Subsecond fluctuations in extracellular dopamine encode reward and punishment prediction errors in humans
In the mammalian brain, midbrain dopamine neuron activity is hypothesized to encode reward prediction errors that promote learning and guide behavior by causing rapid changes in dopamine levels in target brain regions. This hypothesis (and alternatives regarding dopamine's role in punishment-le...
Gespeichert in:
Veröffentlicht in: | Science advances 2023-12, Vol.9 (48), p.eadi4927-eadi4927 |
---|---|
Hauptverfasser: | , , , , , , , |
Format: | Artikel |
Sprache: | eng |
Schlagworte: | |
Online-Zugang: | Volltext |
Tags: |
Tag hinzufügen
Keine Tags, Fügen Sie den ersten Tag hinzu!
|
container_end_page | eadi4927 |
---|---|
container_issue | 48 |
container_start_page | eadi4927 |
container_title | Science advances |
container_volume | 9 |
creator | Sands, L Paul Jiang, Angela Liebenow, Brittany DiMarco, Emily Laxton, Adrian W Tatter, Stephen B Montague, P Read Kishida, Kenneth T |
description | In the mammalian brain, midbrain dopamine neuron activity is hypothesized to encode reward prediction errors that promote learning and guide behavior by causing rapid changes in dopamine levels in target brain regions. This hypothesis (and alternatives regarding dopamine's role in punishment-learning) has limited direct evidence in humans. We report intracranial, subsecond measurements of dopamine release in human striatum measured, while volunteers (i.e., patients undergoing deep brain stimulation surgery) performed a probabilistic reward and punishment learning choice task designed to test whether dopamine release encodes only reward prediction errors or whether dopamine release may also encode adaptive punishment learning signals. Results demonstrate that extracellular dopamine levels can encode both reward and punishment prediction errors within distinct time intervals via independent valence-specific pathways in the human brain. |
doi_str_mv | 10.1126/sciadv.adi4927 |
format | Article |
fullrecord | <record><control><sourceid>proquest_cross</sourceid><recordid>TN_cdi_proquest_miscellaneous_2896807348</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><sourcerecordid>2896807348</sourcerecordid><originalsourceid>FETCH-LOGICAL-c335t-d348389f404917bb9351d1c5d6b3407bcf1f18945ddf484b71147f53286122193</originalsourceid><addsrcrecordid>eNpNkDtPwzAURi0EolXpyog8sqT4mdgjqnhJlRiAOXL8UI0SJ9gxj39PQwtiunf4vnN1DwDnGK0wJuVV0l6Z95UynklSHYE5oRUvCGfi-N8-A8uUXhFCmJUlx_IUzKhAVNJSzIF_yk2yug8GujbrMavR9yFBH6D9HKPStm1zqyI0_aA6Hyy0QffGwmg_VDRQ7YpDDj5tOxtGOERrvJ4Q0MbYxx_QNncqpDNw4lSb7PIwF-Dl9uZ5fV9sHu8e1tebQlPKx8JQJqiQjiEmcdU0knJssOambChDVaMddlhIxo1xTLCmwphVjlMiSkwIlnQBLvfcIfZv2aax7nya3lDB9jnVRMhSoGo6swCrfVTHPqVoXT1E36n4VWNUT4brveH6YHhXuDiwc9NZ8xf_9Um_Ab1Kehg</addsrcrecordid><sourcetype>Aggregation Database</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>2896807348</pqid></control><display><type>article</type><title>Subsecond fluctuations in extracellular dopamine encode reward and punishment prediction errors in humans</title><source>MEDLINE</source><source>DOAJ Directory of Open Access Journals</source><source>EZB-FREE-00999 freely available EZB journals</source><source>PubMed Central</source><creator>Sands, L Paul ; Jiang, Angela ; Liebenow, Brittany ; DiMarco, Emily ; Laxton, Adrian W ; Tatter, Stephen B ; Montague, P Read ; Kishida, Kenneth T</creator><creatorcontrib>Sands, L Paul ; Jiang, Angela ; Liebenow, Brittany ; DiMarco, Emily ; Laxton, Adrian W ; Tatter, Stephen B ; Montague, P Read ; Kishida, Kenneth T</creatorcontrib><description>In the mammalian brain, midbrain dopamine neuron activity is hypothesized to encode reward prediction errors that promote learning and guide behavior by causing rapid changes in dopamine levels in target brain regions. This hypothesis (and alternatives regarding dopamine's role in punishment-learning) has limited direct evidence in humans. We report intracranial, subsecond measurements of dopamine release in human striatum measured, while volunteers (i.e., patients undergoing deep brain stimulation surgery) performed a probabilistic reward and punishment learning choice task designed to test whether dopamine release encodes only reward prediction errors or whether dopamine release may also encode adaptive punishment learning signals. Results demonstrate that extracellular dopamine levels can encode both reward and punishment prediction errors within distinct time intervals via independent valence-specific pathways in the human brain.