Dynamic Nigrostriatal Dopamine Biases Action Selection
Dopamine is thought to play a critical role in reinforcement learning and goal-directed behavior, but its function in action selection remains largely unknown. Here we demonstrate that nigrostriatal dopamine biases ongoing action selection. When mice were trained to dynamically switch the action sel...
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Veröffentlicht in: | Neuron (Cambridge, Mass.) Mass.), 2017-03, Vol.93 (6), p.1436-1450.e8 |
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description | Dopamine is thought to play a critical role in reinforcement learning and goal-directed behavior, but its function in action selection remains largely unknown. Here we demonstrate that nigrostriatal dopamine biases ongoing action selection. When mice were trained to dynamically switch the action selected at different time points, changes in firing rate of nigrostriatal dopamine neurons, as well as dopamine signaling in the dorsal striatum, were found to be associated with action selection. This dopamine profile is specific to behavioral choice, scalable with interval duration, and doesn’t reflect reward prediction error, timing, or value as single factors alone. Genetic deletion of NMDA receptors on dopamine or striatal neurons or optogenetic manipulation of dopamine concentration alters dopamine signaling and biases action selection. These results unveil a crucial role of nigrostriatal dopamine in integrating diverse information for regulating upcoming actions, and they have important implications for neurological disorders, including Parkinson’s disease and substance dependence.
•Nigrostriatal dopamine signaling is associated with ongoing action selection•Dopamine signaling is necessary for appropriate action selection•Optogenetic manipulations can bidirectionally modulate online action selection•Modeling suggests dopamine could bias choice by modifying striatal activity
Howard et al. recorded nigrostriatal dopamine signaling while animals dynamically altered their actions to retrieve rewards. They found that dopamine signaling is associated with action selection and that modulating dopamine biases the online action selection processes. |
doi_str_mv | 10.1016/j.neuron.2017.02.029 |
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•Nigrostriatal dopamine signaling is associated with ongoing action selection•Dopamine signaling is necessary for appropriate action selection•Optogenetic manipulations can bidirectionally modulate online action selection•Modeling suggests dopamine could bias choice by modifying striatal activity
Howard et al. recorded nigrostriatal dopamine signaling while animals dynamically altered their actions to retrieve rewards. They found that dopamine signaling is associated with action selection and that modulating dopamine biases the online action selection processes.</description><identifier>ISSN: 0896-6273</identifier><identifier>EISSN: 1097-4199</identifier><identifier>DOI: 10.1016/j.neuron.2017.02.029</identifier><identifier>PMID: 28285820</identifier><language>eng</language><publisher>United States: Elsevier Inc</publisher><subject>action selection ; Addictive behaviors ; Animals ; basal ganglia ; Behavior ; Caudate-putamen ; conditional knockout ; Conditioning, Operant - physiology ; Corpus Striatum - physiology ; Decision making ; direct and indirect pathway ; Dopamine ; Dopamine - metabolism ; Dopaminergic Neurons - physiology ; electrophysiology ; fast-scan cyclic voltammetry ; Female ; Firing rate ; Glutamic acid receptors (ionotropic) ; Male ; Mice ; Mice, Knockout ; Mice, Transgenic ; N-Methyl-D-aspartic acid receptors ; Neostriatum ; network model ; Neural Pathways - physiology ; Neurological diseases ; Neurons ; Neurosciences ; optogenetics ; Receptors, N-Methyl-D-Aspartate - genetics ; Receptors, N-Methyl-D-Aspartate - physiology ; Reinforcement ; Reward ; striatum ; Substantia Nigra - physiology ; Voltammetry</subject><ispartof>Neuron (Cambridge, Mass.), 2017-03, Vol.93 (6), p.1436-1450.e8</ispartof><rights>2017 Elsevier Inc.</rights><rights>Copyright © 2017 Elsevier Inc. All rights reserved.</rights><rights>Copyright Elsevier Limited Mar 22, 2017</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c557t-a18437785d5fa9fda38a26aa7e4c29c8d335655dae1203b483273a815519d3b73</citedby><cites>FETCH-LOGICAL-c557t-a18437785d5fa9fda38a26aa7e4c29c8d335655dae1203b483273a815519d3b73</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://dx.doi.org/10.1016/j.neuron.2017.02.029$$EHTML$$P50$$Gelsevier$$Hfree_for_read</linktohtml><link.rule.ids>230,314,780,784,885,3550,27924,27925,45995</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/28285820$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Howard, Christopher D.</creatorcontrib><creatorcontrib>Li, Hao</creatorcontrib><creatorcontrib>Geddes, Claire E.</creatorcontrib><creatorcontrib>Jin, Xin</creatorcontrib><title>Dynamic Nigrostriatal Dopamine Biases Action Selection</title><title>Neuron (Cambridge, Mass.)</title><addtitle>Neuron</addtitle><description>Dopamine is thought to play a critical role in reinforcement learning and goal-directed behavior, but its function in action selection remains largely unknown. Here we demonstrate that nigrostriatal dopamine biases ongoing action selection. When mice were trained to dynamically switch the action selected at different time points, changes in firing rate of nigrostriatal dopamine neurons, as well as dopamine signaling in the dorsal striatum, were found to be associated with action selection. This dopamine profile is specific to behavioral choice, scalable with interval duration, and doesn’t reflect reward prediction error, timing, or value as single factors alone. Genetic deletion of NMDA receptors on dopamine or striatal neurons or optogenetic manipulation of dopamine concentration alters dopamine signaling and biases action selection. These results unveil a crucial role of nigrostriatal dopamine in integrating diverse information for regulating upcoming actions, and they have important implications for neurological disorders, including Parkinson’s disease and substance dependence.
