Cerebral dopaminergic and glutamatergic transmission relate to different subjective responses of acute alcohol intake: an in vivo multimodal imaging study
Converging preclinical evidence links extrastriatal dopamine release and glutamatergic transmission via the metabotropic glutamate receptor 5 (mGluR5) to the rewarding properties of alcohol. To date, human evidence is lacking on how and where in the brain these processes occur. Mesocorticolimbic dop...
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description | Converging preclinical evidence links extrastriatal dopamine release and glutamatergic transmission via the metabotropic glutamate receptor 5 (mGluR5) to the rewarding properties of alcohol. To date, human evidence is lacking on how and where in the brain these processes occur. Mesocorticolimbic dopamine release upon intravenous alcohol administration and mGluR5 availability were measured in 11 moderate social drinkers by single‐session [18F]fallypride and [18F]FPEB positron emission tomography, respectively. Additionally, baseline and postalcohol glutamate and glutamine levels in the anterior cingulate cortex (ACC) were measured by using proton‐magnetic resonance spectroscopy. To investigate differences in reward domains linked to both neurotransmitters, regional imaging data were related to subjective alcohol responses. Alcohol induced significant [18F]fallypride displacement in the prefrontal cortex (PFC), temporal and parietal cortices and thalamus (P |
doi_str_mv | 10.1111/adb.12542 |
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In this multimodal imaging study, we linked estrastriatal dopamine (DA) release and glutamatergic transmission to the rewarding properties of alcohol in social drinkers. Overall, our human data revealed new mechanistic understanding and differential neurobiological underpinnings of the effects of acute alcohol consumption on human behavior. Specifically, prefrontal DA release may encode alcohol ‘liking’ and ‘wanting’ effects in specific areas underlying value processing and motivation, whereas mGluR5 availability in distinct prefrontal–temporal–subcortical regions is more related to the alcohol ‘high’ effect.</description><identifier>ISSN: 1355-6215</identifier><identifier>EISSN: 1369-1600</identifier><identifier>DOI: 10.1111/adb.12542</identifier><identifier>PMID: 28884874</identifier><language>eng</language><publisher>United States: John Wiley & Sons, Inc</publisher><subject>[1H]MRS ; Adult ; Alcohol ; Alcoholic beverages ; Benzamides ; Brain - diagnostic imaging ; Brain - drug effects ; Brain - metabolism ; Caudate nucleus ; Caudate Nucleus - diagnostic imaging ; Caudate Nucleus - drug effects ; Caudate Nucleus - metabolism ; Central Nervous System Depressants - pharmacology ; Cortex (cingulate) ; Cortex (parietal) ; Cortex (temporal) ; Dopamine ; Dopamine - metabolism ; Dopamine receptors ; Ethanol - pharmacology ; Female ; glutamate ; Glutamatergic transmission ; Glutamic Acid - drug effects ; Glutamic Acid - metabolism ; Glutamic acid receptors (metabotropic) ; Glutamine ; Glutamine - drug effects ; Glutamine - metabolism ; Humans ; Infusions, Intravenous ; Intravenous administration ; Magnetic resonance spectroscopy ; Male ; Medical imaging ; Middle Aged ; Motivation ; Neuroimaging ; Neurotransmitters ; Nitriles ; Parietal Lobe ; PET ; Positron emission tomography ; Prefrontal cortex ; Prefrontal Cortex - diagnostic imaging ; Prefrontal Cortex - drug effects ; Prefrontal Cortex - metabolism ; Proton Magnetic Resonance Spectroscopy ; Pyridines ; Pyrrolidines ; Radiopharmaceuticals ; Receptor, Metabotropic Glutamate 5 - drug effects ; Receptor, Metabotropic Glutamate 5 - metabolism ; Reinforcement ; Spectrum analysis ; subjective effects ; Synaptic Transmission - drug effects ; Temporal lobe ; Temporal Lobe - diagnostic imaging ; Temporal Lobe - drug effects ; Temporal Lobe - metabolism ; Thalamus ; Thalamus - diagnostic imaging ; Thalamus - drug effects ; Thalamus - metabolism ; Young Adult</subject><ispartof>Addiction biology, 2018-05, Vol.23 (3), p.931-944</ispartof><rights>2017 Society for the Study of Addiction</rights><rights>2017 Society for the Study of Addiction.