Impaired synaptic transmission in dorsal dentate gyrus increases impulsive alcohol seeking

Both human and animal studies indicate that the dentate gyrus (DG) of the hippocampus is highly exploited by drug and alcohol abuse. Yet, it is poorly understood how DG dysfunction affects addiction-related behaviors. Here, we used an animal model of alcohol use disorder (AUD) in automated IntelliCa...

Ausführliche Beschreibung

Gespeichert in:
Bibliographische Detailangaben
Veröffentlicht in:Neuropsychopharmacology (New York, N.Y.) N.Y.), 2023-02, Vol.48 (3), p.436-447
Hauptverfasser: Nalberczak-Skóra, Maria, Beroun, Anna, Skonieczna, Edyta, Cały, Anna, Ziółkowska, Magdalena, Pagano, Roberto, Taheri, Pegah, Kalita, Katarzyna, Salamian, Ahmad, Radwanska, Kasia
Format: Artikel
Sprache:eng
Schlagworte:
Online-Zugang:Volltext
Tags: Tag hinzufügen
Keine Tags, Fügen Sie den ersten Tag hinzu!
container_end_page 447
container_issue 3
container_start_page 436
container_title Neuropsychopharmacology (New York, N.Y.)
container_volume 48
creator Nalberczak-Skóra, Maria
Beroun, Anna
Skonieczna, Edyta
Cały, Anna
Ziółkowska, Magdalena
Pagano, Roberto
Taheri, Pegah
Kalita, Katarzyna
Salamian, Ahmad
Radwanska, Kasia
description Both human and animal studies indicate that the dentate gyrus (DG) of the hippocampus is highly exploited by drug and alcohol abuse. Yet, it is poorly understood how DG dysfunction affects addiction-related behaviors. Here, we used an animal model of alcohol use disorder (AUD) in automated IntelliCages and performed local genetic manipulation to investigate how synaptic transmission in the dorsal DG (dDG) affects alcohol-related behaviors. We show that a cue light induces potentiation-like plasticity of dDG synapses in alcohol-naive mice. This process is impaired in mice trained to drink alcohol. Acamprosate (ACA), a drug that reduces alcohol relapse, rescues the impairment of dDG synaptic transmission in alcohol mice. A molecular manipulation that reduces dDG synaptic AMPAR and NMDAR levels increases impulsive alcohol seeking during cue relapse (CR) in alcohol mice but does not affect alcohol reward, motivation or craving. These findings suggest that hindered dDG synaptic transmission specifically underlies impulsive alcohol seeking induced by alcohol cues, a core symptom of AUD.
doi_str_mv 10.1038/s41386-022-01464-5
format Article
fullrecord <record><control><sourceid>proquest_pubme</sourceid><recordid>TN_cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_9852589</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><sourcerecordid>2720424366</sourcerecordid><originalsourceid>FETCH-LOGICAL-c360t-cf6c915b9616bfbb57bc0d678fc939193d9432e0ec6b57acea85347151c347ef3</originalsourceid><addsrcrecordid>eNpdkU2LFDEQhoMo7jj6BzxIgxcvrfnu5CLI4sfCgheFxUtIp6tns3Ynbap7Yf690VkX9VRF1VtFvfUQ8pzR14wK8wYlE0a3lPOWMqllqx6QHeskbbWQVw_JjhorWibE1Rl5gnhDKVOdNo_JmdDMcGvsjny7mBcfCwwNHpNf1hiatfiEc0SMOTUxNUMu6KdmgLT6FZrDsWxY66GAR6jZvGwTxlto_BTydZ4aBPge0-EpeTT6CeHZXdyTrx_efzn_1F5-_nhx_u6yDULTtQ2jDpap3mqm-7HvVdcHOujOjMEKy6wYrBQcKARdez6AN0rIjikWaoBR7Mnb095l62cYQr2z-MktJc6-HF320f3bSfHaHfKts0ZxVV-0J6_uFpT8YwNcXXUfYJp8gryh4x2nkkuhdZW-_E96k7eSqr2q0toyTmlXVfykCiUjFhjvj2HU_ULnTuhcRed-o3OqDr3428b9yB9W4idBdpc8</addsrcrecordid><sourcetype>Open Access Repository</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>2766912007</pqid></control><display><type>article</type><title>Impaired synaptic transmission in dorsal dentate gyrus increases impulsive alcohol seeking</title><source>PubMed (Medline)</source><source>MEDLINE</source><source>SpringerLink (Online service)</source><source>EZB Electronic Journals Library</source><creator>Nalberczak-Skóra, Maria ; Beroun, Anna ; Skonieczna, Edyta ; Cały, Anna ; Ziółkowska, Magdalena ; Pagano, Roberto ; Taheri, Pegah ; Kalita, Katarzyna ; Salamian, Ahmad ; Radwanska, Kasia</creator><creatorcontrib>Nalberczak-Skóra, Maria ; Beroun, Anna ; Skonieczna, Edyta ; Cały, Anna ; Ziółkowska, Magdalena ; Pagano, Roberto ; Taheri, Pegah ; Kalita, Katarzyna ; Salamian, Ahmad ; Radwanska, Kasia</creatorcontrib><description>Both human and animal studies indicate that the dentate gyrus (DG) of the hippocampus is highly exploited by drug and alcohol abuse. Yet, it is poorly understood how DG dysfunction affects addiction-related behaviors. Here, we used an animal model of alcohol use disorder (AUD) in automated IntelliCages and performed local genetic manipulation to investigate how synaptic transmission in the dorsal DG (dDG) affects alcohol-related behaviors. We show that a cue light induces potentiation-like plasticity of dDG synapses in alcohol-naive mice. This process is impaired in mice trained to drink alcohol. Acamprosate (ACA), a drug that reduces alcohol relapse, rescues the impairment of dDG synaptic transmission in alcohol mice. A molecular manipulation that reduces dDG synaptic AMPAR and NMDAR levels increases impulsive alcohol seeking during cue relapse (CR) in alcohol mice but does not affect alcohol reward, motivation or craving. These findings suggest that hindered dDG synaptic transmission specifically underlies impulsive alcohol seeking induced by alcohol cues, a core symptom of AUD.</description><identifier>ISSN: 0893-133X</identifier><identifier>EISSN: 1740-634X</identifier><identifier>DOI: 10.1038/s41386-022-01464-5</identifier><identifier>PMID: 36182989</identifier><language>eng</language><publisher>England: Nature Publishing Group</publisher><subject>Addictions ; Alcohol ; Alcohol abuse ; Alcoholism - genetics ; Animal models ; Animals ; Dentate Gyrus ; Drug abuse ; Ethanol - pharmacology ; Glutamate receptors ; Humans ; Impulsivity ; Mice ; Motivation ; N-Methyl-D-aspartic acid receptors ; Potentiation ; Recurrence ; Reinforcement ; Synapses ; Synaptic Transmission ; α-Amino-3-hydroxy-5-methyl-4-isoxazole propionic acid receptors</subject><ispartof>Neuropsychopharmacology (New York, N.Y.), 2023-02, Vol.48 (3), p.436-447</ispartof><rights>2022. The Author(s).</rights><rights>The Author(s) 2022. This work is published under http://creativecommons.org/licenses/by/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>The Author(s) 2022</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c360t-cf6c915b9616bfbb57bc0d678fc939193d9432e0ec6b57acea85347151c347ef3</citedby><cites>FETCH-LOGICAL-c360t-cf6c915b9616bfbb57bc0d678fc939193d9432e0ec6b57acea85347151c347ef3</cites><orcidid>0000-0001-7445-6180 ; 0000-0003-2841-9228 ; 0000-0002-7687-4471</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/PMC9852589/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC9852589/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,881,27901,27902,53766,53768</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/36182989$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Nalberczak-Skóra, Maria</creatorcontrib><creatorcontrib>Beroun, Anna</creatorcontrib><creatorcontrib>Skonieczna, Edyta</creatorcontrib><creatorcontrib>Cały, Anna</creatorcontrib><creatorcontrib>Ziółkowska, Magdalena</creatorcontrib><creatorcontrib>Pagano, Roberto</creatorcontrib><creatorcontrib>Taheri, Pegah</creatorcontrib><creatorcontrib>Kalita, Katarzyna</creatorcontrib><creatorcontrib>Salamian, Ahmad</creatorcontrib><creatorcontrib>Radwanska, Kasia</creatorcontrib><title>Impaired synaptic transmission in dorsal dentate gyrus increases impulsive alcohol seeking</title><title>Neuropsychopharmacology (New York, N.Y.)