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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Veröffentlicht in:Addiction biology 2018-05, Vol.23 (3), p.931-944
Hauptverfasser: Leurquin‐Sterk, Gil, Ceccarini, Jenny, Crunelle, Cleo Lina, Weerasekera, Akila, Laat, Bart, Himmelreich, Uwe, Bormans, Guy, Van Laere, Koen
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container_title Addiction biology
container_volume 23
creator Leurquin‐Sterk, Gil
Ceccarini, Jenny
Crunelle, Cleo Lina
Weerasekera, Akila
Laat, Bart
Himmelreich, Uwe
Bormans, Guy
Van Laere, Koen
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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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 &lt; 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 &lt; 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 &lt; 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 &lt; 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. 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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 &lt; 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 &lt; 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 &lt; 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 &lt; 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. 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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 &amp; 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 - 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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 &lt; 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 &lt; 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 &lt; 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 &lt; 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 &amp; 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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identifier ISSN: 1355-6215
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issn 1355-6215
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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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