</rights><rights>2018 Society for the Study of Addiction</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c3532-975529d96cbfc4144ddf64e4e246819a818307f329001005fc3d47bb3da4ced03</citedby><cites>FETCH-LOGICAL-c3532-975529d96cbfc4144ddf64e4e246819a818307f329001005fc3d47bb3da4ced03</cites><orcidid>0000-0003-2774-9516</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1111%2Fadb.12542$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1111%2Fadb.12542$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>314,780,784,1417,27924,27925,45574,45575</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/28884874$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Leurquin‐Sterk, Gil</creatorcontrib><creatorcontrib>Ceccarini, Jenny</creatorcontrib><creatorcontrib>Crunelle, Cleo Lina</creatorcontrib><creatorcontrib>Weerasekera, Akila</creatorcontrib><creatorcontrib>Laat, Bart</creatorcontrib><creatorcontrib>Himmelreich, Uwe</creatorcontrib><creatorcontrib>Bormans, Guy</creatorcontrib><creatorcontrib>Van Laere, Koen</creatorcontrib><title>Cerebral dopaminergic and glutamatergic transmission relate to different subjective responses of acute alcohol intake: an in vivo multimodal imaging study</title><title>Addiction biology</title><addtitle>Addict Biol</addtitle><description>Converging preclinical evidence links extrastriatal dopamine release and glutamatergic transmission via the metabotropic glutamate receptor 5 (mGluR5) to the rewarding properties of alcohol. To date, human evidence is lacking on how and where in the brain these processes occur. Mesocorticolimbic dopamine release upon intravenous alcohol administration and mGluR5 availability were measured in 11 moderate social drinkers by single‐session [18F]fallypride and [18F]FPEB positron emission tomography, respectively. Additionally, baseline and postalcohol glutamate and glutamine levels in the anterior cingulate cortex (ACC) were measured by using proton‐magnetic resonance spectroscopy. To investigate differences in reward domains linked to both neurotransmitters, regional imaging data were related to subjective alcohol responses. Alcohol induced significant [18F]fallypride displacement in the prefrontal cortex (PFC), temporal and parietal cortices and thalamus (P < 0.05, corrected for multiple comparisons). Dopamine release in the ACC and orbitofrontal and ventromedial PFCs were correlated with subjective ‘liking’ and ‘wanting’ effects (P < 0.05). In contrast, baseline mGluR5 availability was positively correlated with the ‘high’ effect of alcohol in dorsolateral, ventrolateral and ventromedial PFCs and in the medial temporal lobe, thalamus and caudate nucleus (P < 0.05). Although neither proton‐magnetic resonance spectroscopy glutamate nor glutamine levels were affected by alcohol, baseline ACC glutamate levels were negatively associated with the alcohol ‘liking’ effect (P < 0.003). These data reveal new mechanistic understanding and differential neurobiological underpinnings of the effects of acute alcohol consumption on human behavior. Specifically, prefrontal dopamine release may encode alcohol ‘liking’ and ‘wanting’ effects in specific areas underlying value processing and motivation, whereas mGluR5 availability in distinct prefrontal–temporal–subcortical regions is more related to the alcohol ‘high’ effect.