</title><addtitle>Neuropsychopharmacology</addtitle><description>Both human and animal studies indicate that the dentate gyrus (DG) of the hippocampus is highly exploited by drug and alcohol abuse. Yet, it is poorly understood how DG dysfunction affects addiction-related behaviors. Here, we used an animal model of alcohol use disorder (AUD) in automated IntelliCages and performed local genetic manipulation to investigate how synaptic transmission in the dorsal DG (dDG) affects alcohol-related behaviors. We show that a cue light induces potentiation-like plasticity of dDG synapses in alcohol-naive mice. This process is impaired in mice trained to drink alcohol. Acamprosate (ACA), a drug that reduces alcohol relapse, rescues the impairment of dDG synaptic transmission in alcohol mice. A molecular manipulation that reduces dDG synaptic AMPAR and NMDAR levels increases impulsive alcohol seeking during cue relapse (CR) in alcohol mice but does not affect alcohol reward, motivation or craving. These findings suggest that hindered dDG synaptic transmission specifically underlies impulsive alcohol seeking induced by alcohol cues, a core symptom of AUD.</description><subject>Addictions</subject><subject>Alcohol</subject><subject>Alcohol abuse</subject><subject>Alcoholism - genetics</subject><subject>Animal models</subject><subject>Animals</subject><subject>Dentate Gyrus</subject><subject>Drug abuse</subject><subject>Ethanol - pharmacology</subject><subject>Glutamate receptors</subject><subject>Humans</subject><subject>Impulsivity</subject><subject>Mice</subject><subject>Motivation</subject><subject>N-Methyl-D-aspartic acid receptors</subject><subject>Potentiation</subject><subject>Recurrence</subject><subject>Reinforcement</subject><subject>Synapses</subject><subject>Synaptic Transmission</subject><subject>α-Amino-3-hydroxy-5-methyl-4-isoxazole propionic acid receptors</subject><issn>0893-133X</issn><issn>1740-634X</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2023</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>BENPR</sourceid><recordid>eNpdkU2LFDEQhoMo7jj6BzxIgxcvrfnu5CLI4sfCgheFxUtIp6tns3Ynbap7Yf690VkX9VRF1VtFvfUQ8pzR14wK8wYlE0a3lPOWMqllqx6QHeskbbWQVw_JjhorWibE1Rl5gnhDKVOdNo_JmdDMcGvsjny7mBcfCwwNHpNf1hiatfiEc0SMOTUxNUMu6KdmgLT6FZrDsWxY66GAR6jZvGwTxlto_BTydZ4aBPge0-EpeTT6CeHZXdyTrx_efzn_1F5-_nhx_u6yDULTtQ2jDpap3mqm-7HvVdcHOujOjMEKy6wYrBQcKARdez6AN0rIjikWaoBR7Mnb095l62cYQr2z-MktJc6-HF320f3bSfHaHfKts0ZxVV-0J6_uFpT8YwNcXXUfYJp8gryh4x2nkkuhdZW-_E96k7eSqr2q0toyTmlXVfykCiUjFhjvj2HU_ULnTuhcRed-o3OqDr3428b9yB9W4idBdpc8</recordid><startdate>20230201</startdate><enddate>20230201</enddate><creator>Nalberczak-Skóra, Maria</creator><creator>Beroun, Anna</creator><creator>Skonieczna, Edyta</creator><creator>Cały, Anna</creator><creator>Ziółkowska, Magdalena</creator><creator>Pagano, Roberto</creator><creator>Taheri, Pegah</creator><creator>Kalita, Katarzyna</creator><creator>Salamian, Ahmad</creator><creator>Radwanska, Kasia</creator><general>Nature Publishing Group</general><general>Springer International Publishing</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>3V.