The neurocomputational bases of explore-exploit decision-making
Flexible decision-making requires animals to forego immediate rewards (exploitation) and try novel choice options (exploration) to discover if they are preferable to familiar alternatives. Using the same task and a partially observable Markov decision process (POMDP) model to quantify the value of c...
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Veröffentlicht in: | Neuron (Cambridge, Mass.) Mass.), 2022-06, Vol.110 (11), p.1869-1879.e5 |
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creator | Hogeveen, Jeremy Mullins, Teagan S. Romero, John D. Eversole, Elizabeth Rogge-Obando, Kimberly Mayer, Andrew R. Costa, Vincent D. |
description | Flexible decision-making requires animals to forego immediate rewards (exploitation) and try novel choice options (exploration) to discover if they are preferable to familiar alternatives. Using the same task and a partially observable Markov decision process (POMDP) model to quantify the value of choices, we first determined that the computational basis for managing explore-exploit tradeoffs is conserved across monkeys and humans. We then used fMRI to identify where in the human brain the immediate value of exploitative choices and relative uncertainty about the value of exploratory choices were encoded. Consistent with prior neurophysiological evidence in monkeys, we observed divergent encoding of reward value and uncertainty in prefrontal and parietal regions, including frontopolar cortex, and parallel encoding of these computations in motivational regions including the amygdala, ventral striatum, and orbitofrontal cortex. These results clarify the interplay between prefrontal and motivational circuits that supports adaptive explore-exploit decisions in humans and nonhuman primates.
•Value and uncertainty direct explore-exploit decisions in humans and monkeys•A prefrontal subdivision unique to primates encodes when exploration is valuable•Frontoparietal brain regions show dissociable encoding of value and uncertainty•Motivational brain regions complement prefrontal contributions to exploration
How do humans and other animals make the decision to explore new options instead of exploiting familiar favorites? Hogeveen et al. find evidence for similar computations underlying explore-exploit decisions across humans and monkeys. Additionally, their study reveals a brain-wide network comprising frontopolar, frontoparietal, frontostriatal, and mesocorticolimbic regions underlying explore-exploit decisions. |
doi_str_mv | 10.1016/j.neuron.2022.03.014 |
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•Value and uncertainty direct explore-exploit decisions in humans and monkeys•A prefrontal subdivision unique to primates encodes when exploration is valuable•Frontoparietal brain regions show dissociable encoding of value and uncertainty•Motivational brain regions complement prefrontal contributions to exploration
How do humans and other animals make the decision to explore new options instead of exploiting familiar favorites? Hogeveen et al. find evidence for similar computations underlying explore-exploit decisions across humans and monkeys. Additionally, their study reveals a brain-wide network comprising frontopolar, frontoparietal, frontostriatal, and mesocorticolimbic regions underlying explore-exploit decisions.</description><identifier>ISSN: 0896-6273</identifier><identifier>EISSN: 1097-4199</identifier><identifier>DOI: 10.1016/j.neuron.2022.03.014</identifier><identifier>PMID: 35390278</identifier><language>eng</language><publisher>United States: Elsevier Inc</publisher><subject>amygdala ; Animals ; Choice Behavior - physiology ; computational modeling ; Decision Making - physiology ; decision-making ; exploration ; explore-exploit dilemma ; fMRI ; frontopolar cortex ; Prefrontal Cortex - diagnostic imaging ; Prefrontal Cortex - physiology ; reinforcement learning ; Reward ; striatum ; Ventral Striatum - diagnostic imaging ; Ventral Striatum - physiology</subject><ispartof>Neuron (Cambridge, Mass.), 2022-06, Vol.110 (11), p.1869-1879.e5</ispartof><rights>2022 Elsevier Inc.</rights><rights>Copyright © 2022 Elsevier Inc. All rights reserved.