Spatial dissociation between recognition and navigation in the primate hippocampus
The primate hippocampus, crucial for both episodic memory and spatial navigation, remains an enigma regarding whether these functions share the same neural substrates. We investigated how identical hippocampal neurons in macaque monkeys dynamically shifted their representations between tasks. In a r...
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Veröffentlicht in: | Science advances 2024-09, Vol.10 (38), p.eado7392 |
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description | The primate hippocampus, crucial for both episodic memory and spatial navigation, remains an enigma regarding whether these functions share the same neural substrates. We investigated how identical hippocampal neurons in macaque monkeys dynamically shifted their representations between tasks. In a recognition memory task, a notable fraction of hippocampal neurons showed that rate modulation strongly correlated with recognition performance. During free navigation in an open arena, spatial view, rather than position, predominantly influenced the spatial selectivity of hippocampal neurons. Neurons selective for recognition memory displayed minimal spatial tuning, while spatially tuned neurons exhibited limited memory-related activity. These neural correlates of recognition memory and space were more pronounced in the anterior and posterior portions of the hippocampus, respectively. These opposing gradients extended further into the anterior and posterior neocortices. Overall, our findings suggest the presence of orthogonal long-axis gradients between recognition memory and spatial navigation in the hippocampal-neocortical networks of macaque monkeys. |
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We investigated how identical hippocampal neurons in macaque monkeys dynamically shifted their representations between tasks. In a recognition memory task, a notable fraction of hippocampal neurons showed that rate modulation strongly correlated with recognition performance. During free navigation in an open arena, spatial view, rather than position, predominantly influenced the spatial selectivity of hippocampal neurons. Neurons selective for recognition memory displayed minimal spatial tuning, while spatially tuned neurons exhibited limited memory-related activity. These neural correlates of recognition memory and space were more pronounced in the anterior and posterior portions of the hippocampus, respectively. These opposing gradients extended further into the anterior and posterior neocortices. 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Distributed under a Creative Commons Attribution NonCommercial License 4.0 (CC BY-NC). 2024 The Authors</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c236t-4d13862920baaab123a34b19855d276f65d93a7f7adab8f04a19a509272d0a4c3</cites><orcidid>0000-0001-6740-7401 ; 0009-0002-5156-5012 ; 0000-0001-5523-657X</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/PMC11409969/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC11409969/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,860,881,27901,27902,53766,53768</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/39292773$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Xu, Xiao</creatorcontrib><creatorcontrib>Du, Kechen</creatorcontrib><creatorcontrib>Mao, Dun</creatorcontrib><title>Spatial dissociation between recognition and navigation in the primate hippocampus</title><title>Science advances</title><addtitle>Sci Adv</addtitle><description>The primate hippocampus, crucial for both episodic memory and spatial navigation, remains an enigma regarding whether these functions share the same neural substrates. We investigated how identical hippocampal neurons in macaque monkeys dynamically shifted their representations between tasks. In a recognition memory task, a notable fraction of hippocampal neurons showed that rate modulation strongly correlated with recognition performance. During free navigation in an open arena, spatial view, rather than position, predominantly influenced the spatial selectivity of hippocampal neurons. Neurons selective for recognition memory displayed minimal spatial tuning, while spatially tuned neurons exhibited limited memory-related activity. These neural correlates of recognition memory and space were more pronounced in the anterior and posterior portions of the hippocampus, respectively. These opposing gradients extended further into the anterior and posterior neocortices. Overall, our findings suggest the presence of orthogonal long-axis gradients between recognition memory and spatial navigation in the hippocampal-neocortical networks of macaque monkeys.