</scope><scope>7TK</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>88G</scope><scope>8AO</scope><scope>8FE</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>LK8</scope><scope>M0S</scope><scope>M1P</scope><scope>M2M</scope><scope>M7P</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>PSYQQ</scope><scope>Q9U</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0001-7445-6180</orcidid><orcidid>https://orcid.org/0000-0003-2841-9228</orcidid><orcidid>https://orcid.org/0000-0002-7687-4471</orcidid></search><sort><creationdate>20230201</creationdate><title>Impaired synaptic transmission in dorsal dentate gyrus increases impulsive alcohol seeking</title><author>Nalberczak-Skóra, Maria ; Beroun, Anna ; Skonieczna, Edyta ; Cały, Anna ; Ziółkowska, Magdalena ; Pagano, Roberto ; Taheri, Pegah ; Kalita, Katarzyna ; Salamian, Ahmad ; Radwanska, Kasia</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c360t-cf6c915b9616bfbb57bc0d678fc939193d9432e0ec6b57acea85347151c347ef3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2023</creationdate><topic>Addictions</topic><topic>Alcohol</topic><topic>Alcohol abuse</topic><topic>Alcoholism - genetics</topic><topic>Animal models</topic><topic>Animals</topic><topic>Dentate Gyrus</topic><topic>Drug abuse</topic><topic>Ethanol - pharmacology</topic><topic>Glutamate receptors</topic><topic>Humans</topic><topic>Impulsivity</topic><topic>Mice</topic><topic>Motivation</topic><topic>N-Methyl-D-aspartic acid receptors</topic><topic>Potentiation</topic><topic>Recurrence</topic><topic>Reinforcement</topic><topic>Synapses</topic><topic>Synaptic Transmission</topic><topic>α-Amino-3-hydroxy-5-methyl-4-isoxazole propionic acid receptors</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Nalberczak-Skóra, Maria</creatorcontrib><creatorcontrib>Beroun, Anna</creatorcontrib><creatorcontrib>Skonieczna, Edyta</creatorcontrib><creatorcontrib>Cały, Anna</creatorcontrib><creatorcontrib>Ziółkowska, Magdalena</creatorcontrib><creatorcontrib>Pagano, Roberto</creatorcontrib><creatorcontrib>Taheri, Pegah</creatorcontrib><creatorcontrib>Kalita, Katarzyna</creatorcontrib><creatorcontrib>Salamian, Ahmad</creatorcontrib><creatorcontrib>Radwanska, Kasia</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>ProQuest Central (Corporate)</collection><collection>Neurosciences Abstracts</collection><collection>ProQuest Health &amp; Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Medical Database (Alumni Edition)</collection><collection>Psychology Database (Alumni)</collection><collection>ProQuest Pharma Collection</collection><collection>ProQuest SciTech 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>ProQuest Central (Alumni)</collection><collection>ProQuest Central UK/Ireland</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>ProQuest Natural Science Collection</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Health &amp; Medical Complete (Alumni)</collection><collection>Biological Sciences</collection><collection>Health &amp; Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>Psychology Database</collection><collection>Biological Science Database</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>PubMed Central (Full Participant titles)</collection><jtitle>Neuropsychopharmacology (New York, N.Y.)