Coordination of entorhinal–hippocampal ensemble activity during associative learning
Simultaneous recordings from hippocampus and entorhinal cortex in rats show that as the animals learn odour guidance cues during their exploration of two-dimensional space in the laboratory, ensembles of coherently firing neurons emerge in both locations, with cortical–hippocampal oscillatory coupli...
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description | Simultaneous recordings from hippocampus and entorhinal cortex in rats show that as the animals learn odour guidance cues during their exploration of two-dimensional space in the laboratory, ensembles of coherently firing neurons emerge in both locations, with cortical–hippocampal oscillatory coupling occurring in a specific range of the beta-gamma frequency band.
Cortical circuits active during learning
During declarative memory formation as well as recall, communication between the hippocampus and cortex is essential. However, the contributions to learning/recall and the nature of such communications are still unknown. Here, Edvard Moser and colleagues simultaneously record from hippocampus and entorhinal cortex to unpack the synchronicity and contributions of these two sites to memory management related to navigational behaviour. As rats learn odour guidance cues during their exploration of space, ensembles of coherently firing neurons emerged in both locations, with cortical–hippocampal coupling occurring with a specific range of the gamma oscillation. Thus, associative learning tasks seem to utilize gamma synchronization as a mechanism for maintaining evolving representations in dispersed neural circuits.
Accumulating evidence points to cortical oscillations as a mechanism for mediating interactions among functionally specialized neurons in distributed brain circuits
1
,
2
,
3
,
4
,
5
,
6
. A brain function that may use such interactions is declarative memory—that is, memory that can be consciously recalled, such as episodes and facts. Declarative memory is enabled by circuits in the entorhinal cortex that interface the hippocampus with the neocortex
7
,
8
. During encoding and retrieval of declarative memories, entorhinal and hippocampal circuits are thought to interact via theta and gamma oscillations
4
,
6
,
8
, which in awake rodents predominate frequency spectra in both regions
9
,
10
,
11
,
12
. In favour of this idea, theta–gamma coupling has been observed between entorhinal cortex and hippocampus under steady-state conditions in well-trained rats
12
; however, the relationship between interregional coupling and memory formation remains poorly understood. Here we show, by multisite recording at successive stages of associative learning, that the coherence of firing patterns in directly connected entorhinal–hippocampus circuits evolves as rats learn to use an odour cue to guide navigational behaviour, and that such coherence is invariably linked |
doi_str_mv | 10.1038/nature13162 |
format | Article |
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Cortical circuits active during learning
During declarative memory formation as well as recall, communication between the hippocampus and cortex is essential. However, the contributions to learning/recall and the nature of such communications are still unknown. Here, Edvard Moser and colleagues simultaneously record from hippocampus and entorhinal cortex to unpack the synchronicity and contributions of these two sites to memory management related to navigational behaviour. As rats learn odour guidance cues during their exploration of space, ensembles of coherently firing neurons emerged in both locations, with cortical–hippocampal coupling occurring with a specific range of the gamma oscillation. Thus, associative learning tasks seem to utilize gamma synchronization as a mechanism for maintaining evolving representations in dispersed neural circuits.
Accumulating evidence points to cortical oscillations as a mechanism for mediating interactions among functionally specialized neurons in distributed brain circuits
1
,
2
,
3
,
4
,
5
,
6
. A brain function that may use such interactions is declarative memory—that is, memory that can be consciously recalled, such as episodes and facts. Declarative memory is enabled by circuits in the entorhinal cortex that interface the hippocampus with the neocortex
7
,
8
. During encoding and retrieval of declarative memories, entorhinal and hippocampal circuits are thought to interact via theta and gamma oscillations