•Nigrostriatal dopamine signaling is associated with ongoing action selection•Dopamine signaling is necessary for appropriate action selection•Optogenetic manipulations can bidirectionally modulate online action selection•Modeling suggests dopamine could bias choice by modifying striatal activity
Howard et al. recorded nigrostriatal dopamine signaling while animals dynamically altered their actions to retrieve rewards. They found that dopamine signaling is associated with action selection and that modulating dopamine biases the online action selection processes.</description><subject>action selection</subject><subject>Addictive behaviors</subject><subject>Animals</subject><subject>basal ganglia</subject><subject>Behavior</subject><subject>Caudate-putamen</subject><subject>conditional knockout</subject><subject>Conditioning, Operant - physiology</subject><subject>Corpus Striatum - physiology</subject><subject>Decision making</subject><subject>direct and indirect pathway</subject><subject>Dopamine</subject><subject>Dopamine - metabolism</subject><subject>Dopaminergic Neurons - physiology</subject><subject>electrophysiology</subject><subject>fast-scan cyclic voltammetry</subject><subject>Female</subject><subject>Firing rate</subject><subject>Glutamic acid receptors (ionotropic)</subject><subject>Male</subject><subject>Mice</subject><subject>Mice, Knockout</subject><subject>Mice, Transgenic</subject><subject>N-Methyl-D-aspartic acid receptors</subject><subject>Neostriatum</subject><subject>network model</subject><subject>Neural Pathways - physiology</subject><subject>Neurological diseases</subject><subject>Neurons</subject><subject>Neurosciences</subject><subject>optogenetics</subject><subject>Receptors, N-Methyl-D-Aspartate - genetics</subject><subject>Receptors, N-Methyl-D-Aspartate - physiology</subject><subject>Reinforcement</subject><subject>Reward</subject><subject>striatum</subject><subject>Substantia Nigra - physiology</subject><subject>Voltammetry</subject><issn>0896-6273</issn><issn>1097-4199</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2017</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp9UU1PGzEQtVARpMA_QNVKvfSywR_rtX2pRIEWJAQH4GxNvBPqaGOn9i4S_x6HUCg9II1ky37zZt57hBwyOmWUtUeLacAxxTDllKkp5aXMFpkwalTdMGM-kQnVpq1brsQu-ZzzglLWSMN2yC7XXEvN6YS0p48Blt5VV_4-xTwkDwP01WlcldeA1Q8PGXN17AYfQ3WDPT7f9sn2HPqMBy_nHrn7eXZ7cl5fXv-6ODm-rJ2UaqiB6UYopWUn52DmHQgNvAVQ2DhunO6EkK2UHSDjVMwaLcqyoJmUzHRipsQe-b7hXY2zJXYOw5Cgt6vkl5AebQRv3_8E_9vexwcrhRGCrgm-vRCk-GfEPNilzw77HgLGMVumVatZozgv0K__QRdxTKHIKyjd8JYWJQXVbFCu2JUTzl-XYdSug7ELuwnGroOxlJcype3Lv0Jem_4m8aYUi50PHpPNzmNw2PlUPLdd9B9PeAI1fqBc</recordid><startdate>20170322</startdate><enddate>20170322</enddate><creator>Howard, Christopher D.</creator><creator>Li, Hao</creator><creator>Geddes, Claire E.</creator><creator>Jin, Xin</creator><general>Elsevier Inc</general><general>Elsevier Limited</general><scope>6I.</scope><scope>AAFTH</scope><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>7QP</scope><scope>7QR</scope><scope>7TK</scope><scope>8FD</scope><scope>FR3</scope><scope>K9.</scope><scope>NAPCQ</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope></search><sort><creationdate>20170322</creationdate><title>Dynamic Nigrostriatal Dopamine Biases Action Selection</title><author>Howard, Christopher D. ; Li, Hao ; Geddes, Claire E. ; Jin, Xin</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c557t-a18437785d5fa9fda38a26aa7e4c29c8d335655dae1203b483273a815519d3b73</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2017</creationdate><topic>action selection</topic><topic>Addictive behaviors</topic><topic>Animals</topic><topic>basal ganglia</topic><topic>Behavior</topic><topic>Caudate-putamen</topic><topic>conditional knockout</topic><topic>Conditioning, Operant - physiology</topic><topic>Corpus Striatum - physiology</topic><topic>Decision making</topic><topic>direct and indirect pathway</topic><topic>Dopamine</topic><topic>Dopamine - metabolism</topic><topic>Dopaminergic Neurons - physiology</topic><topic>electrophysiology</topic><topic>fast-scan cyclic voltammetry</topic><topic>Female</topic><topic>Firing rate</topic><topic>Glutamic acid receptors (ionotropic)</topic><topic>Male</topic><topic>Mice</topic><topic>Mice, Knockout</topic><topic>Mice, Transgenic</topic><topic>N-Methyl-D-aspartic acid receptors</topic><topic>Neostriatum</topic><topic>network model</topic><topic>Neural Pathways - physiology</topic><topic>Neurological diseases</topic><topic>Neurons</topic><topic>Neurosciences</topic><topic>optogenetics</topic><topic>Receptors, N-Methyl-D-Aspartate - genetics</topic><topic>Receptors, N-Methyl-D-Aspartate - physiology</topic><topic>Reinforcement</topic><topic>Reward</topic><topic>striatum</topic><topic>Substantia Nigra - physiology</topic><topic>Voltammetry</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Howard, Christopher D.