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c529t-62e8e8c8cfe320ae19a235cc96cbec553d8065a2547566fd55e83a86309379ab3</citedby><cites>FETCH-LOGICAL-c529t-62e8e8c8cfe320ae19a235cc96cbec553d8065a2547566fd55e83a86309379ab3</cites><orcidid>0000-0003-0592-8556 ; 0000-0001-9612-2085</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://www.sciencedirect.com/science/article/pii/S0896627322002501$$EHTML$$P50$$Gelsevier$$H</linktohtml><link.rule.ids>230,314,776,780,881,3537,27901,27902,65306</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/35390278$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Hogeveen, Jeremy</creatorcontrib><creatorcontrib>Mullins, Teagan S.</creatorcontrib><creatorcontrib>Romero, John D.</creatorcontrib><creatorcontrib>Eversole, Elizabeth</creatorcontrib><creatorcontrib>Rogge-Obando, Kimberly</creatorcontrib><creatorcontrib>Mayer, Andrew R.</creatorcontrib><creatorcontrib>Costa, Vincent D.</creatorcontrib><title>The neurocomputational bases of explore-exploit decision-making</title><title>Neuron (Cambridge, Mass.)</title><addtitle>Neuron</addtitle><description>Flexible decision-making requires animals to forego immediate rewards (exploitation) and try novel choice options (exploration) to discover if they are preferable to familiar alternatives. Using the same task and a partially observable Markov decision process (POMDP) model to quantify the value of choices, we first determined that the computational basis for managing explore-exploit tradeoffs is conserved across monkeys and humans. We then used fMRI to identify where in the human brain the immediate value of exploitative choices and relative uncertainty about the value of exploratory choices were encoded. Consistent with prior neurophysiological evidence in monkeys, we observed divergent encoding of reward value and uncertainty in prefrontal and parietal regions, including frontopolar cortex, and parallel encoding of these computations in motivational regions including the amygdala, ventral striatum, and orbitofrontal cortex. These results clarify the interplay between prefrontal and motivational circuits that supports adaptive explore-exploit decisions in humans and nonhuman primates.
•Value and uncertainty direct explore-exploit decisions in humans and monkeys•A prefrontal subdivision unique to primates encodes when exploration is valuable•Frontoparietal brain regions show dissociable encoding of value and uncertainty•Motivational brain regions complement prefrontal contributions to exploration
How do humans and other animals make the decision to explore new options instead of exploiting familiar favorites? Hogeveen et al. find evidence for similar computations underlying explore-exploit decisions across humans and monkeys. Additionally, their study reveals a brain-wide network comprising frontopolar, frontoparietal, frontostriatal, and mesocorticolimbic regions underlying explore-exploit decisions.</description><subject>amygdala</subject><subject>Animals</subject><subject>Choice Behavior - physiology</subject><subject>computational modeling</subject><subject>Decision Making - physiology</subject><subject>decision-making</subject><subject>exploration</subject><subject>explore-exploit dilemma</subject><subject>fMRI</subject><subject>frontopolar cortex</subject><subject>Prefrontal Cortex - diagnostic imaging</subject><subject>Prefrontal Cortex - physiology</subject><subject>reinforcement learning</subject><subject>Reward</subject><subject>striatum</subject><subject>Ventral Striatum - diagnostic imaging</subject><subject>Ventral Striatum - physiology</subject><issn>0896-6273</issn><issn>1097-4199</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2022</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp9kEtPwzAQhC0EoqXwDxDKkUuCH7FjX0Co4iUhcSlny3U24JLExU4q-PcEWgpcOO1hZ2dmP4SOCc4IJuJskbXQB99mFFOaYZZhku-gMcGqSHOi1C4aY6lEKmjBRuggxgUeFFyRfTRinClMCzlGF7NnSL6MrG-WfWc651tTJ3MTISa-SuBtWfsA6dd0XVKCdXHQpI15ce3TIdqrTB3haDMn6PH6aja9Te8fbu6ml_ep5VR1QwmQIK20FTCKDRBlKOPWKmHnYDlnpcSCG8rzggtRlZyDZEYKhhUrlJmzCTpf-y77eQOlhbYLptbL4BoT3rU3Tv_dtO5ZP_mVVkQUhZCDwenGIPjXHmKnGxct1LVpwfdRU5FLqRQe0ExQvpba4GMMUG1jCNaf7PVCr9nrT_YaMz2QHc5OflfcHn3D_vkBBlArB0FH66C1ULoAttOld_8nfABNdJk6</recordid><startdate>20220601</startdate><enddate>20220601</enddate><creator>Hogeveen, Jeremy</creator><creator>Mullins, Teagan S.</creator><creator>Romero, John D.</creator><creator>Eversole, Elizabeth</creator><creator>Rogge-Obando, Kimberly</creator><creator>Mayer, Andrew R.</creator><creator>Costa, Vincent D.</creator><general>Elsevier 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>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0003-0592-8556</orcidid><orcidid>https://orcid.org/0000-0001-9612-2085</orcidid></search><sort><creationdate>20220601</creationdate><title>The neurocomputational bases of explore-exploit decision-making</title><author>Hogeveen, Jeremy ; Mullins, Teagan S. ; Romero, John D. ; Eversole, Elizabeth ; Rogge-Obando, Kimberly ; Mayer, Andrew R. ; Costa, Vincent D.