Anti-inflammatory drugs prevent memory and hippocampal plasticity deficits following initial binge-like alcohol exposure in adolescent male rats
Rationale Binge drinking during adolescence impairs learning and memory on the long term, and many studies suggest a role of neuroinflammation. However, whether neuroinflammation occurs after the very first exposures to alcohol remains unclear, while initial alcohol exposure impairs learning for sev...
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| Veröffentlicht in: | Psychopharmacology 2022-07, Vol.239 (7), p.2245-2262 |
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| creator | Deschamps, Chloé Uyttersprot, Floriane Debris, Margot Marié, Constance Fouquet, Grégory Marcq, Ingrid Vilpoux, Catherine Naassila, Mickael Pierrefiche, Olivier |
| description | Rationale
Binge drinking during adolescence impairs learning and memory on the long term, and many studies suggest a role of neuroinflammation. However, whether neuroinflammation occurs after the very first exposures to alcohol remains unclear, while initial alcohol exposure impairs learning for several days in male rats.
Objectives
To investigate the role of neuroinflammation in the effects of only two binge-like episodes on learning and on neuronal plasticity in adolescent male rat hippocampus.
Methods
Animals received two ethanol i.p. injections (3 g/kg) 9 h apart. Forty-eight hours later, we recorded long-term depression (LTD) and potentiation (LTP) in CA1 area of hippocampus slices. In isolated CA1, we measured immunolabelings for microglial activation and Toll-like receptor 4 (TLR4) and mRNA levels for several cytokines.
Results
Forty-eight hours after the two binges, rats performed worse than control rats in novel object recognition, LTD was reduced, LTP was increased, and excitatory neurotransmission was more sensitive to an antagonist of the GluN2B subunit of the NMDA receptor. Exposure to ethanol with minocycline or indomethacin, two anti-inflammatory drugs, or with a TLR4 antagonist, prevented all effects of ethanol. Immunolabelings at 48 h showed a reduction of neuronal TLR4 that was prevented by minocycline pretreatment, while microglial reactivity was undetected and inflammatory cytokines mRNA levels were unchanged.
Conclusion
Two binge-like ethanol exposures during adolescence in rat involved neuroinflammation leading to changes in TLR4 expression and in GluN2B functioning inducing disturbances in synaptic plasticity and cognitive deficits. Anti-inflammatory drugs are good candidates to prevent brain function and memory deficits induced by few binge-drinking episodes. |
| doi_str_mv | 10.1007/s00213-022-06112-w |
| format | Article |
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Binge drinking during adolescence impairs learning and memory on the long term, and many studies suggest a role of neuroinflammation. However, whether neuroinflammation occurs after the very first exposures to alcohol remains unclear, while initial alcohol exposure impairs learning for several days in male rats.
Objectives
To investigate the role of neuroinflammation in the effects of only two binge-like episodes on learning and on neuronal plasticity in adolescent male rat hippocampus.
Methods
Animals received two ethanol i.p. injections (3 g/kg) 9 h apart. Forty-eight hours later, we recorded long-term depression (LTD) and potentiation (LTP) in CA1 area of hippocampus slices. In isolated CA1, we measured immunolabelings for microglial activation and Toll-like receptor 4 (TLR4) and mRNA levels for several cytokines.
Results
Forty-eight hours after the two binges, rats performed worse than control rats in novel object recognition, LTD was reduced, LTP was increased, and excitatory neurotransmission was more sensitive to an antagonist of the GluN2B subunit of the NMDA receptor. Exposure to ethanol with minocycline or indomethacin, two anti-inflammatory drugs, or with a TLR4 antagonist, prevented all effects of ethanol. Immunolabelings at 48 h showed a reduction of neuronal TLR4 that was prevented by minocycline pretreatment, while microglial reactivity was undetected and inflammatory cytokines mRNA levels were unchanged.
