L-DOPA reduces model-free control of behavior by attenuating the transfer of value to action

Dopamine is a key neurotransmitter in action control. However, influential theories of dopamine function make conflicting predictions about the effect of boosting dopamine neurotransmission. Here, we tested if increases in dopamine tone by administration of L-DOPA upregulate reward learning as predi...

Ausführliche Beschreibung

Gespeichert in:
Bibliographische Detailangaben
Veröffentlicht in:NeuroImage (Orlando, Fla.) Fla.), 2019-02, Vol.186, p.113-125
Hauptverfasser: Kroemer, Nils B., Lee, Ying, Pooseh, Shakoor, Eppinger, Ben, Goschke, Thomas, Smolka, Michael N.
Format: Artikel
Sprache:eng
Schlagworte:
Online-Zugang:Volltext
Tags: Tag hinzufügen
Keine Tags, Fügen Sie den ersten Tag hinzu!
container_end_page 125
container_issue
container_start_page 113
container_title NeuroImage (Orlando, Fla.)
container_volume 186
creator Kroemer, Nils B.
Lee, Ying
Pooseh, Shakoor
Eppinger, Ben
Goschke, Thomas
Smolka, Michael N.
description Dopamine is a key neurotransmitter in action control. However, influential theories of dopamine function make conflicting predictions about the effect of boosting dopamine neurotransmission. Here, we tested if increases in dopamine tone by administration of L-DOPA upregulate reward learning as predicted by reinforcement learning theories, and if increases are specific for deliberative “model-based” control or reflexive “model-free” control. Alternatively, L-DOPA may impair learning as suggested by “value” or “thrift” theories of dopamine. To this end, we employed a two-stage Markov decision-task to investigate the effect of L-DOPA (randomized cross-over) on behavioral control while brain activation was measured using fMRI. L-DOPA led to attenuated model-free control of behavior as indicated by the reduced impact of reward on choice. Increased model-based control was only observed in participants with high working memory capacity. Furthermore, L-DOPA facilitated exploratory behavior, particularly after a stream of wins in the task. Correspondingly, in the brain, L-DOPA decreased the effect of reward at the outcome stage and when the next decision had to be made. Critically, reward-learning rates and prediction error signals were unaffected by L-DOPA, indicating that differences in behavior and brain response to reward were not driven by differences in learning. Taken together, our results suggest that L-DOPA reduces model-free control of behavior by attenuating the transfer of value to action. These findings provide support for the value and thrift accounts of dopamine and call for a refined integration of valuation and action signals in reinforcement learning models. •Theories make conflicting predictions about the effect of boosting dopamine.•Behaviorally, L-DOPA reduces the reflexive effect of reward (model-free control).•On average, L-DOPA does not change learning rates or model-based control.•In the brain, L-DOPA reduces reward outcome signals and their link to behavior.•Results support thrift and value theories of dopamine.
doi_str_mv 10.1016/j.neuroimage.2018.10.075
format Article
fullrecord <record><control><sourceid>proquest_cross</sourceid><recordid>TN_cdi_proquest_miscellaneous_2127947725</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><els_id>S1053811918320561</els_id><sourcerecordid>2167140328</sourcerecordid><originalsourceid>FETCH-LOGICAL-c452t-d28ed5e4f2c3b0df4a649f1e41b712fcd10681d55281e4e343dce1fe4bc86a7b3</originalsourceid><addsrcrecordid>eNqFkU9r3DAQxU1paNK0X6EIeunFW40s2fIxTdI_sJAe2ltByNIo0eKVUkleyLePzKYt9JKThje_0QzvNQ0BugEK_cfdJuCSot_rW9wwCrLKGzqIF80Z0FG0oxjYy7UWXSsBxtPmdc47SukIXL5qTjvaSWBcnDW_tu3VzfcLktAuBjPZR4tz6xIiMTGUFGcSHZnwTh98TGR6ILoUDIsuPtyScoekJB2yw7RyBz0vVYlEm-JjeNOcOD1nfPv0njc_P1__uPzabm--fLu82LaGC1ZayyRagdwx003UOq57PjpADtMAzBkLtJdghWCyitjxzhoEh3wystfD1J03H47_3qf4e8Fc1N5ng_OsA8YlKwZsGPkwMFHR9_-hu7ikUK-rVD8Apx2TlZJHyqSYc0Kn7lM1Oz0ooGpNQO3UvwTUmsDaqQnU0XdPC5Zpj_bv4B_LK_DpCGB15OAxqWw8BoPWJzRF2eif3_IIHYqcYw</addsrcrecordid><sourcetype>Aggregation Database</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>2167140328</pqid></control><display><type>article</type><title>L-DOPA reduces model-free control of behavior by attenuating the transfer of value to action</title><source>ScienceDirect Journals (5 years ago - present)</source><source>ProQuest Central UK/Ireland</source><creator>Kroemer, Nils B. ; Lee, Ying ; Pooseh, Shakoor ; Eppinger, Ben ; Goschke, Thomas ; Smolka, Michael N.</creator><creatorcontrib>Kroemer, Nils B. ; Lee, Ying ; Pooseh, Shakoor ; Eppinger, Ben ; Goschke, Thomas ; Smolka, Michael N.