZAXj_Djb7U0PeYRBBTUa1-ZxSFbZvIfeBwMxr33anB9z4xo7gdOQjx2YkM4jtLPKu-Tn3dQrF19mzxplI7xa7Em2__xpf_F1c7X7cnlxfrXRJWfjRlQ14URpRVmNOaDrqsQ1LzkHpYUgDZRNQSvWaFYjWtIK4wYUJazhVAnNyUn29i7sYH2USymixIIKgRkTNBFnCzFd91BrcGNQVg7B9Cr8kV4ZuX5xppOt_yULRAtacpIivF8iBP9zgjjK3kQN1ioHfpqTlYigKuVK6Lt_0Me_tFCtsiBTOX1KrOeg8pwzRHAh_qbdPkKlVUNvdGp2Y9L9SvBhJUjMCL_HVk0xysvv3_6f3f1Ys6cHbAfKjl30dpobHtcgvQN18DEGaB6qXCA5z-p9NeQ8q3KZ1SR7c9ihB9H9cJJbgxzkeg</recordid><startdate>20230810</startdate><enddate>20230810</enddate><creator>Fang, Xiaoping</creator><creator>Alsbury-Nealy, Benjamin</creator><creator>Wang, Ying</creator><creator>Frankland, Paul W</creator><creator>Josselyn, Sheena A</creator><creator>Schlichting, Margaret L</creator><creator>Duncan, Katherine D</creator><general>Public Library of Science</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>IOV</scope><scope>ISR</scope><scope>3V.</scope><scope>7QG</scope><scope>7QL</scope><scope>7QO</scope><scope>7RV</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TG</scope><scope>7TM</scope><scope>7U9</scope><scope>7X2</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8AO</scope><scope>8C1</scope><scope>8FD</scope><scope>8FE</scope><scope>8FG</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABJCF</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>ARAPS</scope><scope>ATCPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BGLVJ</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</scope><scope>COVID</scope><scope>D1I</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>H94</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>KB.</scope><scope>KB0</scope><scope>KL.</scope><scope>L6V</scope><scope>LK8</scope><scope>M0K</scope><scope>M0S</scope><scope>M1P</scope><scope>M7N</scope><scope>M7P</scope><scope>M7S</scope><scope>NAPCQ</scope><scope>P5Z</scope><scope>P62</scope><scope>P64</scope><scope>PATMY</scope><scope>PDBOC</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PTHSS</scope><scope>PYCSY</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0001-9208-7155</orcidid></search><sort><creationdate>20230810</creationdate><title>Time separating spatial memories does not influence their integration in humans</title><author>Fang, Xiaoping ; Alsbury-Nealy, Benjamin ; Wang, Ying ; Frankland, Paul W ; Josselyn, Sheena A ; Schlichting, Margaret L ; Duncan, Katherine D</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c576t-89d373aca46d27e0b952d7577eac883fe5f1496fc6d0454922fea436f74a8c73</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2023</creationdate><topic>Analysis</topic><topic>Biology and Life Sciences</topic><topic>Boundary conditions</topic><topic>Delay</topic><topic>Differentiation</topic><topic>Endangered & extinct species</topic><topic>Evaluation</topic><topic>Generalization, Psychological - 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Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>PloS one</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Fang, Xiaoping</au><au>Alsbury-Nealy, Benjamin</au><au>Wang, Ying</au><au>Frankland, Paul W</au><au>Josselyn, Sheena A</au><au>Schlichting, Margaret L</au><au>Duncan, Katherine D</au><au>King, Bradley R.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Time separating spatial memories does not influence their integration in humans</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2023-08-10</date><risdate>2023</risdate><volume>18</volume><issue>8</issue><spage>e0289649</spage><epage>e0289649</epage><pages>e0289649-e0289649</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>Humans can navigate through similar environments-like grocery stores-by integrating across their memories to extract commonalities or by differentiating between each to find idiosyncratic locations. Here, we investigate one factor that might impact whether two related spatial memories are integrated or differentiated: Namely, the temporal delay between experiences. Rodents have been shown to integrate memories more often when they are formed within 6 hours of each other. To test if this effect influences how humans spontaneously integrate spatial memories, we had 131 participants search for rewards in two similar virtual environments. We separated these learning experiences by either 30 minutes, 3 hours, or 27 hours. Memory integration was assessed three days later. Participants were able to integrate and simultaneously differentiate related memories across experiences. However, neither memory integration nor differentiation was modulated by temporal delay, in contrast to previous work. We further showed that both the levels of initial memory reactivation during the second experience and memory generalization to novel environments were comparable across conditions. 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subjects | Analysis Biology and Life Sciences Boundary conditions Delay Differentiation Endangered & extinct species Evaluation Generalization, Psychological - physiology Geospatial data Grocery industry Humans Integration Medicine and Health Sciences Memory Reward Rodents Social Sciences Spatial Memory Supermarkets Virtual environments Wildlife conservation |
title | Time separating spatial memories does not influence their integration in humans |
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