</creatorcontrib><creatorcontrib>Li, Hao</creatorcontrib><creatorcontrib>Geddes, Claire E.</creatorcontrib><creatorcontrib>Jin, Xin</creatorcontrib><collection>ScienceDirect Open Access Titles</collection><collection>Elsevier:ScienceDirect:Open Access</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>Technology Research Database</collection><collection>Engineering Research Database</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Nursing & Allied Health Premium</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Neuron (Cambridge, Mass.)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Howard, Christopher D.</au><au>Li, Hao</au><au>Geddes, Claire E.</au><au>Jin, Xin</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Dynamic Nigrostriatal Dopamine Biases Action Selection</atitle><jtitle>Neuron (Cambridge, Mass.)</jtitle><addtitle>Neuron</addtitle><date>2017-03-22</date><risdate>2017</risdate><volume>93</volume><issue>6</issue><spage>1436</spage><epage>1450.e8</epage><pages>1436-1450.e8</pages><issn>0896-6273</issn><eissn>1097-4199</eissn><abstract>Dopamine is thought to play a critical role in reinforcement learning and goal-directed behavior, but its function in action selection remains largely unknown. Here we demonstrate that nigrostriatal dopamine biases ongoing action selection. When mice were trained to dynamically switch the action selected at different time points, changes in firing rate of nigrostriatal dopamine neurons, as well as dopamine signaling in the dorsal striatum, were found to be associated with action selection. This dopamine profile is specific to behavioral choice, scalable with interval duration, and doesn’t reflect reward prediction error, timing, or value as single factors alone. Genetic deletion of NMDA receptors on dopamine or striatal neurons or optogenetic manipulation of dopamine concentration alters dopamine signaling and biases action selection. These results unveil a crucial role of nigrostriatal dopamine in integrating diverse information for regulating upcoming actions, and they have important implications for neurological disorders, including Parkinson’s disease and substance dependence.
•Nigrostriatal dopamine signaling is associated with ongoing action selection•Dopamine signaling is necessary for appropriate action selection•Optogenetic manipulations can bidirectionally modulate online action selection•Modeling suggests dopamine could bias choice by modifying striatal activity
Howard et al. recorded nigrostriatal dopamine signaling while animals dynamically altered their actions to retrieve rewards. They found that dopamine signaling is associated with action selection and that modulating dopamine biases the online action selection processes.</abstract><cop>United States</cop><pub>Elsevier Inc</pub><pmid>28285820</pmid><doi>10.1016/j.neuron.2017.02.029</doi><oa>free_for_read</oa></addata></record> |
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subjects | action selection Addictive behaviors Animals basal ganglia Behavior Caudate-putamen conditional knockout Conditioning, Operant - physiology Corpus Striatum - physiology Decision making direct and indirect pathway Dopamine Dopamine - metabolism Dopaminergic Neurons - physiology electrophysiology fast-scan cyclic voltammetry Female Firing rate Glutamic acid receptors (ionotropic) Male Mice Mice, Knockout Mice, Transgenic N-Methyl-D-aspartic acid receptors Neostriatum network model Neural Pathways - physiology Neurological diseases Neurons Neurosciences optogenetics Receptors, N-Methyl-D-Aspartate - genetics Receptors, N-Methyl-D-Aspartate - physiology Reinforcement Reward striatum Substantia Nigra - physiology Voltammetry |
title | Dynamic Nigrostriatal Dopamine Biases Action Selection |
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