4
,
6
,
8
, which in awake rodents predominate frequency spectra in both regions
9
,
10
,
11
,
12
. In favour of this idea, theta–gamma coupling has been observed between entorhinal cortex and hippocampus under steady-state conditions in well-trained rats
12
; however, the relationship between interregional coupling and memory formation remains poorly understood. Here we show, by multisite recording at successive stages of associative learning, that the coherence of firing patterns in directly connected entorhinal–hippocampus circuits evolves as rats learn to use an odour cue to guide navigational behaviour, and that such coherence is invariably linked to the development of ensemble representations for unique trial outcomes in each area. Entorhinal–hippocampal coupling was observed specifically in the 20–40-hertz frequency band and specifically between the distal part of hippocampal area CA1 and the lateral part of entorhinal cortex, the subfields that receive the predominant olfactory input to the hippocampal region
13
. Collectively, the results identify 20–40-hertz oscillations as a mechanism for synchronizing evolving representations in dispersed neural circuits during encoding and retrieval of olfactory–spatial associative memory.</description><identifier>ISSN: 0028-0836</identifier><identifier>EISSN: 1476-4687</identifier><identifier>DOI: 10.1038/nature13162</identifier><identifier>PMID: 24739966</identifier><identifier>CODEN: NATUAS</identifier><language>eng</language><publisher>London: Nature Publishing Group UK</publisher><subject>631/378/116/2396 ; 631/378/1595/1554 ; 9/26 ; 9/30 ; Animal cognition ; Animals ; Cues ; Entorhinal Cortex - cytology ; Entorhinal Cortex - physiology ; Exploratory Behavior - physiology ; Food ; Hippocampus (Brain) ; Hippocampus - cytology ; Hippocampus - physiology ; Humanities and Social Sciences ; Learning - physiology ; letter ; Male ; Memory - physiology ; Models, Neurological ; multidisciplinary ; Neural circuitry ; Neurological research ; Neurology ; Neurons - physiology ; Odorants - analysis ; Physiological aspects ; Rats ; Rats, Long-Evans ; Rodents ; Science ; Smell ; Space Perception - physiology ; Variance analysis</subject><ispartof>Nature (London), 2014-06, Vol.510 (7503), p.143-147</ispartof><rights>Springer Nature Limited 2014</rights><rights>COPYRIGHT 2014 Nature Publishing Group</rights><rights>Copyright Nature Publishing Group Jun 5, 2014</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c659t-c2e0bb583c3966a79f0bcc64161fe26e26dd5fe874cd1b4572720f2d71777ff03</citedby><cites>FETCH-LOGICAL-c659t-c2e0bb583c3966a79f0bcc64161fe26e26dd5fe874cd1b4572720f2d71777ff03</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>314,780,784,27924,27925</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/24739966$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Igarashi, Kei M.</creatorcontrib><creatorcontrib>Lu, Li</creatorcontrib><creatorcontrib>Colgin, Laura L.</creatorcontrib><creatorcontrib>Moser, May-Britt</creatorcontrib><creatorcontrib>Moser, Edvard I.</creatorcontrib><title>Coordination of entorhinal–hippocampal ensemble activity during associative learning</title><title>Nature (London)</title><addtitle>Nature</addtitle><addtitle>Nature</addtitle><description>Simultaneous recordings from hippocampus and entorhinal cortex in rats show that as the animals learn odour guidance cues during their exploration of two-dimensional space in the laboratory, ensembles of coherently firing neurons emerge in both locations, with cortical–hippocampal oscillatory coupling occurring in a specific range of the beta-gamma frequency band.
Cortical circuits active during learning
During declarative memory formation as well as recall, communication between the hippocampus and cortex is essential. However, the contributions to learning/recall and the nature of such communications are still unknown. Here, Edvard Moser and colleagues simultaneously record from hippocampus and entorhinal cortex to unpack the synchronicity and contributions of these two sites to memory management related to navigational behaviour. As rats learn odour guidance cues during their exploration of space, ensembles of coherently firing neurons emerged in both locations, with cortical–hippocampal coupling occurring with a specific range of the gamma oscillation. Thus, associative learning tasks seem to utilize gamma synchronization as a mechanism for maintaining evolving representations in dispersed neural circuits.
