Glucocorticoid Enhancement of Memory Requires Arousal-Induced Noradrenergic Activation in the Basolateral Amygdala
Considerable evidence indicates that glucocorticoid hormones enhance the consolidation of long-term memories for emotionally arousing experiences but not that for less arousing or neutral information. However, previous studies have not determined the basis of such arousal-induced selectivity. Here w...
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Veröffentlicht in: | Proceedings of the National Academy of Sciences - PNAS 2006-04, Vol.103 (17), p.6741-6746 |
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description | Considerable evidence indicates that glucocorticoid hormones enhance the consolidation of long-term memories for emotionally arousing experiences but not that for less arousing or neutral information. However, previous studies have not determined the basis of such arousal-induced selectivity. Here we report the finding that endogenous noradrenergic activation of the basolateral complex of the amygdala (BLA) induced by emotional arousal is essential in enabling glucocorticoid memory enhancement. Corticosterone administered immediately after object recognition training enhanced 24-h memory of naive male rats but not that of rats previously habituated to the training context in order to reduce novelty-induced emotional arousal. The β-adrenoceptor antagonist propranolol administered either systemically or into the BLA blocked the corticosterone-induced memory enhancement. Further, in habituated rats, corticosterone activated BLA neurons, as assessed by phosphorylated cAMP response element binding (pCREB) immunoreactivity levels, and enhanced memory only when norepinephrine release was stimulated by administration of the α₂-adrenoceptor antagonist yohimbine. These findings strongly suggest that synergistic actions of glucocorticoids and emotional arousal-induced noradrenergic activation of the BLA constitute a neural mechanism by which glucocorticoids may selectively enhance memory consolidation for emotionally arousing experiences. |
doi_str_mv | 10.1073/pnas.0601874103 |
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However, previous studies have not determined the basis of such arousal-induced selectivity. Here we report the finding that endogenous noradrenergic activation of the basolateral complex of the amygdala (BLA) induced by emotional arousal is essential in enabling glucocorticoid memory enhancement. Corticosterone administered immediately after object recognition training enhanced 24-h memory of naive male rats but not that of rats previously habituated to the training context in order to reduce novelty-induced emotional arousal. The β-adrenoceptor antagonist propranolol administered either systemically or into the BLA blocked the corticosterone-induced memory enhancement. Further, in habituated rats, corticosterone activated BLA neurons, as assessed by phosphorylated cAMP response element binding (pCREB) immunoreactivity levels, and enhanced memory only when norepinephrine release was stimulated by administration of the α₂-adrenoceptor antagonist yohimbine. These findings strongly suggest that synergistic actions of glucocorticoids and emotional arousal-induced noradrenergic activation of the BLA constitute a neural mechanism by which glucocorticoids may selectively enhance memory consolidation for emotionally arousing experiences.</description><identifier>ISSN: 0027-8424</identifier><identifier>EISSN: 1091-6490</identifier><identifier>DOI: 10.1073/pnas.0601874103</identifier><identifier>PMID: 16611726</identifier><language>eng</language><publisher>United States: National Academy of Sciences</publisher><subject>Adrenergic alpha-Antagonists - pharmacology ; Adrenergic beta-Antagonists - pharmacology ; Amygdala ; Amygdala - anatomy & histology ; Amygdala - drug effects ; Amygdala - physiology ; Animals ; Arousal - drug effects ; Arousal - physiology ; Behavioral neuroscience ; Biological Sciences ; Brain ; Corticosterone ; Corticosterone - pharmacology ; Cyclic AMP Response Element-Binding Protein - chemistry ; Cyclic AMP Response Element-Binding Protein - metabolism ; Glucocorticoids ; Habituation ; Habituation, Psychophysiologic - physiology ; Hippocampus ; Hormones ; Male ; Memory ; Memory - drug effects ; Memory - physiology ; Neurosciences ; Norepinephrine ; Norepinephrine - physiology ; Object recognition ; Phosphorylation ; Propranolol - pharmacology ; Rats ; Rats, Sprague-Dawley ; Rodents ; Vehicles ; Yohimbine - pharmacology</subject><ispartof>Proceedings of the National Academy of Sciences - PNAS, 2006-04, Vol.103 (17), p.6741-6746</ispartof><rights>Copyright 2006 National Academy of Sciences of the United States of America</rights><rights>Copyright National Academy of Sciences Apr 25, 2006</rights><rights>2006 by The National Academy of Sciences of the USA 2006</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c594t-90cafb47aa2ecced4a075e1ccbaf9bf10c9ebc6d64978e9824102031c23b6ff33</citedby><cites>FETCH-LOGICAL-c594t-90cafb47aa2ecced4a075e1ccbaf9bf10c9ebc6d64978e9824102031c23b6ff33</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/30052271$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/30052271$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>230,315,728,781,785,804,886,27929,27930,53796,53798,58022,58255</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/16611726$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Roozendaal, Benno</creatorcontrib><creatorcontrib>Okuda, Shoki</creatorcontrib><creatorcontrib>Van der Zee, Eddy A.