</creatorcontrib><description>Dopamine is a key neurotransmitter in action control. However, influential theories of dopamine function make conflicting predictions about the effect of boosting dopamine neurotransmission. Here, we tested if increases in dopamine tone by administration of L-DOPA upregulate reward learning as predicted by reinforcement learning theories, and if increases are specific for deliberative “model-based” control or reflexive “model-free” control. Alternatively, L-DOPA may impair learning as suggested by “value” or “thrift” theories of dopamine. To this end, we employed a two-stage Markov decision-task to investigate the effect of L-DOPA (randomized cross-over) on behavioral control while brain activation was measured using fMRI. L-DOPA led to attenuated model-free control of behavior as indicated by the reduced impact of reward on choice. Increased model-based control was only observed in participants with high working memory capacity. Furthermore, L-DOPA facilitated exploratory behavior, particularly after a stream of wins in the task. Correspondingly, in the brain, L-DOPA decreased the effect of reward at the outcome stage and when the next decision had to be made. Critically, reward-learning rates and prediction error signals were unaffected by L-DOPA, indicating that differences in behavior and brain response to reward were not driven by differences in learning. Taken together, our results suggest that L-DOPA reduces model-free control of behavior by attenuating the transfer of value to action. These findings provide support for the value and thrift accounts of dopamine and call for a refined integration of valuation and action signals in reinforcement learning models. •Theories make conflicting predictions about the effect of boosting dopamine.•Behaviorally, L-DOPA reduces the reflexive effect of reward (model-free control).•On average, L-DOPA does not change learning rates or model-based control.•In the brain, L-DOPA reduces reward outcome signals and their link to behavior.•Results support thrift and value theories of dopamine.</description><identifier>ISSN: 1053-8119</identifier><identifier>EISSN: 1095-9572</identifier><identifier>DOI: 10.1016/j.neuroimage.2018.10.075</identifier><identifier>PMID: 30381245</identifier><language>eng</language><publisher>United States: Elsevier Inc</publisher><subject>Behavior ; Brain mapping ; Computational modeling ; Data analysis ; Decision making ; Dihydroxyphenylalanine ; Dopamine ; Expected values ; Exploratory behavior ; fMRI ; Functional magnetic resonance imaging ; Goal-directed behavior ; Learning ; Levodopa ; Mental task performance ; Neurotransmission ; Pharmacology ; Reinforcement ; Reward ; Short term memory</subject><ispartof>NeuroImage (Orlando, Fla.), 2019-02, Vol.186, p.113-125</ispartof><rights>2018 Elsevier Inc.</rights><rights>Copyright © 2018 Elsevier Inc. All rights reserved.</rights><rights>Copyright Elsevier Limited Feb 1, 2019</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c452t-d28ed5e4f2c3b0df4a649f1e41b712fcd10681d55281e4e343dce1fe4bc86a7b3</citedby><cites>FETCH-LOGICAL-c452t-d28ed5e4f2c3b0df4a649f1e41b712fcd10681d55281e4e343dce1fe4bc86a7b3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://www.proquest.com/docview/2167140328?pq-origsite=primo$$EHTML$$P50$$Gproquest$$H</linktohtml><link.rule.ids>314,780,784,3550,27924,27925,45995,64385,64387,64389,72469</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/30381245$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Kroemer, Nils B.</creatorcontrib><creatorcontrib>Lee, Ying</creatorcontrib><creatorcontrib>Pooseh, Shakoor</creatorcontrib><creatorcontrib>Eppinger, Ben</creatorcontrib><creatorcontrib>Goschke, Thomas</creatorcontrib><creatorcontrib>Smolka, Michael N.</creatorcontrib><title>L-DOPA reduces model-free control of behavior by attenuating the transfer of value to action</title><title>NeuroImage (Orlando, Fla.)</title><addtitle>Neuroimage</addtitle><description>Dopamine is a key neurotransmitter in action control. However, influential theories of dopamine function make conflicting predictions about the effect of boosting dopamine neurotransmission. Here, we tested if increases in dopamine tone by administration of L-DOPA upregulate reward learning as predicted by reinforcement learning theories, and if increases are specific for deliberative “model-based” control or reflexive “model-free” control. Alternatively, L-DOPA may impair learning as suggested by “value” or “thrift” theories of dopamine. To this end, we employed a two-stage Markov decision-task to investigate the effect of L-DOPA (randomized cross-over) on behavioral control while brain activation was measured using fMRI. L-DOPA led to attenuated model-free control of behavior as indicated by the reduced impact of reward on choice. Increased model-based control was only observed in participants with high working memory capacity. Furthermore, L-DOPA facilitated exploratory behavior, particularly after a stream of