In this multimodal imaging study, we linked estrastriatal dopamine (DA) release and glutamatergic transmission to the rewarding properties of alcohol in social drinkers. Overall, our human data revealed new mechanistic understanding and differential neurobiological underpinnings of the effects of acute alcohol consumption on human behavior. Specifically, prefrontal DA release may encode alcohol ‘liking’ and ‘wanting’ effects in specific areas underlying value processing and motivation, whereas mGluR5 availability in distinct prefrontal–temporal–subcortical regions is more related to the alcohol ‘high’ effect.</description><subject>[1H]MRS</subject><subject>Adult</subject><subject>Alcohol</subject><subject>Alcoholic beverages</subject><subject>Benzamides</subject><subject>Brain - diagnostic imaging</subject><subject>Brain - drug effects</subject><subject>Brain - metabolism</subject><subject>Caudate nucleus</subject><subject>Caudate Nucleus - diagnostic imaging</subject><subject>Caudate Nucleus - drug effects</subject><subject>Caudate Nucleus - metabolism</subject><subject>Central Nervous System Depressants - pharmacology</subject><subject>Cortex (cingulate)</subject><subject>Cortex (parietal)</subject><subject>Cortex (temporal)</subject><subject>Dopamine</subject><subject>Dopamine - metabolism</subject><subject>Dopamine receptors</subject><subject>Ethanol - pharmacology</subject><subject>Female</subject><subject>glutamate</subject><subject>Glutamatergic transmission</subject><subject>Glutamic Acid - drug effects</subject><subject>Glutamic Acid - metabolism</subject><subject>Glutamic acid receptors (metabotropic)</subject><subject>Glutamine</subject><subject>Glutamine - drug effects</subject><subject>Glutamine - metabolism</subject><subject>Humans</subject><subject>Infusions, Intravenous</subject><subject>Intravenous administration</subject><subject>Magnetic resonance spectroscopy</subject><subject>Male</subject><subject>Medical imaging</subject><subject>Middle Aged</subject><subject>Motivation</subject><subject>Neuroimaging</subject><subject>Neurotransmitters</subject><subject>Nitriles</subject><subject>Parietal Lobe</subject><subject>PET</subject><subject>Positron emission tomography</subject><subject>Prefrontal cortex</subject><subject>Prefrontal Cortex - diagnostic imaging</subject><subject>Prefrontal Cortex - drug effects</subject><subject>Prefrontal Cortex - metabolism</subject><subject>Proton Magnetic Resonance Spectroscopy</subject><subject>Pyridines</subject><subject>Pyrrolidines</subject><subject>Radiopharmaceuticals</subject><subject>Receptor, Metabotropic Glutamate 5 - drug effects</subject><subject>Receptor, Metabotropic Glutamate 5 - metabolism</subject><subject>Reinforcement</subject><subject>Spectrum analysis</subject><subject>subjective effects</subject><subject>Synaptic Transmission - drug effects</subject><subject>Temporal lobe</subject><subject>Temporal Lobe - diagnostic imaging</subject><subject>Temporal Lobe - drug effects</subject><subject>Temporal Lobe - metabolism</subject><subject>Thalamus</subject><subject>Thalamus - diagnostic imaging</subject><subject>Thalamus - drug effects</subject><subject>Thalamus - metabolism</subject><subject>Young Adult</subject><issn>1355-6215</issn><issn>1369-1600</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2018</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp1kclO5DAQhi00iP3AC4wszYlDGq9ZuEGzSkhc4Bw5Xhr3JHZjO436VXhaDAFu1KVK5U9_lesH4BijGc5xKlQ3w4QzsgX2MC2bApcI_fmoOS9Kgvku2I9xiRAmFac7YJfUdc3qiu2Bt7kOuguih8qvxGCdDgsroXAKLvoxiUGkqZOCcHGwMVrvYNB97sPkobLGZAWXYBy7pZbJrnV-jivvoo7QGyjkmFHRS__se2hdEv_1WR6QS7i2aw-HsU928CrvYAexsG4BYxrV5hBsG9FHffSVD8DT9dXj_La4f7i5m5_fF5JySoqm4pw0qillZyTDjCllSqaZJqyscSNqXFNUGUqa_H-EuJFUsarrqBJMaoXoAfg36a6Cfxl1TO3Sj8HlkS1BJJ-v4g3P1MlEyeBjDNq0q5DXDZsWo_bDhTa70H66kNm_X4pjN2j1Q36fPQOnE_Bqe735Xak9v7yYJN8BY6CT9w</recordid><startdate>201805</startdate><enddate>201805</enddate><creator>Leurquin‐Sterk, Gil</creator><creator>Ceccarini, Jenny</creator><creator>Crunelle, Cleo Lina</creator><creator>Weerasekera, Akila</creator><creator>Laat, Bart</creator><creator>Himmelreich, Uwe</creator><creator>Bormans, Guy</creator><creator>Van Laere, Koen</creator><general>John Wiley & Sons, Inc</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>7T5</scope><scope>7TM</scope><scope>H94</scope><orcidid>https://orcid.org/0000-0003-2774-9516</orcidid></search><sort><creationdate>201805</creationdate><title>Cerebral