Modeling the effects of motivation on choice and learning in the basal ganglia
Decision making relies on adequately evaluating the consequences of actions on the basis of past experience and the current physiological state. A key role in this process is played by the basal ganglia, where neural activity and plasticity are modulated by dopaminergic input from the midbrain. Inte...
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description | Decision making relies on adequately evaluating the consequences of actions on the basis of past experience and the current physiological state. A key role in this process is played by the basal ganglia, where neural activity and plasticity are modulated by dopaminergic input from the midbrain. Internal physiological factors, such as hunger, scale signals encoded by dopaminergic neurons and thus they alter the motivation for taking actions and learning. However, to our knowledge, no formal mathematical formulation exists for how a physiological state affects learning and action selection in the basal ganglia. We developed a framework for modelling the effect of motivation on choice and learning. The framework defines the motivation to obtain a particular resource as the difference between the desired and the current level of this resource, and proposes how the utility of reinforcements depends on the motivation. To account for dopaminergic activity previously recorded in different physiological states, the paper argues that the prediction error encoded in the dopaminergic activity needs to be redefined as the difference between utility and expected utility, which depends on both the objective reinforcement and the motivation. We also demonstrate a possible mechanism by which the evaluation and learning of utility of actions can be implemented in the basal ganglia network. The presented theory brings together models of learning in the basal ganglia with the incentive salience theory in a single simple framework, and it provides a mechanistic insight into how decision processes and learning in the basal ganglia are modulated by the motivation. Moreover, this theory is also consistent with data on neural underpinnings of overeating and obesity, and makes further experimental predictions. |
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To account for dopaminergic activity previously recorded in different physiological states, the paper argues that the prediction error encoded in the dopaminergic activity needs to be redefined as the difference between utility and expected utility, which depends on both the objective reinforcement and the motivation. We also demonstrate a possible mechanism by which the evaluation and learning of utility of actions can be implemented in the basal ganglia network. The presented theory brings together models of learning in the basal ganglia with the incentive salience theory in a single simple framework, and it provides a mechanistic insight into how decision processes and learning in the basal ganglia are modulated by the motivation. 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This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. 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A key role in this process is played by the basal ganglia, where neural activity and plasticity are modulated by dopaminergic input from the midbrain. Internal physiological factors, such as hunger, scale signals encoded by dopaminergic neurons and thus they alter the motivation for taking actions and learning. However, to our knowledge, no formal mathematical formulation exists for how a physiological state affects learning and action selection in the basal ganglia. We developed a framework for modelling the effect of motivation on choice and learning. The framework defines the motivation to obtain a particular resource as the difference between the desired and the current level of this resource, and proposes how the utility of reinforcements depends on the motivation. To account for dopaminergic activity previously recorded in different physiological states, the paper argues that the prediction error encoded in the dopaminergic activity needs to be redefined as the difference between utility and expected utility, which depends on both the objective reinforcement and the motivation. We also demonstrate a possible mechanism by which the evaluation and learning of utility of actions can be implemented in the basal ganglia network. The presented theory brings together models of learning in the basal ganglia with the incentive salience theory in a single simple framework, and it provides a mechanistic insight into how decision processes and learning in the basal ganglia are modulated by the motivation. Moreover, this theory is also consistent with data on neural underpinnings of overeating and obesity, and makes further experimental predictions.