</creatorcontrib><creatorcontrib>McGaugh, James L.</creatorcontrib><title>Glucocorticoid Enhancement of Memory Requires Arousal-Induced Noradrenergic Activation in the Basolateral Amygdala</title><title>Proceedings of the National Academy of Sciences - PNAS</title><addtitle>Proc Natl Acad Sci U S A</addtitle><description>Considerable evidence indicates that glucocorticoid hormones enhance the consolidation of long-term memories for emotionally arousing experiences but not that for less arousing or neutral information. 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These findings strongly suggest that synergistic actions of glucocorticoids and emotional arousal-induced noradrenergic activation of the BLA constitute a neural mechanism by which glucocorticoids may selectively enhance memory consolidation for emotionally arousing experiences.</description><subject>Adrenergic alpha-Antagonists - pharmacology</subject><subject>Adrenergic beta-Antagonists - pharmacology</subject><subject>Amygdala</subject><subject>Amygdala - anatomy & histology</subject><subject>Amygdala - drug effects</subject><subject>Amygdala - physiology</subject><subject>Animals</subject><subject>Arousal - drug effects</subject><subject>Arousal - physiology</subject><subject>Behavioral neuroscience</subject><subject>Biological Sciences</subject><subject>Brain</subject><subject>Corticosterone</subject><subject>Corticosterone - pharmacology</subject><subject>Cyclic AMP Response Element-Binding Protein - chemistry</subject><subject>Cyclic AMP Response Element-Binding Protein - metabolism</subject><subject>Glucocorticoids</subject><subject>Habituation</subject><subject>Habituation, Psychophysiologic - physiology</subject><subject>Hippocampus</subject><subject>Hormones</subject><subject>Male</subject><subject>Memory</subject><subject>Memory - drug effects</subject><subject>Memory - physiology</subject><subject>Neurosciences</subject><subject>Norepinephrine</subject><subject>Norepinephrine - physiology</subject><subject>Object recognition</subject><subject>Phosphorylation</subject><subject>Propranolol - pharmacology</subject><subject>Rats</subject><subject>Rats, Sprague-Dawley</subject><subject>Rodents</subject><subject>Vehicles</subject><subject>Yohimbine - pharmacology</subject><issn>0027-8424</issn><issn>1091-6490</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2006</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqFkc1v1DAQxS0EokvhzAlkceCWdsZJ7PiCtK36JRWQEJwtx3F2vUrsrZ1U2v8er3bVAhdOPsxvnue9R8h7hDMEUZ5vvU5nwAEbUSGUL8gCQWLBKwkvyQKAiaKpWHVC3qS0AQBZN_CanCDniILxBYk3w2yCCXFyJriOXvm19saO1k809PSrHUPc0R_2YXbRJrqMYU56KO58Nxvb0W8h6i5ab-PKGbo0k3vUkwueOk-ntaUXOoVBTzbqgS7H3arTg35LXvV6SPbd8T0lv66vfl7eFvffb-4ul_eFqWU1FRKM7ttKaM2syX9VGkRt0ZhW97LtEYy0reFd9ioaKxuWA2BQomFly_u-LE_Jl4Pudm5H25lsKZ-httGNOu5U0E79PfFurVbhUWFVN7LGLPD5KBDDw2zTpEaXjB0G7W2OQXEhgWMF_wVRYA2c7RU__QNuwhx9TkExwFI0KFmGzg-QiSGlaPunkxHUvnW1b109t543Pv7p9Jk_1pyBDwdgk6YQn-YlQM2YwPI3iEW1hQ</recordid><startdate>20060425</startdate><enddate>20060425</enddate><creator>Roozendaal, Benno</creator><creator>Okuda, Shoki</creator><creator>Van der Zee, Eddy A.</creator><creator>McGaugh, James L.</creator><general>National Academy of Sciences</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>7QL</scope><scope>7QP</scope><scope>7QR</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TK</scope><scope>7TM</scope><scope>7TO</scope><scope>7U9</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>H94</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope></search><sort><creationdate>20060425</creationdate><title>Glucocorticoid Enhancement of Memory Requires Arousal-Induced Noradrenergic Activation in the Basolateral Amygdala</title><author>Roozendaal, Benno ; Okuda, Shoki ; Van der Zee, Eddy A. ; McGaugh, James L.