wins in the task. Correspondingly, in the brain, L-DOPA decreased the effect of reward at the outcome stage and when the next decision had to be made. Critically, reward-learning rates and prediction error signals were unaffected by L-DOPA, indicating that differences in behavior and brain response to reward were not driven by differences in learning. Taken together, our results suggest that L-DOPA reduces model-free control of behavior by attenuating the transfer of value to action. These findings provide support for the value and thrift accounts of dopamine and call for a refined integration of valuation and action signals in reinforcement learning models. •Theories make conflicting predictions about the effect of boosting dopamine.•Behaviorally, L-DOPA reduces the reflexive effect of reward (model-free control).•On average, L-DOPA does not change learning rates or model-based control.•In the brain, L-DOPA reduces reward outcome signals and their link to behavior.•Results support thrift and value theories of dopamine.</description><subject>Behavior</subject><subject>Brain mapping</subject><subject>Computational modeling</subject><subject>Data analysis</subject><subject>Decision making</subject><subject>Dihydroxyphenylalanine</subject><subject>Dopamine</subject><subject>Expected values</subject><subject>Exploratory behavior</subject><subject>fMRI</subject><subject>Functional magnetic resonance imaging</subject><subject>Goal-directed behavior</subject><subject>Learning</subject><subject>Levodopa</subject><subject>Mental task performance</subject><subject>Neurotransmission</subject><subject>Pharmacology</subject><subject>Reinforcement</subject><subject>Reward</subject><subject>Short term memory</subject><issn>1053-8119</issn><issn>1095-9572</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2019</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>eNqFkU9r3DAQxU1paNK0X6EIeunFW40s2fIxTdI_sJAe2ltByNIo0eKVUkleyLePzKYt9JKThje_0QzvNQ0BugEK_cfdJuCSot_rW9wwCrLKGzqIF80Z0FG0oxjYy7UWXSsBxtPmdc47SukIXL5qTjvaSWBcnDW_tu3VzfcLktAuBjPZR4tz6xIiMTGUFGcSHZnwTh98TGR6ILoUDIsuPtyScoekJB2yw7RyBz0vVYlEm-JjeNOcOD1nfPv0njc_P1__uPzabm--fLu82LaGC1ZayyRagdwx003UOq57PjpADtMAzBkLtJdghWCyitjxzhoEh3wystfD1J03H47_3qf4e8Fc1N5ng_OsA8YlKwZsGPkwMFHR9_-hu7ikUK-rVD8Apx2TlZJHyqSYc0Kn7lM1Oz0ooGpNQO3UvwTUmsDaqQnU0XdPC5Zpj_bv4B_LK_DpCGB15OAxqWw8BoPWJzRF2eif3_IIHYqcYw</recordid><startdate>20190201</startdate><enddate>20190201</enddate><creator>Kroemer, Nils B.</creator><creator>Lee, Ying</creator><creator>Pooseh, Shakoor</creator><creator>Eppinger, Ben</creator><creator>Goschke, Thomas</creator><creator>Smolka, Michael N.</creator><general>Elsevier Inc</general><general>Elsevier Limited</general><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>8FD</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>FR3</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>P64</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>PSYQQ</scope><scope>Q9U</scope><scope>RC3</scope><scope>7X8</scope></search><sort><creationdate>20190201</creationdate><title>L-DOPA reduces model-free control of behavior by attenuating the transfer of value to action</title><author>Kroemer, Nils B. ; Lee, Ying ; Pooseh, Shakoor ; Eppinger, Ben ; Goschke, Thomas ; Smolka, Michael N.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c452t-d28ed5e4f2c3b0df4a649f1e41b712fcd10681d55281e4e343dce1fe4bc86a7b3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2019</creationdate><topic>Behavior</topic><topic>Brain mapping</topic><topic>Computational modeling</topic><topic>Data analysis</topic><topic>Decision making</topic><topic>Dihydroxyphenylalanine</topic><topic>Dopamine</topic><topic>Expected values</topic><topic>Exploratory behavior</topic><topic>fMRI</topic><topic>Functional magnetic resonance imaging</topic><topic>Goal-directed behavior</topic><topic>Learning</topic><topic>Levodopa</topic><topic>Mental task performance</topic><topic>Neurotransmission</topic><topic>Pharmacology</topic><topic>Reinforcement</topic><topic>Reward</topic><topic>Short term memory</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Kroemer, Nils B.</creatorcontrib><creatorcontrib>Lee, Ying</creatorcontrib><creatorcontrib>Pooseh, Shakoor</creatorcontrib><creatorcontrib>Eppinger, Ben</creatorcontrib><creatorcontrib>Goschke, Thomas</creatorcontrib><creatorcontrib>Smolka, Michael N.