Accumulating evidence points to cortical oscillations as a mechanism for mediating interactions among functionally specialized neurons in distributed brain circuits
1
,
2
,
3
,
4
,
5
,
6
. A brain function that may use such interactions is declarative memory—that is, memory that can be consciously recalled, such as episodes and facts. Declarative memory is enabled by circuits in the entorhinal cortex that interface the hippocampus with the neocortex
7
,
8
. During encoding and retrieval of declarative memories, entorhinal and hippocampal circuits are thought to interact via theta and gamma oscillations
4
,
6
,
8
, which in awake rodents predominate frequency spectra in both regions
9
,
10
,
11
,
12
. In favour of this idea, theta–gamma coupling has been observed between entorhinal cortex and hippocampus under steady-state conditions in well-trained rats
12
; however, the relationship between interregional coupling and memory formation remains poorly understood. Here we show, by multisite recording at successive stages of associative learning, that the coherence of firing patterns in directly connected entorhinal–hippocampus circuits evolves as rats learn to use an odour cue to guide navigational behaviour, and that such coherence is invariably linked to the development of ensemble representations for unique trial outcomes in each area. Entorhinal–hippocampal coupling was observed specifically in the 20–40-hertz frequency band and specifically between the distal part of hippocampal area CA1 and the lateral part of entorhinal cortex, the subfields that receive the predominant olfactory input to the hippocampal region
13
. Collectively, the results identify 20–40-hertz oscillations as a mechanism for synchronizing evolving representations in dispersed neural circuits during encoding and retrieval of olfactory–spatial associative memory.</description><subject>631/378/116/2396</subject><subject>631/378/1595/1554</subject><subject>9/26</subject><subject>9/30</subject><subject>Animal cognition</subject><subject>Animals</subject><subject>Cues</subject><subject>Entorhinal Cortex - cytology</subject><subject>Entorhinal Cortex - physiology</subject><subject>Exploratory Behavior - physiology</subject><subject>Food</subject><subject>Hippocampus (Brain)</subject><subject>Hippocampus - cytology</subject><subject>Hippocampus - physiology</subject><subject>Humanities and Social Sciences</subject><subject>Learning - physiology</subject><subject>letter</subject><subject>Male</subject><subject>Memory - physiology</subject><subject>Models, Neurological</subject><subject>multidisciplinary</subject><subject>Neural circuitry</subject><subject>Neurological research</subject><subject>Neurology</subject><subject>Neurons - physiology</subject><subject>Odorants - analysis</subject><subject>Physiological aspects</subject><subject>Rats</subject><subject>Rats, Long-Evans</subject><subject>Rodents</subject><subject>Science</subject><subject>Smell</subject><subject>Space Perception - physiology</subject><subject>Variance analysis</subject><issn>0028-0836</issn><issn>1476-4687</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2014</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>8G5</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>GNUQQ</sourceid><sourceid>GUQSH</sourceid><sourceid>M2O</sourceid><recordid>eNp10t9r1TAUB_AgirubPvkuRV8U7cyPNmkfLxedg6GgUx9Dmp7cZbRNl6Rje_N_8D_0L1mum3qvVBoonHzyJTkchJ4QfEgwq94MKk4eCCOc3kMLUgieF7wS99ECY1rluGJ8D-2HcI4xLokoHqI9WghW15wv0NeVc761KcO6IXMmgyE6f5YK3c_vP87sODqt-lF1aSNA33SQKR3tpY3XWTt5O6wzFYLTNgVcQtaB8kMqPkIPjOoCPL77H6Av796ert7nJx-PjlfLk1zzso65poCbpqyYZuk2StQGN1rzgnBigPK02rY0UIlCt6QpSkEFxYa2ggghjMHsAL24zR29u5ggRNnboKHr1ABuCpKUrCCYMlIn-vwfeu4mn975S5V1ISjjf9VadSDtYFz0Sm9C5ZKJ1FxMS5JUPqPWMIBXnRvA2FTe8c9mvB7thdxGhzMofS30Vs-mvtw5kEyEq7hWUwjy-POnXfvq_3Z5-m31YVZr70LwYOToba_8tSRYboZObg1d0k_vOjs1PbR_7O8pS-D1LQjjZmLAb7V-Ju8GsELeqw</recordid><startdate>20140605</startdate><enddate>20140605</enddate><creator>Igarashi, Kei M.</creator><creator>Lu, Li</creator><creator>Colgin, Laura L.</creator><creator>Moser, May-Britt</creator><creator>Moser, Edvard I.</creator><general>Nature Publishing Group UK</general><general>Nature Publishing Group</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>ATWCN</scope><scope>3V.</scope><scope>7QG</scope><scope>7QL</scope><scope>7QP</scope><scope>7QR</scope><scope>7RV</scope><scope>7SN</scope><scope>7SS</scope><scope>7ST</scope><scope>7T5</scope><scope>7TG</scope><scope>7TK</scope><scope>7TM</scope><scope>7TO</scope><scope>7U9</scope><scope>7X2</scope><scope>7X7</scope><scope>7XB</scope><scope>88A</scope><scope>88E</scope><scope>88G</scope><scope>88I</scope><scope>8AF</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>8G5</scope><scope>ABJCF</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>ARAPS</scope><scope>ATCPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BEC</scope><scope>BENPR</scope><scope>BGLVJ</scope><scope>BHPHI</scope><scope>BKSAR</scope><scope>C1K</scope><scope>CCPQU</scope><scope>D1I</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>GUQSH</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>M2M</scope><scope>M2O</scope><scope>M2P</scope><scope>M7N</scope><scope>M7P</scope><scope>M7S</scope><scope>MBDVC</scope><scope>NAPCQ</scope><scope>P5Z</scope><scope>P62</scope><scope>P64</scope><scope>PATMY</scope><scope>PCBAR</scope><scope>PDBOC</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PSYQQ</scope><scope>PTHSS</scope><scope>PYCSY</scope><scope>Q9U</scope><scope>R05</scope><scope>RC3</scope><scope>S0X</scope><scope>SOI</scope><scope>7X8</scope></search><sort><creationdate>20140605</creationdate><title>Coordination of entorhinal–hippocampal ensemble activity during associative learning</title><author>Igarashi, Kei M. ; Lu, Li ; Colgin, Laura L. ; Moser, May-Britt ; Moser, Edvard I.