</description><subject>Animals</subject><subject>Basal ganglia</subject><subject>Basal Ganglia - physiology</subject><subject>Behavior, Animal</subject><subject>Biology and Life Sciences</subject><subject>Choice Behavior</subject><subject>Choice learning</subject><subject>Computer Simulation</subject><subject>Decision making</subject><subject>Dopamine</subject><subject>Dopamine - physiology</subject><subject>Dopamine receptors</subject><subject>Dopaminergic Neurons - physiology</subject><subject>Expected utility</subject><subject>Expected values</subject><subject>Ganglia</subject><subject>Humans</subject><subject>Hunger</subject><subject>Learning</subject><subject>Mathematical models</subject><subject>Medicine and Health Sciences</subject><subject>Mesencephalon</subject><subject>Mesencephalon - physiology</subject><subject>Mice</subject><subject>Models, Neurological</subject><subject>Motivation</subject><subject>Motivation (Psychology)</subject><subject>Neural Pathways - physiology</subject><subject>Neural plasticity</subject><subject>Neuroplasticity</subject><subject>Physical Sciences</subject><subject>Physiological aspects</subject><subject>Physiological effects</subject><subject>Physiological factors</subject><subject>Physiology</subject><subject>Psychological aspects</subject><subject>Reinforcement, Psychology</subject><subject>Research and Analysis Methods</subject><subject>Reward</subject><subject>Social Sciences</subject><subject>Utility functions</subject><issn>1553-7358</issn><issn>1553-734X</issn><issn>1553-7358</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2020</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>BENPR</sourceid><sourceid>DOA</sourceid><recordid>eNqVkl1rFDEUhgdRbK3-A9EBb-rFrsnka3MjlFJ1oVbw4zqcycdslmyyncwW_fdmutPSld5IAgnnPO-bnMOpqtcYzTER-MM67foIYb7VrZ9jhATl7El1jBkjM0HY4umD-1H1Iuc1QuUq-fPqiDSUEdGw4-rqazI2-NjVw8rW1jmrh1wnV2_S4G9g8CnWZetV8trWEE0dLPRxFPh4q2khQ6g7iF3w8LJ65iBk-2o6T6pfny5-nn-ZXX77vDw_u5xpzvEwAyI0EVJaQzlHDmHXusYsCG4kFpRKbaQjyCJa0gYz22rsmKMSAHHudEtOqrd7321IWU2tyKqhHAkmF4QXYrknTIK12vZ-A_0flcCr20DqOwX94HWwylDaUINbKrCmreQLhxeiabEEDlaDK14fp9d27cYabePQQzgwPcxEv1JdulGiKdUIVgxOJ4M-Xe9sHtTGZ21DgGjTbvw3EgQTxlFB3_2DPl7dRHVQCvDRpfKuHk3VGSeNpKVPuFDzR6iyjN14naJ1vsQPBO8PBIUZ7O-hg13Oavnj-3-wV4cs3bO6Tzn31t33DiM1TvNdkWqcZjVNc5G9edj3e9Hd-JK_e0Xu3Q</recordid><startdate>20200501</startdate><enddate>20200501</enddate><creator>van Swieten, Maaike M H</creator><creator>Bogacz, Rafal</creator><general>Public Library of Science</general><general>Public Library of Science (PLoS)</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>ISN</scope><scope>ISR</scope><scope>3V.</scope><scope>7QO</scope><scope>7QP</scope><scope>7TK</scope><scope>7TM</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8AL</scope><scope>8FD</scope><scope>8FE</scope><scope>8FG</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AEUYN</scope><scope>AFKRA</scope><scope>ARAPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BGLVJ</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>JQ2</scope><scope>K7-</scope><scope>K9.</scope><scope>LK8</scope><scope>M0N</scope><scope>M0S</scope><scope>M1P</scope><scope>M7P</scope><scope>P5Z</scope><scope>P62</scope><scope>P64</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>Q9U</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope><orcidid>https://orcid.org/0000-0002-7361-9467</orcidid><orcidid>https://orcid.org/0000-0002-8994-1661</orcidid></search><sort><creationdate>20200501</creationdate><title>Modeling the effects of motivation on choice and learning in the basal ganglia</title><author>van Swieten, Maaike M H ; Bogacz, Rafal</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c661t-a37c3799ed4660f01fbf2d8312917449cd9f30e04466d15ebc1f5f49aa066fcb3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2020</creationdate><topic>Animals</topic><topic>Basal ganglia</topic><topic>Basal Ganglia - physiology</topic><topic>Behavior, Animal</topic><topic>Biology and Life Sciences</topic><topic>Choice Behavior</topic><topic>Choice learning</topic><topic>Computer Simulation</topic><topic>Decision making</topic><topic>Dopamine</topic><topic>Dopamine - physiology</topic><topic>Dopamine receptors</topic><topic>Dopaminergic Neurons - physiology</topic><topic>Expected utility</topic><topic>Expected values</topic><topic>Ganglia</topic><topic>Humans</topic><topic>Hunger</topic><topic>Learning</topic><topic>Mathematical models</topic><topic>Medicine and Health Sciences</topic><topic>Mesencephalon</topic><topic>Mesencephalon - physiology</topic><topic>Mice</topic><topic>Models, Neurological</topic><topic>Motivation</topic><topic>Motivation (Psychology)</topic><topic>Neural Pathways - physiology</topic><topic>Neural plasticity</topic><topic>Neuroplasticity</topic><topic>Physical Sciences</topic><topic>Physiological aspects</topic><topic>Physiological effects</topic><topic>Physiological factors</topic><topic>Physiology</topic><topic>Psychological aspects</topic><topic>Reinforcement, Psychology</topic><topic>Research and Analysis Methods</topic><topic>Reward</topic><topic>Social Sciences</topic><topic>Utility functions</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>van Swieten, Maaike M