Conclusion
Two binge-like ethanol exposures during adolescence in rat involved neuroinflammation leading to changes in TLR4 expression and in GluN2B functioning inducing disturbances in synaptic plasticity and cognitive deficits. Anti-inflammatory drugs are good candidates to prevent brain function and memory deficits induced by few binge-drinking episodes.</description><identifier>ISSN: 0033-3158</identifier><identifier>EISSN: 1432-2072</identifier><identifier>DOI: 10.1007/s00213-022-06112-w</identifier><identifier>PMID: 35314896</identifier><language>eng</language><publisher>Berlin/Heidelberg: Springer Berlin Heidelberg</publisher><subject>Adolescents ; Alcohol ; Alcohol, Denatured ; Analysis ; Anti-inflammatory agents ; Antibiotics ; Biomedical and Life Sciences ; Biomedicine ; Child development ; Cognitive ability ; Cytokines ; Depression, Mental ; Dosage and administration ; Drinking behavior ; Drug development ; Ethanol ; Glutamic acid receptors (ionotropic) ; Hippocampal plasticity ; Hippocampus ; Human health and pathology ; Immunohistochemistry ; Indomethacin ; Inflammation ; Learning ; Life Sciences ; Long-term depression ; Long-term potentiation ; Memory ; Minocycline ; mRNA ; N-Methyl-D-aspartic acid receptors ; Neuroplasticity ; Neurosciences ; Neurotransmission ; Original Investigation ; Pattern recognition ; Pharmacology/Toxicology ; Psychiatry ; Psychological aspects ; Rodents ; Teenagers ; TLR4 protein ; Toll-like receptors</subject><ispartof>Psychopharmacology, 2022-07, Vol.239 (7), p.2245-2262</ispartof><rights>The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature 2022</rights><rights>2022. The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature.</rights><rights>COPYRIGHT 2022 Springer</rights><rights>The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature 2022.</rights><rights>Distributed under a Creative Commons Attribution 4.0 International License</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c406t-8c71047c4886df1c6198a40f2f530e2490e67ba7fd315cb09ee1df6744b477243</citedby><cites>FETCH-LOGICAL-c406t-8c71047c4886df1c6198a40f2f530e2490e67ba7fd315cb09ee1df6744b477243</cites><orcidid>0000-0003-1427-9332 ; 0009-0008-0384-4344 ; 0000-0003-0790-1197 ; 0000-0002-9788-0918 ; 0000-0003-2462-2878 ; 0000-0002-4031-224X</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://link.springer.com/content/pdf/10.1007/s00213-022-06112-w$$EPDF$$P50$$Gspringer$$H</linktopdf><linktohtml>$$Uhttps://link.springer.com/10.1007/s00213-022-06112-w$$EHTML$$P50$$Gspringer$$H</linktohtml><link.rule.ids>230,314,780,784,885,27924,27925,41488,42557,51319</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/35314896$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://u-picardie.hal.science/hal-03703787$$DView record in HAL$$Hfree_for_read</backlink></links><search><creatorcontrib>Deschamps, Chloé</creatorcontrib><creatorcontrib>Uyttersprot, Floriane</creatorcontrib><creatorcontrib>Debris, Margot</creatorcontrib><creatorcontrib>Marié, Constance</creatorcontrib><creatorcontrib>Fouquet, Grégory</creatorcontrib><creatorcontrib>Marcq, Ingrid</creatorcontrib><creatorcontrib>Vilpoux, Catherine</creatorcontrib><creatorcontrib>Naassila, Mickael</creatorcontrib><creatorcontrib>Pierrefiche, Olivier</creatorcontrib><title>Anti-inflammatory drugs prevent memory and hippocampal plasticity deficits following initial binge-like alcohol exposure in adolescent male rats</title><title>Psychopharmacology</title><addtitle>Psychopharmacology</addtitle><addtitle>Psychopharmacology (Berl)</addtitle><description>Rationale
Binge drinking during adolescence impairs learning and memory on the long term, and many studies suggest a role of neuroinflammation. However, whether neuroinflammation occurs after the very first exposures to alcohol remains unclear, while initial alcohol exposure impairs learning for several days in male rats.
Objectives
To investigate the role of neuroinflammation in the effects of only two binge-like episodes on learning and on neuronal plasticity in adolescent male rat hippocampus.