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c594t-90cafb47aa2ecced4a075e1ccbaf9bf10c9ebc6d64978e9824102031c23b6ff33</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2006</creationdate><topic>Adrenergic alpha-Antagonists - pharmacology</topic><topic>Adrenergic beta-Antagonists - pharmacology</topic><topic>Amygdala</topic><topic>Amygdala - anatomy & histology</topic><topic>Amygdala - drug effects</topic><topic>Amygdala - physiology</topic><topic>Animals</topic><topic>Arousal - drug effects</topic><topic>Arousal - physiology</topic><topic>Behavioral neuroscience</topic><topic>Biological Sciences</topic><topic>Brain</topic><topic>Corticosterone</topic><topic>Corticosterone - pharmacology</topic><topic>Cyclic AMP Response Element-Binding Protein - chemistry</topic><topic>Cyclic AMP Response Element-Binding Protein - metabolism</topic><topic>Glucocorticoids</topic><topic>Habituation</topic><topic>Habituation, Psychophysiologic - physiology</topic><topic>Hippocampus</topic><topic>Hormones</topic><topic>Male</topic><topic>Memory</topic><topic>Memory - drug effects</topic><topic>Memory - physiology</topic><topic>Neurosciences</topic><topic>Norepinephrine</topic><topic>Norepinephrine - physiology</topic><topic>Object recognition</topic><topic>Phosphorylation</topic><topic>Propranolol - pharmacology</topic><topic>Rats</topic><topic>Rats, Sprague-Dawley</topic><topic>Rodents</topic><topic>Vehicles</topic><topic>Yohimbine - pharmacology</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Roozendaal, Benno</creatorcontrib><creatorcontrib>Okuda, Shoki</creatorcontrib><creatorcontrib>Van der Zee, Eddy A.</creatorcontrib><creatorcontrib>McGaugh, James L.</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>Bacteriology Abstracts (Microbiology B)</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Ecology Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Immunology 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>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Engineering Research Database</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Proceedings of the National Academy of Sciences - PNAS</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Roozendaal, Benno</au><au>Okuda, Shoki</au><au>Van der Zee, Eddy A.</au><au>McGaugh, James L.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Glucocorticoid Enhancement of Memory Requires Arousal-Induced Noradrenergic Activation in the Basolateral Amygdala</atitle><jtitle>Proceedings of the National Academy of Sciences - PNAS</jtitle><addtitle>Proc Natl Acad Sci U S A</addtitle><date>2006-04-25</date><risdate>2006</risdate><volume>103</volume><issue>17</issue><spage>6741</spage><epage>6746</epage><pages>6741-6746</pages><issn>0027-8424</issn><eissn>1091-6490</eissn><abstract>Considerable evidence indicates that glucocorticoid hormones enhance the consolidation of long-term memories for emotionally arousing experiences but not that for less arousing or neutral information. However, previous studies have not determined the basis of such arousal-induced selectivity. Here we report the finding that endogenous noradrenergic activation of the basolateral complex of the amygdala (BLA) induced by emotional arousal is essential in enabling glucocorticoid memory enhancement. Corticosterone administered immediately after object recognition training enhanced 24-h memory of naive male rats but not that of rats previously habituated to the training context in order to reduce novelty-induced emotional arousal. The β-adrenoceptor antagonist propranolol administered either systemically or into the BLA blocked the corticosterone-induced memory enhancement. Further, in habituated rats, corticosterone activated BLA neurons, as assessed by phosphorylated cAMP response element binding (pCREB) immunoreactivity levels, and enhanced memory only when norepinephrine release was stimulated by administration of the α₂-adrenoceptor antagonist yohimbine. These findings strongly suggest that synergistic actions of glucocorticoids and emotional arousal-induced noradrenergic activation of the BLA constitute a neural mechanism by which glucocorticoids may selectively enhance memory consolidation for emotionally arousing experiences.</abstract><cop>United States</cop><pub>National Academy of Sciences</pub><pmid>16611726</pmid><doi>10.1073/pnas.0601874103</doi><tpages>6</tpages><oa>free_for_read</oa></addata></record> |
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subjects | Adrenergic alpha-Antagonists - pharmacology Adrenergic beta-Antagonists - pharmacology Amygdala Amygdala - anatomy & histology Amygdala - drug effects Amygdala - physiology Animals Arousal - drug effects Arousal - physiology Behavioral neuroscience Biological Sciences Brain Corticosterone Corticosterone - pharmacology Cyclic AMP Response Element-Binding Protein - chemistry Cyclic AMP Response Element-Binding Protein - metabolism Glucocorticoids Habituation Habituation, Psychophysiologic - physiology Hippocampus Hormones Male Memory Memory - drug effects Memory - physiology Neurosciences Norepinephrine Norepinephrine - physiology Object recognition Phosphorylation Propranolol - pharmacology Rats Rats, Sprague-Dawley Rodents Vehicles Yohimbine - pharmacology |
title | Glucocorticoid Enhancement of Memory Requires Arousal-Induced Noradrenergic Activation in the Basolateral Amygdala |
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