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c659t-c2e0bb583c3966a79f0bcc64161fe26e26dd5fe874cd1b4572720f2d71777ff03</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2014</creationdate><topic>631/378/116/2396</topic><topic>631/378/1595/1554</topic><topic>9/26</topic><topic>9/30</topic><topic>Animal cognition</topic><topic>Animals</topic><topic>Cues</topic><topic>Entorhinal Cortex - cytology</topic><topic>Entorhinal Cortex - physiology</topic><topic>Exploratory Behavior - physiology</topic><topic>Food</topic><topic>Hippocampus (Brain)</topic><topic>Hippocampus - cytology</topic><topic>Hippocampus - physiology</topic><topic>Humanities and Social Sciences</topic><topic>Learning - physiology</topic><topic>letter</topic><topic>Male</topic><topic>Memory - physiology</topic><topic>Models, Neurological</topic><topic>multidisciplinary</topic><topic>Neural circuitry</topic><topic>Neurological research</topic><topic>Neurology</topic><topic>Neurons - physiology</topic><topic>Odorants - analysis</topic><topic>Physiological aspects</topic><topic>Rats</topic><topic>Rats, Long-Evans</topic><topic>Rodents</topic><topic>Science</topic><topic>Smell</topic><topic>Space Perception - physiology</topic><topic>Variance analysis</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Igarashi, Kei M.</creatorcontrib><creatorcontrib>Lu, Li</creatorcontrib><creatorcontrib>Colgin, Laura L.</creatorcontrib><creatorcontrib>Moser, May-Britt</creatorcontrib><creatorcontrib>Moser, Edvard I.</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Gale In Context: Middle School</collection><collection>ProQuest Central (Corporate)</collection><collection>Animal Behavior Abstracts</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Nursing & Allied Health Database</collection><collection>Ecology Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Environment Abstracts</collection><collection>Immunology Abstracts</collection><collection>Meteorological & Geoastrophysical Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Oncogenes and Growth Factors Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Agricultural Science Collection</collection><collection>ProQuest Health and Medical</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Biology Database (Alumni Edition)</collection><collection>Medical Database (Alumni Edition)</collection><collection>Psychology Database (Alumni)</collection><collection>Science Database (Alumni Edition)</collection><collection>STEM Database</collection><collection>ProQuest Pharma Collection</collection><collection>Public Health Database (Proquest)</collection><collection>Technology Research Database</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Technology Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>Research Library (Alumni Edition)</collection><collection>Materials Science & Engineering Collection</collection><collection>ProQuest Central (Alumni)</collection><collection>ProQuest Central</collection><collection>Advanced Technologies & Aerospace Collection</collection><collection>Agricultural & Environmental Science Collection</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>eLibrary</collection><collection>ProQuest Central</collection><collection>Technology Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Earth, Atmospheric & Aquatic Science Collection</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ProQuest One Community College</collection><collection>ProQuest Materials Science Collection</collection><collection>ProQuest Central</collection><collection>Engineering Research Database</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>Research Library Prep</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Materials Science Database</collection><collection>Nursing & Allied Health Database (Alumni Edition)</collection><collection>Meteorological & Geoastrophysical Abstracts - 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Academic</collection><jtitle>Nature (London)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Igarashi, Kei M.</au><au>Lu, Li</au><au>Colgin, Laura L.</au><au>Moser, May-Britt</au><au>Moser, Edvard I.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Coordination of entorhinal–hippocampal ensemble activity during associative learning</atitle><jtitle>Nature (London)</jtitle><stitle>Nature</stitle><addtitle>Nature</addtitle><date>2014-06-05</date><risdate>2014</risdate><volume>510</volume><issue>7503</issue><spage>143</spage><epage>147</epage><pages>143-147</pages><issn>0028-0836</issn><eissn>1476-4687</eissn><coden>NATUAS</coden><abstract>Simultaneous recordings from hippocampus and entorhinal cortex in rats show that as the animals learn odour guidance cues during their exploration of two-dimensional space in the laboratory, ensembles of coherently firing neurons emerge in both locations, with cortical–hippocampal oscillatory coupling occurring in a specific range of the beta-gamma frequency band.