Methods
Animals received two ethanol i.p. injections (3 g/kg) 9 h apart. Forty-eight hours later, we recorded long-term depression (LTD) and potentiation (LTP) in CA1 area of hippocampus slices. In isolated CA1, we measured immunolabelings for microglial activation and Toll-like receptor 4 (TLR4) and mRNA levels for several cytokines.
Results
Forty-eight hours after the two binges, rats performed worse than control rats in novel object recognition, LTD was reduced, LTP was increased, and excitatory neurotransmission was more sensitive to an antagonist of the GluN2B subunit of the NMDA receptor. Exposure to ethanol with minocycline or indomethacin, two anti-inflammatory drugs, or with a TLR4 antagonist, prevented all effects of ethanol. Immunolabelings at 48 h showed a reduction of neuronal TLR4 that was prevented by minocycline pretreatment, while microglial reactivity was undetected and inflammatory cytokines mRNA levels were unchanged.
Conclusion
Two binge-like ethanol exposures during adolescence in rat involved neuroinflammation leading to changes in TLR4 expression and in GluN2B functioning inducing disturbances in synaptic plasticity and cognitive deficits. Anti-inflammatory drugs are good candidates to prevent brain function and memory deficits induced by few binge-drinking episodes.</description><subject>Adolescents</subject><subject>Alcohol</subject><subject>Alcohol, Denatured</subject><subject>Analysis</subject><subject>Anti-inflammatory agents</subject><subject>Antibiotics</subject><subject>Biomedical and Life Sciences</subject><subject>Biomedicine</subject><subject>Child development</subject><subject>Cognitive ability</subject><subject>Cytokines</subject><subject>Depression, Mental</subject><subject>Dosage and administration</subject><subject>Drinking behavior</subject><subject>Drug development</subject><subject>Ethanol</subject><subject>Glutamic acid receptors (ionotropic)</subject><subject>Hippocampal plasticity</subject><subject>Hippocampus</subject><subject>Human health and pathology</subject><subject>Immunohistochemistry</subject><subject>Indomethacin</subject><subject>Inflammation</subject><subject>Learning</subject><subject>Life Sciences</subject><subject>Long-term depression</subject><subject>Long-term potentiation</subject><subject>Memory</subject><subject>Minocycline</subject><subject>mRNA</subject><subject>N-Methyl-D-aspartic acid receptors</subject><subject>Neuroplasticity</subject><subject>Neurosciences</subject><subject>Neurotransmission</subject><subject>Original Investigation</subject><subject>Pattern recognition</subject><subject>Pharmacology/Toxicology</subject><subject>Psychiatry</subject><subject>Psychological aspects</subject><subject>Rodents</subject><subject>Teenagers</subject><subject>TLR4 protein</subject><subject>Toll-like receptors</subject><issn>0033-3158</issn><issn>1432-2072</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2022</creationdate><recordtype>article</recordtype><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>GNUQQ</sourceid><recordid>eNp9ks9u1DAQxi0EosvCC3BAlrjAIcX_YifHVQUUaSUucLYcx9l1ceJgJ136Fjwyk6a0AiEcS4nHv5n4G38IvaTknBKi3mVCGOUFYawgklJWnB6hDRWcFYwo9hhtCOG84LSsztCznK8IDFGJp-iMl5yKqpYb9HM3TL7wQxdM35spphvcpvmQ8ZjctRsm3Lt-CZqhxUc_jtGafjQBj8HkyVs_Ae-65SPjLoYQT344YD_4yQPVwMIVwX9z2AQbjzFg92OMeU4OGGzaGFy2t78xweFkpvwcPelMyO7F3XuLvn54_-Xisth__vjpYrcvrCByKiqrKBHKiqqSbUetpHVlBOlYV3LimKiJk6oxqmtBv21I7RxtO6mEaIRSTPAtervWPZqgx-R7k250NF5f7vZ6iRGuYFbqmgL7ZmXHFL_PLk-693DsEMzg4pw1k4JWkito6xa9_gu9inMaQAlQStWlqKV4oA4gW0P345SMXYrqnSKqpEJWS63zf1DwtK73Ng7Qd4j_kcDWBJtizsl198Io0Ytl9GoZDZbRt5bRJ0h6dXfiuelde5_y2yMA8BXIsAX3mR4k_afsL9jezH0</recordid><startdate>20220701</startdate><enddate>20220701</enddate><creator>Deschamps, Chloé</creator><creator>Uyttersprot, Floriane</creator><creator>Debris, Margot</creator><creator>Marié, Constance</creator><creator>Fouquet, Grégory</creator><creator>Marcq, Ingrid</creator><creator>Vilpoux, Catherine</creator><creator>Naassila, Mickael</creator><creator>Pierrefiche, Olivier</creator><general>Springer Berlin Heidelberg</general><general>Springer</general><general>Springer Nature B.V</general><general>Springer 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drugs prevent memory and hippocampal plasticity deficits following initial binge-like