</description><identifier>ISSN: 2375-2548</identifier><identifier>EISSN: 2375-2548</identifier><identifier>DOI: 10.1126/sciadv.adi4927</identifier><identifier>PMID: 38039368</identifier><language>eng</language><publisher>United States</publisher><subject>Animals ; Brain - metabolism ; Dopamine - metabolism ; Humans ; Learning - physiology ; Mammals - metabolism ; Punishment ; Reward</subject><ispartof>Science advances, 2023-12, Vol.9 (48), p.eadi4927-eadi4927</ispartof><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c335t-d348389f404917bb9351d1c5d6b3407bcf1f18945ddf484b71147f53286122193</citedby><cites>FETCH-LOGICAL-c335t-d348389f404917bb9351d1c5d6b3407bcf1f18945ddf484b71147f53286122193</cites><orcidid>0009-0003-1552-5504 ; 0000-0002-1063-0431 ; 0009-0004-5150-4628 ; 0000-0002-7394-8922 ; 0000-0003-2451-6530 ; 0000-0003-2950-4395 ; 0000-0002-4631-5476</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>314,780,784,864,27924,27925</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/38039368$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Sands, L Paul</creatorcontrib><creatorcontrib>Jiang, Angela</creatorcontrib><creatorcontrib>Liebenow, Brittany</creatorcontrib><creatorcontrib>DiMarco, Emily</creatorcontrib><creatorcontrib>Laxton, Adrian W</creatorcontrib><creatorcontrib>Tatter, Stephen B</creatorcontrib><creatorcontrib>Montague, P Read</creatorcontrib><creatorcontrib>Kishida, Kenneth T</creatorcontrib><title>Subsecond fluctuations in extracellular dopamine encode reward and punishment prediction errors in humans</title><title>Science advances</title><addtitle>Sci Adv</addtitle><description>In the mammalian brain, midbrain dopamine neuron activity is hypothesized to encode reward prediction errors that promote learning and guide behavior by causing rapid changes in dopamine levels in target brain regions. This hypothesis (and alternatives regarding dopamine's role in punishment-learning) has limited direct evidence in humans. We report intracranial, subsecond measurements of dopamine release in human striatum measured, while volunteers (i.e., patients undergoing deep brain stimulation surgery) performed a probabilistic reward and punishment learning choice task designed to test whether dopamine release encodes only reward prediction errors or whether dopamine release may also encode adaptive punishment learning signals. Results demonstrate that extracellular dopamine levels can encode both reward and punishment prediction errors within distinct time intervals via independent valence-specific pathways in the human brain.</description><subject>Animals</subject><subject>Brain - metabolism</subject><subject>Dopamine - metabolism</subject><subject>Humans</subject><subject>Learning - physiology</subject><subject>Mammals - metabolism</subject><subject>Punishment</subject><subject>Reward</subject><issn>2375-2548</issn><issn>2375-2548</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2023</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNpNkDtPwzAURi0EolXpyog8sqT4mdgjqnhJlRiAOXL8UI0SJ9gxj39PQwtiunf4vnN1DwDnGK0wJuVV0l6Z95UynklSHYE5oRUvCGfi-N8-A8uUXhFCmJUlx_IUzKhAVNJSzIF_yk2yug8GujbrMavR9yFBH6D9HKPStm1zqyI0_aA6Hyy0QffGwmg_VDRQ7YpDDj5tOxtGOERrvJ4Q0MbYxx_QNncqpDNw4lSb7PIwF-Dl9uZ5fV9sHu8e1tebQlPKx8JQJqiQjiEmcdU0knJssOambChDVaMddlhIxo1xTLCmwphVjlMiSkwIlnQBLvfcIfZv2aax7nya3lDB9jnVRMhSoGo6swCrfVTHPqVoXT1E36n4VWNUT4brveH6YHhXuDiwc9NZ8xf_9Um_Ab1Kehg</recordid><startdate>202312</startdate><enddate>202312</enddate><creator>Sands, L Paul</creator><creator>Jiang, Angela</creator><creator>Liebenow, Brittany</creator><creator>DiMarco, Emily</creator><creator>Laxton, Adrian W</creator><creator>Tatter, Stephen B</creator><creator>Montague, P Read</creator><creator>Kishida, Kenneth T</creator><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>7X8</scope><orcidid>https://orcid.org/0009-0003-1552-5504</orcidid><orcidid>https://orcid.org/0000-0002-1063-0431</orcidid><orcidid>https://orcid.org/0009-0004-5150-4628</orcidid><orcidid>https://orcid.org/0000-0002-7394-8922</orcidid><orcidid>https://orcid.org/0000-0003-2451-6530</orcidid><orcidid>https://orcid.org/0000-0003-2950-4395</orcidid><orcidid>https://orcid.org/0000-0002-4631-5476</orcidid></search><sort><creationdate>202312</creationdate><title>Subsecond fluctuations in extracellular dopamine encode reward and punishment prediction errors in