Context Fear Learning in the Absence of the Hippocampus
Lesions of the rodent hippocampus invariably abolish context fear memories formed in the recent past but do not always prevent new learning. To better understand this discrepancy, we thoroughly examined the acquisition of context fear in rats with pretraining excitotoxic lesions of the dorsal hippoc...
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Veröffentlicht in: | The Journal of neuroscience 2006-05, Vol.26 (20), p.5484-5491 |
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description | Lesions of the rodent hippocampus invariably abolish context fear memories formed in the recent past but do not always prevent new learning. To better understand this discrepancy, we thoroughly examined the acquisition of context fear in rats with pretraining excitotoxic lesions of the dorsal hippocampus. In the first experiment, animals received a shock immediately after placement in the context or after variable delays. Immediate shock produced no context fear learning in lesioned rats or controls. In contrast, delayed shock produced robust context fear learning in both groups. The absence of fear with immediate shock occurs because animals need time to form a representation of the context before shock is presented. The fact that it occurs in both sham and lesioned rats suggests that they learn about the context in a similar manner. However, despite learning about the context in the delay condition, lesioned rats did not acquire as much fear as controls. The second experiment showed that this lesion-induced deficit could be overcome by increasing the number of conditioning trials. Lesioned animals learned normally after multiple shocks, regardless of freezing level or trial spacing. The last experiment showed that animals with complete hippocampus lesions could also learn about the context, although the same lesions produced devastating retrograde amnesia. These results demonstrate that alternative systems can acquire context fear but do so less efficiently than the hippocampus. |
doi_str_mv | 10.1523/JNEUROSCI.2685-05.2006 |
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To better understand this discrepancy, we thoroughly examined the acquisition of context fear in rats with pretraining excitotoxic lesions of the dorsal hippocampus. In the first experiment, animals received a shock immediately after placement in the context or after variable delays. Immediate shock produced no context fear learning in lesioned rats or controls. In contrast, delayed shock produced robust context fear learning in both groups. The absence of fear with immediate shock occurs because animals need time to form a representation of the context before shock is presented. The fact that it occurs in both sham and lesioned rats suggests that they learn about the context in a similar manner. However, despite learning about the context in the delay condition, lesioned rats did not acquire as much fear as controls. The second experiment showed that this lesion-induced deficit could be overcome by increasing the number of conditioning trials. Lesioned animals learned normally after multiple shocks, regardless of freezing level or trial spacing. The last experiment showed that animals with complete hippocampus lesions could also learn about the context, although the same lesions produced devastating retrograde amnesia. These results demonstrate that alternative systems can acquire context fear but do so less efficiently than the hippocampus.</description><identifier>ISSN: 0270-6474</identifier><identifier>EISSN: 1529-2401</identifier><identifier>DOI: 10.1523/JNEUROSCI.2685-05.2006</identifier><identifier>PMID: 16707800</identifier><language>eng</language><publisher>United States: Soc Neuroscience</publisher><subject>Amnesia, Retrograde - etiology ; Amnesia, Retrograde - physiopathology ; Animals ; Avoidance Learning - physiology ; Conditioning (Psychology) - physiology ; Denervation ; Disease Models, Animal ; Electric Stimulation ; Fear - physiology ; Female ; Hippocampus - injuries ; Hippocampus - physiopathology ; Hippocampus - surgery ; Learning - physiology ; Learning Disorders - etiology ; Learning Disorders - physiopathology ; Male ; Memory - physiology ; Memory Disorders - etiology ; Memory Disorders - physiopathology ; Rats ; Rats, Long-Evans</subject><ispartof>The Journal of neuroscience, 2006-05, Vol.26 (20), p.5484-5491</ispartof><rights>Copyright © 