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Nalberczak-Skóra, Maria</au><au>Beroun, Anna</au><au>Skonieczna, Edyta</au><au>Cały, Anna</au><au>Ziółkowska, Magdalena</au><au>Pagano, Roberto</au><au>Taheri, Pegah</au><au>Kalita, Katarzyna</au><au>Salamian, Ahmad</au><au>Radwanska, Kasia</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Impaired synaptic transmission in dorsal dentate gyrus increases impulsive alcohol seeking</atitle><jtitle>Neuropsychopharmacology (New York, N.Y.)</jtitle><addtitle>Neuropsychopharmacology</addtitle><date>2023-02-01</date><risdate>2023</risdate><volume>48</volume><issue>3</issue><spage>436</spage><epage>447</epage><pages>436-447</pages><issn>0893-133X</issn><eissn>1740-634X</eissn><abstract>Both human and animal studies indicate that the dentate gyrus (DG) of the hippocampus is highly exploited by drug and alcohol abuse. Yet, it is poorly understood how DG dysfunction affects addiction-related behaviors. Here, we used an animal model of alcohol use disorder (AUD) in automated IntelliCages and performed local genetic manipulation to investigate how synaptic transmission in the dorsal DG (dDG) affects alcohol-related behaviors. We show that a cue light induces potentiation-like plasticity of dDG synapses in alcohol-naive mice. This process is impaired in mice trained to drink alcohol. Acamprosate (ACA), a drug that reduces alcohol relapse, rescues the impairment of dDG synaptic transmission in alcohol mice. A molecular manipulation that reduces dDG synaptic AMPAR and NMDAR levels increases impulsive alcohol seeking during cue relapse (CR) in alcohol mice but does not affect alcohol reward, motivation or craving. These findings suggest that hindered dDG synaptic transmission specifically underlies impulsive alcohol seeking induced by alcohol cues, a core symptom of AUD.</abstract><cop>England</cop><pub>Nature Publishing Group</pub><pmid>36182989</pmid><doi>10.1038/s41386-022-01464-5</doi><tpages>12</tpages><orcidid>https://orcid.org/0000-0001-7445-6180</orcidid><orcidid>https://orcid.org/0000-0003-2841-9228</orcidid><orcidid>https://orcid.org/0000-0002-7687-4471</orcidid><oa>free_for_read</oa></addata></record>
fulltext fulltext
identifier ISSN: 0893-133X
ispartof Neuropsychopharmacology (New York, N.Y.), 2023-02, Vol.48 (3), p.436-447
issn 0893-133X
1740-634X
language eng
recordid cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_9852589
source PubMed (Medline); MEDLINE; SpringerLink (Online service); EZB Electronic Journals Library
subjects Addictions
Alcohol
Alcohol abuse
Alcoholism - genetics
Animal models
Animals
Dentate Gyrus
Drug abuse
Ethanol - pharmacology
Glutamate receptors
Humans
Impulsivity
Mice
Motivation
N-Methyl-D-aspartic acid receptors
Potentiation
Recurrence
Reinforcement
Synapses
Synaptic Transmission
α-Amino-3-hydroxy-5-methyl-4-isoxazole propionic acid receptors
title Impaired synaptic transmission in dorsal dentate gyrus increases impulsive alcohol seeking
url https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-02-07T15%3A59%3A34IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-proquest_pubme&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Impaired%20synaptic%20transmission%20in%20dorsal%20dentate%20gyrus%20increases%20impulsive%20alcohol%20seeking&rft.jtitle=Neuropsychopharmacology%20(New%20York,%20N.Y.)&rft.au=Nalberczak-Sk%C3%B3ra,%20Maria&rft.date=2023-02-01&rft.volume=48&rft.issue=3&rft.spage=436&rft.epage=447&rft.pages=436-447&rft.issn=0893-133X&rft.eissn=1740-634X&rft_id=info:doi/10.1038/s41386-022-01464-5&rft_dat=%3Cproquest_pubme%3E2720424366%3C/proquest_pubme%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=2766912007&rft_id=info:pmid/36182989&rfr_iscdi=true