dopaminergic and glutamatergic transmission relate to different subjective responses of acute alcohol intake: an in vivo multimodal imaging study</title><author>Leurquin‐Sterk, Gil ; Ceccarini, Jenny ; Crunelle, Cleo Lina ; Weerasekera, Akila ; Laat, Bart ; Himmelreich, Uwe ; Bormans, Guy ; Van Laere, Koen</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c3532-975529d96cbfc4144ddf64e4e246819a818307f329001005fc3d47bb3da4ced03</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2018</creationdate><topic>[1H]MRS</topic><topic>Adult</topic><topic>Alcohol</topic><topic>Alcoholic beverages</topic><topic>Benzamides</topic><topic>Brain - diagnostic imaging</topic><topic>Brain - drug effects</topic><topic>Brain - metabolism</topic><topic>Caudate nucleus</topic><topic>Caudate Nucleus - diagnostic imaging</topic><topic>Caudate Nucleus - drug effects</topic><topic>Caudate Nucleus - metabolism</topic><topic>Central Nervous System Depressants - pharmacology</topic><topic>Cortex (cingulate)</topic><topic>Cortex (parietal)</topic><topic>Cortex (temporal)</topic><topic>Dopamine</topic><topic>Dopamine - metabolism</topic><topic>Dopamine receptors</topic><topic>Ethanol - pharmacology</topic><topic>Female</topic><topic>glutamate</topic><topic>Glutamatergic transmission</topic><topic>Glutamic Acid - drug effects</topic><topic>Glutamic Acid - metabolism</topic><topic>Glutamic acid receptors (metabotropic)</topic><topic>Glutamine</topic><topic>Glutamine - drug effects</topic><topic>Glutamine - metabolism</topic><topic>Humans</topic><topic>Infusions, Intravenous</topic><topic>Intravenous administration</topic><topic>Magnetic resonance spectroscopy</topic><topic>Male</topic><topic>Medical imaging</topic><topic>Middle Aged</topic><topic>Motivation</topic><topic>Neuroimaging</topic><topic>Neurotransmitters</topic><topic>Nitriles</topic><topic>Parietal Lobe</topic><topic>PET</topic><topic>Positron emission tomography</topic><topic>Prefrontal cortex</topic><topic>Prefrontal Cortex - diagnostic imaging</topic><topic>Prefrontal Cortex - drug effects</topic><topic>Prefrontal Cortex - metabolism</topic><topic>Proton Magnetic Resonance Spectroscopy</topic><topic>Pyridines</topic><topic>Pyrrolidines</topic><topic>Radiopharmaceuticals</topic><topic>Receptor, Metabotropic Glutamate 5 - drug effects</topic><topic>Receptor, Metabotropic Glutamate 5 - metabolism</topic><topic>Reinforcement</topic><topic>Spectrum analysis</topic><topic>subjective effects</topic><topic>Synaptic Transmission - drug effects</topic><topic>Temporal lobe</topic><topic>Temporal Lobe - diagnostic imaging</topic><topic>Temporal Lobe - drug effects</topic><topic>Temporal Lobe - metabolism</topic><topic>Thalamus</topic><topic>Thalamus - diagnostic imaging</topic><topic>Thalamus - drug effects</topic><topic>Thalamus - metabolism</topic><topic>Young Adult</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Leurquin‐Sterk, Gil</creatorcontrib><creatorcontrib>Ceccarini, Jenny</creatorcontrib><creatorcontrib>Crunelle, Cleo Lina</creatorcontrib><creatorcontrib>Weerasekera, Akila</creatorcontrib><creatorcontrib>Laat, Bart</creatorcontrib><creatorcontrib>Himmelreich, Uwe</creatorcontrib><creatorcontrib>Bormans, Guy</creatorcontrib><creatorcontrib>Van Laere, Koen</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>Immunology Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>AIDS and Cancer Research Abstracts</collection><jtitle>Addiction biology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Leurquin‐Sterk, Gil</au><au>Ceccarini, Jenny</au><au>Crunelle, Cleo Lina</au><au>Weerasekera, Akila</au><au>Laat, Bart</au><au>Himmelreich, Uwe</au><au>Bormans, Guy</au><au>Van Laere, Koen</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Cerebral dopaminergic and glutamatergic transmission relate to different subjective responses of acute alcohol intake: an in vivo multimodal imaging study</atitle><jtitle>Addiction biology</jtitle><addtitle>Addict Biol</addtitle><date>2018-05</date><risdate>2018</risdate><volume>23</volume><issue>3</issue><spage>931</spage><epage>944</epage><pages>931-944</pages><issn>1355-6215</issn><eissn>1369-1600</eissn><abstract>Converging preclinical evidence links extrastriatal dopamine release and glutamatergic transmission via the metabotropic glutamate receptor 5 (mGluR5) to the rewarding properties