Local and global consequences of reward-evoked striatal dopamine release
© 2020, The Author(s), under exclusive licence to Springer Nature Limited. The neurotransmitter dopamine is required for the reinforcement of actions by rewarding stimuli1. Neuroscientists have tried to define the functions of dopamine in concise conceptual terms2, but the practical implications of...
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| Format: | Article |
| Language: | English |
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Springer Science and Business Media LLC
2021
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| Online Access: | https://hdl.handle.net/1721.1/133022 |
| _version_ | 1826213825711439872 |
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| author | Li, Nan Jasanoff, Alan Pradip |
| author2 | Massachusetts Institute of Technology. Department of Biological Engineering |
| author_facet | Massachusetts Institute of Technology. Department of Biological Engineering Li, Nan Jasanoff, Alan Pradip |
| author_sort | Li, Nan |
| collection | MIT |
| description | © 2020, The Author(s), under exclusive licence to Springer Nature Limited. The neurotransmitter dopamine is required for the reinforcement of actions by rewarding stimuli1. Neuroscientists have tried to define the functions of dopamine in concise conceptual terms2, but the practical implications of dopamine release depend on its diverse brain-wide consequences. Although molecular and cellular effects of dopaminergic signalling have been extensively studied3, the effects of dopamine on larger-scale neural activity profiles are less well-understood. Here we combine dynamic dopamine-sensitive molecular imaging4 and functional magnetic resonance imaging to determine how striatal dopamine release shapes local and global responses to rewarding stimulation in rat brains. We find that dopamine consistently alters the duration, but not the magnitude, of stimulus responses across much of the striatum, via quantifiable postsynaptic effects that vary across subregions. Striatal dopamine release also potentiates a network of distal responses, which we delineate using neurochemically dependent functional connectivity analyses. Hot spots of dopaminergic drive notably include cortical regions that are associated with both limbic and motor function. Our results reveal distinct neuromodulatory actions of striatal dopamine that extend well beyond its sites of peak release, and that result in enhanced activation of remote neural populations necessary for the performance of motivated actions. Our findings also suggest brain-wide biomarkers of dopaminergic function and could provide a basis for the improved interpretation of neuroimaging results that are relevant to learning and addiction. |
| first_indexed | 2024-09-23T15:55:25Z |
| format | Article |
| id | mit-1721.1/133022 |
| institution | Massachusetts Institute of Technology |
| language | English |
| last_indexed | 2024-09-23T15:55:25Z |
| publishDate | 2021 |
| publisher | Springer Science and Business Media LLC |
| record_format | dspace |
| spelling | mit-1721.1/1330222022-10-02T05:04:17Z Local and global consequences of reward-evoked striatal dopamine release Li, Nan Jasanoff, Alan Pradip Massachusetts Institute of Technology. Department of Biological Engineering Massachusetts Institute of Technology. Department of Brain and Cognitive Sciences Massachusetts Institute of Technology. Department of Nuclear Science and Engineering © 2020, The Author(s), under exclusive licence to Springer Nature Limited. The neurotransmitter dopamine is required for the reinforcement of actions by rewarding stimuli1. Neuroscientists have tried to define the functions of dopamine in concise conceptual terms2, but the practical implications of dopamine release depend on its diverse brain-wide consequences. Although molecular and cellular effects of dopaminergic signalling have been extensively studied3, the effects of dopamine on larger-scale neural activity profiles are less well-understood. Here we combine dynamic dopamine-sensitive molecular imaging4 and functional magnetic resonance imaging to determine how striatal dopamine release shapes local and global responses to rewarding stimulation in rat brains. We find that dopamine consistently alters the duration, but not the magnitude, of stimulus responses across much of the striatum, via quantifiable postsynaptic effects that vary across subregions. Striatal dopamine release also potentiates a network of distal responses, which we delineate using neurochemically dependent functional connectivity analyses. Hot spots of dopaminergic drive notably include cortical regions that are associated with both limbic and motor function. Our results reveal distinct neuromodulatory actions of striatal dopamine that extend well beyond its sites of peak release, and that result in enhanced activation of remote neural populations necessary for the performance of motivated actions. Our findings also suggest brain-wide biomarkers of dopaminergic function and could provide a basis for the improved interpretation of neuroimaging results that are relevant to learning and addiction. NIH (Grants R01 DA038642 and U01 NS103470) 2021-10-18T14:46:26Z 2021-10-18T14:46:26Z 2020 2021-09-03T18:00:47Z Article http://purl.org/eprint/type/JournalArticle https://hdl.handle.net/1721.1/133022 Li, Nan and Jasanoff, Alan Pradip. 2020. "Local and global consequences of reward-evoked striatal dopamine release." Nature, 580 (7802). en 10.1038/S41586-020-2158-3 Nature Article is made available in accordance with the publisher's policy and may be subject to US copyright law. Please refer to the publisher's site for terms of use. application/pdf Springer Science and Business Media LLC PMC |
| spellingShingle | Li, Nan Jasanoff, Alan Pradip Local and global consequences of reward-evoked striatal dopamine release |
| title | Local and global consequences of reward-evoked striatal dopamine release |
| title_full | Local and global consequences of reward-evoked striatal dopamine release |
| title_fullStr | Local and global consequences of reward-evoked striatal dopamine release |
| title_full_unstemmed | Local and global consequences of reward-evoked striatal dopamine release |
| title_short | Local and global consequences of reward-evoked striatal dopamine release |
| title_sort | local and global consequences of reward evoked striatal dopamine release |
| url | https://hdl.handle.net/1721.1/133022 |
| work_keys_str_mv | AT linan localandglobalconsequencesofrewardevokedstriataldopaminerelease AT jasanoffalanpradip localandglobalconsequencesofrewardevokedstriataldopaminerelease |