alcohol exposure in adolescent male rats</title><author>Deschamps, Chloé ; Uyttersprot, Floriane ; Debris, Margot ; Marié, Constance ; Fouquet, Grégory ; Marcq, Ingrid ; Vilpoux, Catherine ; Naassila, Mickael ; Pierrefiche, Olivier</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c406t-8c71047c4886df1c6198a40f2f530e2490e67ba7fd315cb09ee1df6744b477243</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2022</creationdate><topic>Adolescents</topic><topic>Alcohol</topic><topic>Alcohol, Denatured</topic><topic>Analysis</topic><topic>Anti-inflammatory agents</topic><topic>Antibiotics</topic><topic>Biomedical and Life Sciences</topic><topic>Biomedicine</topic><topic>Child development</topic><topic>Cognitive ability</topic><topic>Cytokines</topic><topic>Depression, Mental</topic><topic>Dosage and administration</topic><topic>Drinking behavior</topic><topic>Drug development</topic><topic>Ethanol</topic><topic>Glutamic acid receptors (ionotropic)</topic><topic>Hippocampal plasticity</topic><topic>Hippocampus</topic><topic>Human health and pathology</topic><topic>Immunohistochemistry</topic><topic>Indomethacin</topic><topic>Inflammation</topic><topic>Learning</topic><topic>Life Sciences</topic><topic>Long-term depression</topic><topic>Long-term potentiation</topic><topic>Memory</topic><topic>Minocycline</topic><topic>mRNA</topic><topic>N-Methyl-D-aspartic acid receptors</topic><topic>Neuroplasticity</topic><topic>Neurosciences</topic><topic>Neurotransmission</topic><topic>Original Investigation</topic><topic>Pattern recognition</topic><topic>Pharmacology/Toxicology</topic><topic>Psychiatry</topic><topic>Psychological aspects</topic><topic>Rodents</topic><topic>Teenagers</topic><topic>TLR4 protein</topic><topic>Toll-like receptors</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Deschamps, Chloé</creatorcontrib><creatorcontrib>Uyttersprot, Floriane</creatorcontrib><creatorcontrib>Debris, Margot</creatorcontrib><creatorcontrib>Marié, Constance</creatorcontrib><creatorcontrib>Fouquet, Grégory</creatorcontrib><creatorcontrib>Marcq, Ingrid</creatorcontrib><creatorcontrib>Vilpoux, Catherine</creatorcontrib><creatorcontrib>Naassila, Mickael</creatorcontrib><creatorcontrib>Pierrefiche, Olivier</creatorcontrib><collection>PubMed</collection><collection>CrossRef</collection><collection>ProQuest Central (Corporate)</collection><collection>Animal Behavior Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Nursing & Allied Health Database</collection><collection>Neurosciences Abstracts</collection><collection>Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Medical 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(Alumni)</collection><collection>Nursing & Allied Health Database (Alumni Edition)</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>Psychology Database</collection><collection>Nursing & Allied Health Premium</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>ProQuest Central China</collection><collection>ProQuest One Psychology</collection><collection>ProQuest Central Basic</collection><collection>MEDLINE - Academic</collection><collection>Hyper Article en Ligne (HAL)</collection><jtitle>Psychopharmacology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Deschamps, Chloé</au><au>Uyttersprot, Floriane</au><au>Debris, Margot</au><au>Marié, Constance</au><au>Fouquet, Grégory</au><au>Marcq, Ingrid</au><au>Vilpoux, Catherine</au><au>Naassila, Mickael</au><au>Pierrefiche, Olivier</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Anti-inflammatory drugs prevent memory and hippocampal plasticity deficits following initial binge-like alcohol exposure in adolescent male rats</atitle><jtitle>Psychopharmacology</jtitle><stitle>Psychopharmacology</stitle><addtitle>Psychopharmacology (Berl)</addtitle><date>2022-07-01</date><risdate>2022</risdate><volume>239</volume><issue>7</issue><spage>2245</spage><epage>2262</epage><pages>2245-2262</pages><issn>0033-3158</issn><eissn>1432-2072</eissn><abstract>Rationale
Binge drinking during adolescence impairs learning and memory on the long term, and many studies suggest a role of neuroinflammation. However, whether neuroinflammation occurs after the very first exposures to alcohol remains unclear, while initial alcohol exposure impairs learning for several days in male rats.