</description><subject>Animals</subject><subject>Hippocampus - physiology</subject><subject>Macaca mulatta</subject><subject>Male</subject><subject>Neurons - physiology</subject><subject>Neurophysiology</subject><subject>Neuroscience</subject><subject>Primates - physiology</subject><subject>Recognition, Psychology - physiology</subject><subject>SciAdv r-articles</subject><subject>Spatial Navigation - physiology</subject><issn>2375-2548</issn><issn>2375-2548</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNpVkUlPwzAQhS0EolXplSPKkUuKl8SJTwhVbBISEsvZmthOa5TYIU6K-PeEplTl5JHnmzdP8xA6J3hBCOVXQVnQmwVonzFBj9CUsiyNaZrkxwf1BM1D-MAYk4TzlIhTNBloQbOMTdHLawOdhSrSNgQ_6HXWu6gw3ZcxLmqN8itnt3_gdORgY1cjYl3UrU3UtLaGzkRr2zReQd304QydlFAFM9-9M_R-d_u2fIifnu8flzdPsaKMd3GiCcv54AMXAFAQyoAlBRF5mmqa8ZKnWjDIygw0FHmJEyACUjz4phpDotgMXY-6TV_URivjuhYquXXUfksPVv7vOLuWK7-RhCRYCC4GhcudQus_exM6WdugTFWBM74PkhHMM0YpwwO6GFHV-hBaU-73ECx_w5BjGHIXxjBwcehuj_-dnv0ARgaJjA</recordid><startdate>20240920</startdate><enddate>20240920</enddate><creator>Xu, Xiao</creator><creator>Du, Kechen</creator><creator>Mao, Dun</creator><general>American Association for the Advancement 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>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0001-6740-7401</orcidid><orcidid>https://orcid.org/0009-0002-5156-5012</orcidid><orcidid>https://orcid.org/0000-0001-5523-657X</orcidid></search><sort><creationdate>20240920</creationdate><title>Spatial dissociation between recognition and navigation in the primate hippocampus</title><author>Xu, Xiao ; Du, Kechen ; Mao, Dun</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c236t-4d13862920baaab123a34b19855d276f65d93a7f7adab8f04a19a509272d0a4c3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2024</creationdate><topic>Animals</topic><topic>Hippocampus - physiology</topic><topic>Macaca mulatta</topic><topic>Male</topic><topic>Neurons - physiology</topic><topic>Neurophysiology</topic><topic>Neuroscience</topic><topic>Primates - physiology</topic><topic>Recognition, Psychology - physiology</topic><topic>SciAdv r-articles</topic><topic>Spatial Navigation - physiology</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Xu, Xiao</creatorcontrib><creatorcontrib>Du, Kechen</creatorcontrib><creatorcontrib>Mao, Dun</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><collection>PubMed Central (Full Participant titles)</collection><jtitle>Science advances</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Xu, Xiao</au><au>Du, Kechen</au><au>Mao, Dun</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Spatial dissociation between recognition and navigation in the primate hippocampus</atitle><jtitle>Science advances</jtitle><addtitle>Sci Adv</addtitle><date>2024-09-20</date><risdate>2024</risdate><volume>10</volume><issue>38</issue><spage>eado7392</spage><pages>eado7392-</pages><issn>2375-2548</issn><eissn>2375-2548</eissn><abstract>The primate hippocampus, crucial for both episodic memory and spatial navigation, remains an enigma regarding whether these functions share the same neural substrates. We investigated how identical hippocampal neurons in macaque monkeys dynamically shifted their representations between tasks. In a recognition memory task, a notable fraction of hippocampal neurons showed that rate modulation strongly correlated with recognition performance. During free navigation in an open arena, spatial view, rather than position, predominantly influenced the spatial selectivity of hippocampal neurons. Neurons selective for recognition memory displayed minimal spatial tuning, while spatially tuned neurons exhibited limited memory-related activity. These neural correlates of recognition memory and space were more pronounced in the anterior and posterior portions of the hippocampus, respectively. These opposing gradients extended further into the anterior and posterior neocortices. 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subjects | Animals Hippocampus - physiology Macaca mulatta Male Neurons - physiology Neurophysiology Neuroscience Primates - physiology Recognition, Psychology - physiology SciAdv r-articles Spatial Navigation - physiology |
title | Spatial dissociation between recognition and navigation in the primate hippocampus |
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