Cortical circuits active during learning
During declarative memory formation as well as recall, communication between the hippocampus and cortex is essential. However, the contributions to learning/recall and the nature of such communications are still unknown. Here, Edvard Moser and colleagues simultaneously record from hippocampus and entorhinal cortex to unpack the synchronicity and contributions of these two sites to memory management related to navigational behaviour. As rats learn odour guidance cues during their exploration of space, ensembles of coherently firing neurons emerged in both locations, with cortical–hippocampal coupling occurring with a specific range of the gamma oscillation. Thus, associative learning tasks seem to utilize gamma synchronization as a mechanism for maintaining evolving representations in dispersed neural circuits.
Accumulating evidence points to cortical oscillations as a mechanism for mediating interactions among functionally specialized neurons in distributed brain circuits
1
,
2
,
3
,
4
,
5
,
6
. A brain function that may use such interactions is declarative memory—that is, memory that can be consciously recalled, such as episodes and facts. Declarative memory is enabled by circuits in the entorhinal cortex that interface the hippocampus with the neocortex
7
,
8
. During encoding and retrieval of declarative memories, entorhinal and hippocampal circuits are thought to interact via theta and gamma oscillations
4
,
6
,
8
, which in awake rodents predominate frequency spectra in both regions
9
,
10
,
11
,
12
. In favour of this idea, theta–gamma coupling has been observed between entorhinal cortex and hippocampus under steady-state conditions in well-trained rats
12
; however, the relationship between interregional coupling and memory formation remains poorly understood. Here we show, by multisite recording at successive stages of associative learning, that the coherence of firing patterns in directly connected entorhinal–hippocampus circuits evolves as rats learn to use an odour cue to guide navigational behaviour, and that such coherence is invariably linked to the development of ensemble representations for unique trial outcomes in each area. Entorhinal–hippocampal coupling was observed specifically in the 20–40-hertz frequency band and specifically between the distal part of hippocampal area CA1 and the lateral part of entorhinal cortex, the subfields that receive the predominant olfactory input to the hippocampal region
13
. Collectively, the results identify 20–40-hertz oscillations as a mechanism for synchronizing evolving representations in dispersed neural circuits during encoding and retrieval of olfactory–spatial associative memory.</abstract><cop>London</cop><pub>Nature Publishing Group UK</pub><pmid>24739966</pmid><doi>10.1038/nature13162</doi><tpages>5</tpages><oa>free_for_read</oa></addata></record> |
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recordid | cdi_proquest_miscellaneous_1534102319 |
source | MEDLINE; Nature; Alma/SFX Local Collection |
subjects | 631/378/116/2396 631/378/1595/1554 9/26 9/30 Animal cognition Animals Cues Entorhinal Cortex - cytology Entorhinal Cortex - physiology Exploratory Behavior - physiology Food Hippocampus (Brain) Hippocampus - cytology Hippocampus - physiology Humanities and Social Sciences Learning - physiology letter Male Memory - physiology Models, Neurological multidisciplinary Neural circuitry Neurological research Neurology Neurons - physiology Odorants - analysis Physiological aspects Rats Rats, Long-Evans Rodents Science Smell Space Perception - physiology Variance analysis |
title | Coordination of entorhinal–hippocampal ensemble activity during associative learning |
url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2024-12-25T10%3A43%3A59IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-gale_proqu&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Coordination%20of%20entorhinal%E2%80%93hippocampal%20ensemble%20activity%20during%20associative%20learning&rft.jtitle=Nature%20(London)&rft.au=Igarashi,%20Kei%20M.&rft.date=2014-06-05&rft.volume=510&rft.issue=7503&rft.spage=143&rft.epage=147&rft.pages=143-147&rft.issn=0028-0836&rft.eissn=1476-4687&rft.coden=NATUAS&rft_id=info:doi/10.1038/nature13162&rft_dat=%3Cgale_proqu%3EA371470251%3C/gale_proqu%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=1535947236&rft_id=info:pmid/24739966&rft_galeid=A371470251&rfr_iscdi=true |