humans</title><author>Sands, L Paul ; Jiang, Angela ; Liebenow, Brittany ; DiMarco, Emily ; Laxton, Adrian W ; Tatter, Stephen B ; Montague, P Read ; Kishida, Kenneth T</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c335t-d348389f404917bb9351d1c5d6b3407bcf1f18945ddf484b71147f53286122193</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2023</creationdate><topic>Animals</topic><topic>Brain - metabolism</topic><topic>Dopamine - metabolism</topic><topic>Humans</topic><topic>Learning - physiology</topic><topic>Mammals - metabolism</topic><topic>Punishment</topic><topic>Reward</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Sands, L Paul</creatorcontrib><creatorcontrib>Jiang, Angela</creatorcontrib><creatorcontrib>Liebenow, Brittany</creatorcontrib><creatorcontrib>DiMarco, Emily</creatorcontrib><creatorcontrib>Laxton, Adrian W</creatorcontrib><creatorcontrib>Tatter, Stephen B</creatorcontrib><creatorcontrib>Montague, P Read</creatorcontrib><creatorcontrib>Kishida, Kenneth T</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><jtitle>Science advances</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Sands, L Paul</au><au>Jiang, Angela</au><au>Liebenow, Brittany</au><au>DiMarco, Emily</au><au>Laxton, Adrian W</au><au>Tatter, Stephen B</au><au>Montague, P Read</au><au>Kishida, Kenneth T</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Subsecond fluctuations in extracellular dopamine encode reward and punishment prediction errors in humans</atitle><jtitle>Science advances</jtitle><addtitle>Sci Adv</addtitle><date>2023-12</date><risdate>2023</risdate><volume>9</volume><issue>48</issue><spage>eadi4927</spage><epage>eadi4927</epage><pages>eadi4927-eadi4927</pages><issn>2375-2548</issn><eissn>2375-2548</eissn><abstract>In the mammalian brain, midbrain dopamine neuron activity is hypothesized to encode reward prediction errors that promote learning and guide behavior by causing rapid changes in dopamine levels in target brain regions. This hypothesis (and alternatives regarding dopamine's role in punishment-learning) has limited direct evidence in humans. We report intracranial, subsecond measurements of dopamine release in human striatum measured, while volunteers (i.e., patients undergoing deep brain stimulation surgery) performed a probabilistic reward and punishment learning choice task designed to test whether dopamine release encodes only reward prediction errors or whether dopamine release may also encode adaptive punishment learning signals. Results demonstrate that extracellular dopamine levels can encode both reward and punishment prediction errors within distinct time intervals via independent valence-specific pathways in the human brain.</abstract><cop>United States</cop><pmid>38039368</pmid><doi>10.1126/sciadv.adi4927</doi><orcidid>https://orcid.org/0009-0003-1552-5504</orcidid><orcidid>https://orcid.org/0000-0002-1063-0431</orcidid><orcidid>https://orcid.org/0009-0004-5150-4628</orcidid><orcidid>https://orcid.org/0000-0002-7394-8922</orcidid><orcidid>https://orcid.org/0000-0003-2451-6530</orcidid><orcidid>https://orcid.org/0000-0003-2950-4395</orcidid><orcidid>https://orcid.org/0000-0002-4631-5476</orcidid><oa>free_for_read</oa></addata></record> |
fulltext | fulltext |
identifier | ISSN: 2375-2548 |
ispartof | Science advances, 2023-12, Vol.9 (48), p.eadi4927-eadi4927 |
issn | 2375-2548 2375-2548 |
language | eng |
recordid | cdi_proquest_miscellaneous_2896807348 |
source | MEDLINE; DOAJ Directory of Open Access Journals; EZB-FREE-00999 freely available EZB journals; PubMed Central |
subjects | Animals Brain - metabolism Dopamine - metabolism Humans Learning - physiology Mammals - metabolism Punishment Reward |
title | Subsecond fluctuations in extracellular dopamine encode reward and punishment prediction errors in humans |
url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-01-07T08%3A38%3A17IST&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=Subsecond%20fluctuations%20in%20extracellular%20dopamine%20encode%20reward%20and%20punishment%20prediction%20errors%20in%20humans&rft.jtitle=Science%20advances&rft.au=Sands,%20L%20Paul&rft.date=2023-12&rft.volume=9&rft.issue=48&rft.spage=eadi4927&rft.epage=eadi4927&rft.pages=eadi4927-eadi4927&rft.issn=2375-2548&rft.eissn=2375-2548&rft_id=info:doi/10.1126/sciadv.adi4927&rft_dat=%3Cproquest_cross%3E2896807348%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=2896807348&rft_id=info:pmid/38039368&rfr_iscdi=true |