Objectives
To investigate the role of neuroinflammation in the effects of only two binge-like episodes on learning and on neuronal plasticity in adolescent male rat hippocampus.
Methods
Animals received two ethanol i.p. injections (3 g/kg) 9 h apart. Forty-eight hours later, we recorded long-term depression (LTD) and potentiation (LTP) in CA1 area of hippocampus slices. In isolated CA1, we measured immunolabelings for microglial activation and Toll-like receptor 4 (TLR4) and mRNA levels for several cytokines.
Results
Forty-eight hours after the two binges, rats performed worse than control rats in novel object recognition, LTD was reduced, LTP was increased, and excitatory neurotransmission was more sensitive to an antagonist of the GluN2B subunit of the NMDA receptor. Exposure to ethanol with minocycline or indomethacin, two anti-inflammatory drugs, or with a TLR4 antagonist, prevented all effects of ethanol. Immunolabelings at 48 h showed a reduction of neuronal TLR4 that was prevented by minocycline pretreatment, while microglial reactivity was undetected and inflammatory cytokines mRNA levels were unchanged.
Conclusion
Two binge-like ethanol exposures during adolescence in rat involved neuroinflammation leading to changes in TLR4 expression and in GluN2B functioning inducing disturbances in synaptic plasticity and cognitive deficits. Anti-inflammatory drugs are good candidates to prevent brain function and memory deficits induced by few binge-drinking episodes.</abstract><cop>Berlin/Heidelberg</cop><pub>Springer Berlin Heidelberg</pub><pmid>35314896</pmid><doi>10.1007/s00213-022-06112-w</doi><tpages>18</tpages><orcidid>https://orcid.org/0000-0003-1427-9332</orcidid><orcidid>https://orcid.org/0009-0008-0384-4344</orcidid><orcidid>https://orcid.org/0000-0003-0790-1197</orcidid><orcidid>https://orcid.org/0000-0002-9788-0918</orcidid><orcidid>https://orcid.org/0000-0003-2462-2878</orcidid><orcidid>https://orcid.org/0000-0002-4031-224X</orcidid></addata></record> |
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| ispartof | Psychopharmacology, 2022-07, Vol.239 (7), p.2245-2262 |
| issn | 0033-3158 1432-2072 |
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| source | SpringerNature Journals |
| subjects | Adolescents Alcohol Alcohol, Denatured Analysis Anti-inflammatory agents Antibiotics Biomedical and Life Sciences Biomedicine Child development Cognitive ability Cytokines Depression, Mental Dosage and administration Drinking behavior Drug development Ethanol Glutamic acid receptors (ionotropic) Hippocampal plasticity Hippocampus Human health and pathology Immunohistochemistry Indomethacin Inflammation Learning Life Sciences Long-term depression Long-term potentiation Memory Minocycline mRNA N-Methyl-D-aspartic acid receptors Neuroplasticity Neurosciences Neurotransmission Original Investigation Pattern recognition Pharmacology/Toxicology Psychiatry Psychological aspects Rodents Teenagers TLR4 protein Toll-like receptors |
| title | Anti-inflammatory drugs prevent memory and hippocampal plasticity deficits following initial binge-like alcohol exposure in adolescent male rats |
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