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c529t-62e8e8c8cfe320ae19a235cc96cbec553d8065a2547566fd55e83a86309379ab3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2022</creationdate><topic>amygdala</topic><topic>Animals</topic><topic>Choice Behavior - physiology</topic><topic>computational modeling</topic><topic>Decision Making - physiology</topic><topic>decision-making</topic><topic>exploration</topic><topic>explore-exploit dilemma</topic><topic>fMRI</topic><topic>frontopolar cortex</topic><topic>Prefrontal Cortex - diagnostic imaging</topic><topic>Prefrontal Cortex - physiology</topic><topic>reinforcement learning</topic><topic>Reward</topic><topic>striatum</topic><topic>Ventral Striatum - diagnostic imaging</topic><topic>Ventral Striatum - physiology</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Hogeveen, Jeremy</creatorcontrib><creatorcontrib>Mullins, Teagan S.</creatorcontrib><creatorcontrib>Romero, John D.</creatorcontrib><creatorcontrib>Eversole, Elizabeth</creatorcontrib><creatorcontrib>Rogge-Obando, Kimberly</creatorcontrib><creatorcontrib>Mayer, Andrew R.</creatorcontrib><creatorcontrib>Costa, Vincent D.</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><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>Hogeveen, Jeremy</au><au>Mullins, Teagan S.</au><au>Romero, John D.</au><au>Eversole, Elizabeth</au><au>Rogge-Obando, Kimberly</au><au>Mayer, Andrew R.</au><au>Costa, Vincent D.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>The neurocomputational bases of explore-exploit decision-making</atitle><jtitle>Neuron (Cambridge, Mass.)</jtitle><addtitle>Neuron</addtitle><date>2022-06-01</date><risdate>2022</risdate><volume>110</volume><issue>11</issue><spage>1869</spage><epage>1879.e5</epage><pages>1869-1879.e5</pages><issn>0896-6273</issn><eissn>1097-4199</eissn><abstract>Flexible decision-making requires animals to forego immediate rewards (exploitation) and try novel choice options (exploration) to discover if they are preferable to familiar alternatives. Using the same task and a partially observable Markov decision process (POMDP) model to quantify the value of choices, we first determined that the computational basis for managing explore-exploit tradeoffs is conserved across monkeys and humans. We then used fMRI to identify where in the human brain the immediate value of exploitative choices and relative uncertainty about the value of exploratory choices were encoded. Consistent with prior neurophysiological evidence in monkeys, we observed divergent encoding of reward value and uncertainty in prefrontal and parietal regions, including frontopolar cortex, and parallel encoding of these computations in motivational regions including the amygdala, ventral striatum, and orbitofrontal cortex. These results clarify the interplay between prefrontal and motivational circuits that supports adaptive explore-exploit decisions in humans and nonhuman primates.
•Value and uncertainty direct explore-exploit decisions in humans and monkeys•A prefrontal subdivision unique to primates encodes when exploration is valuable•Frontoparietal brain regions show dissociable encoding of value and uncertainty•Motivational brain regions complement prefrontal contributions to exploration
How do humans and other animals make the decision to explore new options instead of exploiting familiar favorites? Hogeveen et al. find evidence for similar computations underlying explore-exploit decisions across humans and monkeys. Additionally, their study reveals a brain-wide network comprising frontopolar, frontoparietal, frontostriatal, and mesocorticolimbic regions underlying explore-exploit decisions.</abstract><cop>United States</cop><pub>Elsevier Inc</pub><pmid>35390278</pmid><doi>10.1016/j.neuron.2022.03.014</doi><orcidid>https://orcid.org/0000-0003-0592-8556</orcidid><orcidid>https://orcid.org/0000-0001-9612-2085</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | amygdala Animals Choice Behavior - physiology computational modeling Decision Making - physiology decision-making exploration explore-exploit dilemma fMRI frontopolar cortex Prefrontal Cortex - diagnostic imaging Prefrontal Cortex - physiology reinforcement learning Reward striatum Ventral Striatum - diagnostic imaging Ventral Striatum - physiology |
title | The neurocomputational bases of explore-exploit decision-making |
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