2006 Society for Neuroscience 0270-6474/06/265484-08$15.00/0 2006</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c594t-bc3fdd0c6d1eace2b708278aefca42f09d0515ade0b666cdb5c3a62bb67410b63</citedby><cites>FETCH-LOGICAL-c594t-bc3fdd0c6d1eace2b708278aefca42f09d0515ade0b666cdb5c3a62bb67410b63</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/PMC6675287/pdf/$$EPDF$$P50$$Gpubmedcentral$$H</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC6675287/$$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/16707800$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Wiltgen, Brian J</creatorcontrib><creatorcontrib>Sanders, Matthew J</creatorcontrib><creatorcontrib>Anagnostaras, Stephan G</creatorcontrib><creatorcontrib>Sage, Jennifer R</creatorcontrib><creatorcontrib>Fanselow, Michael S</creatorcontrib><title>Context Fear Learning in the Absence of the Hippocampus</title><title>The Journal of neuroscience</title><addtitle>J Neurosci</addtitle><description>Lesions of the rodent hippocampus invariably abolish context fear memories formed in the recent past but do not always prevent new learning. To better understand this discrepancy, we thoroughly examined the acquisition of context fear in rats with pretraining excitotoxic lesions of the dorsal hippocampus. In the first experiment, animals received a shock immediately after placement in the context or after variable delays. Immediate shock produced no context fear learning in lesioned rats or controls. In contrast, delayed shock produced robust context fear learning in both groups. The absence of fear with immediate shock occurs because animals need time to form a representation of the context before shock is presented. The fact that it occurs in both sham and lesioned rats suggests that they learn about the context in a similar manner. However, despite learning about the context in the delay condition, lesioned rats did not acquire as much fear as controls. The second experiment showed that this lesion-induced deficit could be overcome by increasing the number of conditioning trials. Lesioned animals learned normally after multiple shocks, regardless of freezing level or trial spacing. The last experiment showed that animals with complete hippocampus lesions could also learn about the context, although the same lesions produced devastating retrograde amnesia. These results demonstrate that alternative systems can acquire context fear but do so less efficiently than the hippocampus.</description><subject>Amnesia, Retrograde - etiology</subject><subject>Amnesia, Retrograde - physiopathology</subject><subject>Animals</subject><subject>Avoidance Learning - physiology</subject><subject>Conditioning (Psychology) - physiology</subject><subject>Denervation</subject><subject>Disease Models, Animal</subject><subject>Electric Stimulation</subject><subject>Fear - physiology</subject><subject>Female</subject><subject>Hippocampus - injuries</subject><subject>Hippocampus - physiopathology</subject><subject>Hippocampus - surgery</subject><subject>Learning - physiology</subject><subject>Learning Disorders - etiology</subject><subject>Learning Disorders - physiopathology</subject><subject>Male</subject><subject>Memory - physiology</subject><subject>Memory Disorders - etiology</subject><subject>Memory Disorders - physiopathology</subject><subject>Rats</subject><subject>Rats, Long-Evans</subject><issn>0270-6474</issn><issn>1529-2401</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2006</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqFkclOwzAQhi0EgrK8AsoJTiljx0t6QUJV2VSBxHK2HGfSGmUjTim8PS6tWE5cPLLnm18efYQcUxhSwZKz27vJ88P94_hmyGQqYhBDBiC3yCB0RzHjQLfJAJiCWHLF98i-9y8AoICqXbJHpQKVAgyIGjd1j-99dImmi6bhqF09i1wd9XOMLjKPtcWoKb6u165tG2uqduEPyU5hSo9Hm3pAni8nT-PreHp_dTO-mMZWjHgfZzYp8hyszCkaiyxTkDKVGiys4ayAUQ6CCpMjZFJKm2fCJkayLJOK0_CWHJDzdW67yCrMLdZ9Z0rddq4y3YdujNN_O7Wb61nzpqVUgqUqBJxsArrmdYG-15XzFsvS1NgsvJZqlHLG6L8gVYxTJiCAcg3arvG-w-L7NxT0So7-lqNXcjQIvZITBo9_7_IztrERgNM1MHez-dJ1qH1lyjLgVC-XSyZDjhY85ckn8fiaMg</recordid><startdate>20060517</startdate><enddate>20060517</enddate><creator>Wiltgen, Brian J</creator><creator>Sanders, Matthew J</creator><creator>Anagnostaras, Stephan G</creator><creator>Sage, Jennifer R</creator><creator>Fanselow, Michael S</creator><general>Soc Neuroscience</general><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>7TK</scope><scope>7X8</scope><scope>5PM</scope></search><sort><creationdate>20060517</creationdate><title>Context