Prolonged dopamine signalling in striatum signals proximity and value of distant rewards

Predictions about future rewarding events have a powerful influence on behaviour. The phasic spike activity of dopamine-containing neurons, and corresponding dopamine transients in the striatum, are thought to underlie these predictions, encoding positive and negative reward prediction errors. Howev...

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Main Authors: Howe, Mark William, Sandberg, Stefan G., Phillips, Paul E. M., Graybiel, Ann M., Tierney, Patrick
Other Authors: Massachusetts Institute of Technology. Department of Brain and Cognitive Sciences
Format: Article
Language:en_US
Published: Nature Publishing Group 2014
Online Access:http://hdl.handle.net/1721.1/91049
https://orcid.org/0000-0003-2384-089X
https://orcid.org/0000-0002-4326-7720
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author Howe, Mark William
Sandberg, Stefan G.
Phillips, Paul E. M.
Graybiel, Ann M.
Tierney, Patrick
author2 Massachusetts Institute of Technology. Department of Brain and Cognitive Sciences
author_facet Massachusetts Institute of Technology. Department of Brain and Cognitive Sciences
Howe, Mark William
Sandberg, Stefan G.
Phillips, Paul E. M.
Graybiel, Ann M.
Tierney, Patrick
author_sort Howe, Mark William
collection MIT
description Predictions about future rewarding events have a powerful influence on behaviour. The phasic spike activity of dopamine-containing neurons, and corresponding dopamine transients in the striatum, are thought to underlie these predictions, encoding positive and negative reward prediction errors. However, many behaviours are directed towards distant goals, for which transient signals may fail to provide sustained drive. Here we report an extended mode of reward-predictive dopamine signalling in the striatum that emerged as rats moved towards distant goals. These dopamine signals, which were detected with fast-scan cyclic voltammetry (FSCV), gradually increased or—in rare instances—decreased as the animals navigated mazes to reach remote rewards, rather than having phasic or steady tonic profiles. These dopamine increases (ramps) scaled flexibly with both the distance and size of the rewards. During learning, these dopamine signals showed spatial preferences for goals in different locations and readily changed in magnitude to reflect changing values of the distant rewards. Such prolonged dopamine signalling could provide sustained motivational drive, a control mechanism that may be important for normal behaviour and that can be impaired in a range of neurologic and neuropsychiatric disorders.
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spelling mit-1721.1/910492022-10-01T09:27:59Z Prolonged dopamine signalling in striatum signals proximity and value of distant rewards Howe, Mark William Sandberg, Stefan G. Phillips, Paul E. M. Graybiel, Ann M. Tierney, Patrick Massachusetts Institute of Technology. Department of Brain and Cognitive Sciences McGovern Institute for Brain Research at MIT Howe, Mark William Tierney, Patrick Graybiel, Ann M. Predictions about future rewarding events have a powerful influence on behaviour. The phasic spike activity of dopamine-containing neurons, and corresponding dopamine transients in the striatum, are thought to underlie these predictions, encoding positive and negative reward prediction errors. However, many behaviours are directed towards distant goals, for which transient signals may fail to provide sustained drive. Here we report an extended mode of reward-predictive dopamine signalling in the striatum that emerged as rats moved towards distant goals. These dopamine signals, which were detected with fast-scan cyclic voltammetry (FSCV), gradually increased or—in rare instances—decreased as the animals navigated mazes to reach remote rewards, rather than having phasic or steady tonic profiles. These dopamine increases (ramps) scaled flexibly with both the distance and size of the rewards. During learning, these dopamine signals showed spatial preferences for goals in different locations and readily changed in magnitude to reflect changing values of the distant rewards. Such prolonged dopamine signalling could provide sustained motivational drive, a control mechanism that may be important for normal behaviour and that can be impaired in a range of neurologic and neuropsychiatric disorders. National Institutes of Health (U.S.) (Grant R01 MH060379) National Parkinson Foundation (U.S.) Cure Huntington’s Disease Initiative, Inc. (Grant A-5552) Stanley H. and Sheila G. Sydney Fund 2014-10-21T16:46:36Z 2014-10-21T16:46:36Z 2013-08 2013-01 Article http://purl.org/eprint/type/JournalArticle 0028-0836 1476-4687 http://hdl.handle.net/1721.1/91049 Howe, Mark W., Patrick L. Tierney, Stefan G. Sandberg, Paul E. M. Phillips, and Ann M. Graybiel. “Prolonged Dopamine Signalling in Striatum Signals Proximity and Value of Distant Rewards.” Nature 500, no. 7464 (August 4, 2013): 575–579. https://orcid.org/0000-0003-2384-089X https://orcid.org/0000-0002-4326-7720 en_US http://dx.doi.org/10.1038/nature12475 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 Nature Publishing Group PMC
spellingShingle Howe, Mark William
Sandberg, Stefan G.
Phillips, Paul E. M.
Graybiel, Ann M.
Tierney, Patrick
Prolonged dopamine signalling in striatum signals proximity and value of distant rewards
title Prolonged dopamine signalling in striatum signals proximity and value of distant rewards
title_full Prolonged dopamine signalling in striatum signals proximity and value of distant rewards
title_fullStr Prolonged dopamine signalling in striatum signals proximity and value of distant rewards
title_full_unstemmed Prolonged dopamine signalling in striatum signals proximity and value of distant rewards
title_short Prolonged dopamine signalling in striatum signals proximity and value of distant rewards
title_sort prolonged dopamine signalling in striatum signals proximity and value of distant rewards
url http://hdl.handle.net/1721.1/91049
https://orcid.org/0000-0003-2384-089X
https://orcid.org/0000-0002-4326-7720
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