H</creatorcontrib><creatorcontrib>Bogacz, Rafal</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Gale In Context: Canada</collection><collection>Gale In Context: Science</collection><collection>ProQuest Central (Corporate)</collection><collection>Biotechnology Research Abstracts</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Medical Database (Alumni Edition)</collection><collection>Computing Database (Alumni Edition)</collection><collection>Technology Research Database</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Technology 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 One Sustainability</collection><collection>ProQuest Central UK/Ireland</collection><collection>Advanced Technologies & Aerospace Collection</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>Technology Collection</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 Computer Science Collection</collection><collection>Computer Science Database</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>ProQuest Biological Science Collection</collection><collection>Computing Database</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>Biological Science Database</collection><collection>Advanced Technologies & Aerospace Database</collection><collection>ProQuest Advanced Technologies & Aerospace Collection</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Publicly Available Content Database</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 Central Basic</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PLoS computational biology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>van Swieten, Maaike M H</au><au>Bogacz, Rafal</au><au>Rubin, Jonathan</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Modeling the effects of motivation on choice and learning in the basal ganglia</atitle><jtitle>PLoS computational biology</jtitle><addtitle>PLoS Comput Biol</addtitle><date>2020-05-01</date><risdate>2020</risdate><volume>16</volume><issue>5</issue><spage>e1007465</spage><epage>e1007465</epage><pages>e1007465-e1007465</pages><issn>1553-7358</issn><issn>1553-734X</issn><eissn>1553-7358</eissn><abstract>Decision making relies on adequately evaluating the consequences of actions on the basis of past experience and the current physiological state. A key role in this process is played by the basal ganglia, where neural activity and plasticity are modulated by dopaminergic input from the midbrain. Internal physiological factors, such as hunger, scale signals encoded by dopaminergic neurons and thus they alter the motivation for taking actions and learning. However, to our knowledge, no formal mathematical formulation exists for how a physiological state affects learning and action selection in the basal ganglia. We developed a framework for modelling the effect of motivation on choice and learning. The framework defines the motivation to obtain a particular resource as the difference between the desired and the current level of this resource, and proposes how the utility of reinforcements depends on the motivation. To account for dopaminergic activity previously recorded in different physiological states, the paper argues that the prediction error encoded in the dopaminergic activity needs to be redefined as the difference between utility and expected utility, which depends on both the objective reinforcement and the motivation. We also demonstrate a possible mechanism by which the evaluation and learning of utility of actions can be implemented in the basal ganglia network. The presented theory brings together models of learning in the basal ganglia with the incentive salience theory in a single simple framework, and it provides a mechanistic insight into how decision processes and learning in the basal ganglia are modulated by the motivation. Moreover, this theory is also consistent with data on neural underpinnings of overeating and obesity, and makes further experimental predictions.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>32453725</pmid><doi>10.1371/journal.pcbi.1007465</doi><orcidid>https://orcid.org/0000-0002-7361-9467</orcidid><orcidid>https://orcid.org/0000-0002-8994-1661</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Animals Basal ganglia Basal Ganglia - physiology Behavior, Animal Biology and Life Sciences Choice Behavior Choice learning Computer Simulation Decision making Dopamine Dopamine - physiology Dopamine receptors Dopaminergic Neurons - physiology Expected utility Expected values Ganglia Humans Hunger Learning Mathematical models Medicine and Health Sciences Mesencephalon Mesencephalon - physiology Mice Models, Neurological Motivation Motivation (Psychology) Neural Pathways - physiology Neural plasticity Neuroplasticity Physical Sciences Physiological aspects Physiological effects Physiological factors Physiology Psychological aspects Reinforcement, Psychology Research and Analysis Methods Reward Social Sciences Utility functions |
title | Modeling the effects of motivation on choice and learning in the basal ganglia |
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