Fear Learning in the Absence of the Hippocampus</title><author>Wiltgen, Brian J ; Sanders, Matthew J ; Anagnostaras, Stephan G ; Sage, Jennifer R ; Fanselow, Michael S</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c594t-bc3fdd0c6d1eace2b708278aefca42f09d0515ade0b666cdb5c3a62bb67410b63</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2006</creationdate><topic>Amnesia, Retrograde - etiology</topic><topic>Amnesia, Retrograde - physiopathology</topic><topic>Animals</topic><topic>Avoidance Learning - physiology</topic><topic>Conditioning (Psychology) - physiology</topic><topic>Denervation</topic><topic>Disease Models, Animal</topic><topic>Electric Stimulation</topic><topic>Fear - physiology</topic><topic>Female</topic><topic>Hippocampus - injuries</topic><topic>Hippocampus - physiopathology</topic><topic>Hippocampus - surgery</topic><topic>Learning - physiology</topic><topic>Learning Disorders - etiology</topic><topic>Learning Disorders - physiopathology</topic><topic>Male</topic><topic>Memory - physiology</topic><topic>Memory Disorders - etiology</topic><topic>Memory Disorders - physiopathology</topic><topic>Rats</topic><topic>Rats, Long-Evans</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Wiltgen, Brian J</creatorcontrib><creatorcontrib>Sanders, Matthew J</creatorcontrib><creatorcontrib>Anagnostaras, Stephan G</creatorcontrib><creatorcontrib>Sage, Jennifer R</creatorcontrib><creatorcontrib>Fanselow, Michael S</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>Neurosciences 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>Wiltgen, Brian J</au><au>Sanders, Matthew J</au><au>Anagnostaras, Stephan G</au><au>Sage, Jennifer R</au><au>Fanselow, Michael S</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Context Fear Learning in the Absence of the Hippocampus</atitle><jtitle>The Journal of neuroscience</jtitle><addtitle>J Neurosci</addtitle><date>2006-05-17</date><risdate>2006</risdate><volume>26</volume><issue>20</issue><spage>5484</spage><epage>5491</epage><pages>5484-5491</pages><issn>0270-6474</issn><eissn>1529-2401</eissn><abstract>Lesions of the rodent hippocampus invariably abolish context fear memories formed in the recent past but do not always prevent new learning. To better understand this discrepancy, we thoroughly examined the acquisition of context fear in rats with pretraining excitotoxic lesions of the dorsal hippocampus. In the first experiment, animals received a shock immediately after placement in the context or after variable delays. Immediate shock produced no context fear learning in lesioned rats or controls. In contrast, delayed shock produced robust context fear learning in both groups. The absence of fear with immediate shock occurs because animals need time to form a representation of the context before shock is presented. The fact that it occurs in both sham and lesioned rats suggests that they learn about the context in a similar manner. However, despite learning about the context in the delay condition, lesioned rats did not acquire as much fear as controls. The second experiment showed that this lesion-induced deficit could be overcome by increasing the number of conditioning trials. Lesioned animals learned normally after multiple shocks, regardless of freezing level or trial spacing. The last experiment showed that animals with complete hippocampus lesions could also learn about the context, although the same lesions produced devastating retrograde amnesia. These results demonstrate that alternative systems can acquire context fear but do so less efficiently than the hippocampus.</abstract><cop>United States</cop><pub>Soc Neuroscience</pub><pmid>16707800</pmid><doi>10.1523/JNEUROSCI.2685-05.2006</doi><tpages>8</tpages><oa>free_for_read</oa></addata></record> |
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subjects | Amnesia, Retrograde - etiology Amnesia, Retrograde - physiopathology Animals Avoidance Learning - physiology Conditioning (Psychology) - physiology Denervation Disease Models, Animal Electric Stimulation Fear - physiology Female Hippocampus - injuries Hippocampus - physiopathology Hippocampus - surgery Learning - physiology Learning Disorders - etiology Learning Disorders - physiopathology Male Memory - physiology Memory Disorders - etiology Memory Disorders - physiopathology Rats Rats, Long-Evans |
title | Context Fear Learning in the Absence of the Hippocampus |
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