</creatorcontrib><collection>PubMed</collection><collection>CrossRef</collection><collection>ProQuest Central (Corporate)</collection><collection>Neurosciences Abstracts</collection><collection>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>Technology Research Database</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 Edition)</collection><collection>ProQuest Central UK/Ireland</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>Natural Science Collection</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central Korea</collection><collection>Engineering Research Database</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>ProQuest Biological Science Collection</collection><collection>Health &amp; Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>Psychology Database</collection><collection>Biological Science Database</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>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><jtitle>NeuroImage (Orlando, Fla.)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Kroemer, Nils B.</au><au>Lee, Ying</au><au>Pooseh, Shakoor</au><au>Eppinger, Ben</au><au>Goschke, Thomas</au><au>Smolka, Michael N.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>L-DOPA reduces model-free control of behavior by attenuating the transfer of value to action</atitle><jtitle>NeuroImage (Orlando, Fla.)</jtitle><addtitle>Neuroimage</addtitle><date>2019-02-01</date><risdate>2019</risdate><volume>186</volume><spage>113</spage><epage>125</epage><pages>113-125</pages><issn>1053-8119</issn><eissn>1095-9572</eissn><abstract>Dopamine is a key neurotransmitter in action control. However, influential theories of dopamine function make conflicting predictions about the effect of boosting dopamine neurotransmission. Here, we tested if increases in dopamine tone by administration of L-DOPA upregulate reward learning as predicted by reinforcement learning theories, and if increases are specific for deliberative “model-based” control or reflexive “model-free” control. Alternatively, L-DOPA may impair learning as suggested by “value” or “thrift” theories of dopamine. To this end, we employed a two-stage Markov decision-task to investigate the effect of L-DOPA (randomized cross-over) on behavioral control while brain activation was measured using fMRI. L-DOPA led to attenuated model-free control of behavior as indicated by the reduced impact of reward on choice. Increased model-based control was only observed in participants with high working memory capacity. Furthermore, L-DOPA facilitated exploratory behavior, particularly after a stream of wins in the task. Correspondingly, in the brain, L-DOPA decreased the effect of reward at the outcome stage and when the next decision had to be made. Critically, reward-learning rates and prediction error signals were unaffected by L-DOPA, indicating that differences in behavior and brain response to reward were not driven by differences in learning. Taken together, our results suggest that L-DOPA reduces model-free control of behavior by attenuating the transfer of value to action. These findings provide support for the value and thrift accounts of dopamine and call for a refined integration of valuation and action signals in reinforcement learning models. •Theories make conflicting predictions about the effect of boosting dopamine.•Behaviorally, L-DOPA reduces the reflexive effect of reward (model-free control).•On average, L-DOPA does not change learning rates or model-based control.•In the brain, L-DOPA reduces reward outcome signals and their link to behavior.•Results support thrift and value theories of dopamine.</abstract><cop>United States</cop><pub>Elsevier Inc</pub><pmid>30381245</pmid><doi>10.1016/j.neuroimage.2018.10.075</doi><tpages>13</tpages><oa>free_for_read</oa></addata></record>
fulltext fulltext
identifier ISSN: 1053-8119
ispartof NeuroImage (Orlando, Fla.), 2019-02, Vol.186, p.113-125
issn 1053-8119
1095-9572
language eng
recordid cdi_proquest_miscellaneous_2127947725
source ScienceDirect Journals (5 years ago - present); ProQuest Central UK/Ireland
subjects Behavior
Brain mapping
Computational modeling
Data analysis
Decision making
Dihydroxyphenylalanine
Dopamine
Expected values
Exploratory behavior
fMRI
Functional magnetic resonance imaging
Goal-directed behavior
Learning
Levodopa
Mental task performance
Neurotransmission
Pharmacology
Reinforcement
Reward
Short term memory
title L-DOPA reduces model-free control of behavior by attenuating the transfer of value to action
url https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-01-06T12%3A57%3A55IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-proquest_cross&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=L-DOPA%20reduces%20model-free%20control%20of%20behavior%20by%20attenuating%20the%20transfer%20of%20value%20to%20action&rft.jtitle=NeuroImage%20(Orlando,%20Fla.)&rft.au=Kroemer,%20Nils%20B.&rft.date=2019-02-01&rft.volume=186&rft.spage=113&rft.epage=125&rft.pages=113-125&rft.issn=1053-8119&rft.eissn=1095-9572&rft_id=info:doi/10.1016/j.neuroimage.2018.10.075&rft_dat=%3Cproquest_cross%3E2167140328%3C/proquest_cross%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=2167140328&rft_id=info:pmid/30381245&rft_els_id=S1053811918320561&rfr_iscdi=true