of alcohol. To date, human evidence is lacking on how and where in the brain these processes occur. Mesocorticolimbic dopamine release upon intravenous alcohol administration and mGluR5 availability were measured in 11 moderate social drinkers by single‐session [18F]fallypride and [18F]FPEB positron emission tomography, respectively. Additionally, baseline and postalcohol glutamate and glutamine levels in the anterior cingulate cortex (ACC) were measured by using proton‐magnetic resonance spectroscopy. To investigate differences in reward domains linked to both neurotransmitters, regional imaging data were related to subjective alcohol responses. Alcohol induced significant [18F]fallypride displacement in the prefrontal cortex (PFC), temporal and parietal cortices and thalamus (P < 0.05, corrected for multiple comparisons). Dopamine release in the ACC and orbitofrontal and ventromedial PFCs were correlated with subjective ‘liking’ and ‘wanting’ effects (P < 0.05). In contrast, baseline mGluR5 availability was positively correlated with the ‘high’ effect of alcohol in dorsolateral, ventrolateral and ventromedial PFCs and in the medial temporal lobe, thalamus and caudate nucleus (P < 0.05). Although neither proton‐magnetic resonance spectroscopy glutamate nor glutamine levels were affected by alcohol, baseline ACC glutamate levels were negatively associated with the alcohol ‘liking’ effect (P < 0.003). These data reveal new mechanistic understanding and differential neurobiological underpinnings of the effects of acute alcohol consumption on human behavior. Specifically, prefrontal dopamine release may encode alcohol ‘liking’ and ‘wanting’ effects in specific areas underlying value processing and motivation, whereas mGluR5 availability in distinct prefrontal–temporal–subcortical regions is more related to the alcohol ‘high’ effect.
In this multimodal imaging study, we linked estrastriatal dopamine (DA) release and glutamatergic transmission to the rewarding properties of alcohol in social drinkers. Overall, our human data revealed new mechanistic understanding and differential neurobiological underpinnings of the effects of acute alcohol consumption on human behavior. Specifically, prefrontal DA release may encode alcohol ‘liking’ and ‘wanting’ effects in specific areas underlying value processing and motivation, whereas mGluR5 availability in distinct prefrontal–temporal–subcortical regions is more related to the alcohol ‘high’ effect.</abstract><cop>United States</cop><pub>John Wiley & Sons, Inc</pub><pmid>28884874</pmid><doi>10.1111/adb.12542</doi><tpages>14</tpages><orcidid>https://orcid.org/0000-0003-2774-9516</orcidid></addata></record> |
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subjects | [1H]MRS Adult Alcohol Alcoholic beverages Benzamides Brain - diagnostic imaging Brain - drug effects Brain - metabolism Caudate nucleus Caudate Nucleus - diagnostic imaging Caudate Nucleus - drug effects Caudate Nucleus - metabolism Central Nervous System Depressants - pharmacology Cortex (cingulate) Cortex (parietal) Cortex (temporal) Dopamine Dopamine - metabolism Dopamine receptors Ethanol - pharmacology Female glutamate Glutamatergic transmission Glutamic Acid - drug effects Glutamic Acid - metabolism Glutamic acid receptors (metabotropic) Glutamine Glutamine - drug effects Glutamine - metabolism Humans Infusions, Intravenous Intravenous administration Magnetic resonance spectroscopy Male Medical imaging Middle Aged Motivation Neuroimaging Neurotransmitters Nitriles Parietal Lobe PET Positron emission tomography Prefrontal cortex Prefrontal Cortex - diagnostic imaging Prefrontal Cortex - drug effects Prefrontal Cortex - metabolism Proton Magnetic Resonance Spectroscopy Pyridines Pyrrolidines Radiopharmaceuticals Receptor, Metabotropic Glutamate 5 - drug effects Receptor, Metabotropic Glutamate 5 - metabolism Reinforcement Spectrum analysis subjective effects Synaptic Transmission - drug effects Temporal lobe Temporal Lobe - diagnostic imaging Temporal Lobe - drug effects Temporal Lobe - metabolism Thalamus Thalamus - diagnostic imaging Thalamus - drug effects Thalamus - metabolism Young Adult |
title | Cerebral dopaminergic and glutamatergic transmission relate to different subjective responses of acute alcohol intake: an in vivo multimodal imaging study |
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