Dopamine neuron ensembles signal the content of sensory prediction errors
Dopamine neurons respond to errors in predicting value-neutral sensory information. These data, combined with causal evidence that dopamine transients support sensory-based associative learning, suggest that the dopamine system signals a multidimensional prediction error. Yet such complexity is not...
| Main Authors: | , , , , , |
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| Format: | Article |
| Language: | English |
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eLife Sciences Publications Ltd
2019-11-01
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| Series: | eLife |
| Subjects: | |
| Online Access: | https://elifesciences.org/articles/49315 |
| _version_ | 1811201357480198144 |
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| author | Thomas A Stalnaker James D Howard Yuji K Takahashi Samuel J Gershman Thorsten Kahnt Geoffrey Schoenbaum |
| author_facet | Thomas A Stalnaker James D Howard Yuji K Takahashi Samuel J Gershman Thorsten Kahnt Geoffrey Schoenbaum |
| author_sort | Thomas A Stalnaker |
| collection | DOAJ |
| description | Dopamine neurons respond to errors in predicting value-neutral sensory information. These data, combined with causal evidence that dopamine transients support sensory-based associative learning, suggest that the dopamine system signals a multidimensional prediction error. Yet such complexity is not evident in the activity of individual neurons or population averages. How then do downstream areas know what to learn in response to these signals? One possibility is that information about content is contained in the pattern of firing across many dopamine neurons. Consistent with this, here we show that the pattern of firing across a small group of dopamine neurons recorded in rats signals the identity of a mis-predicted sensory event. Further, this same information is reflected in the BOLD response elicited by sensory prediction errors in human midbrain. These data provide evidence that ensembles of dopamine neurons provide highly specific teaching signals, opening new possibilities for how this system might contribute to learning. |
| first_indexed | 2024-04-12T02:20:31Z |
| format | Article |
| id | doaj.art-d724c355d72b4277a79e3f6d0a6a63c0 |
| institution | Directory Open Access Journal |
| issn | 2050-084X |
| language | English |
| last_indexed | 2024-04-12T02:20:31Z |
| publishDate | 2019-11-01 |
| publisher | eLife Sciences Publications Ltd |
| record_format | Article |
| series | eLife |
| spelling | doaj.art-d724c355d72b4277a79e3f6d0a6a63c02022-12-22T03:52:08ZengeLife Sciences Publications LtdeLife2050-084X2019-11-01810.7554/eLife.49315Dopamine neuron ensembles signal the content of sensory prediction errorsThomas A Stalnaker0https://orcid.org/0000-0003-4402-5448James D Howard1https://orcid.org/0000-0002-9309-3773Yuji K Takahashi2Samuel J Gershman3https://orcid.org/0000-0002-6546-3298Thorsten Kahnt4https://orcid.org/0000-0002-3575-2670Geoffrey Schoenbaum5https://orcid.org/0000-0001-8180-0701Intramural Research Program, National Institute on Drug Abuse, National Institutes of Health, Baltimore, United StatesDepartment of Neurology, Feinberg School of Medicine, Northwestern University, Chicago, United StatesIntramural Research Program, National Institute on Drug Abuse, National Institutes of Health, Baltimore, United StatesDepartment of Psychology and Center for Brain Science, Harvard University, Cambridge, United StatesDepartment of Neurology, Feinberg School of Medicine, Northwestern University, Chicago, United States; Department of Psychiatry and Behavioral Sciences, Feinberg School of Medicine, Northwestern University, Chicago, United States; Department of Psychology, Weinberg College of Arts and Sciences, Northwestern University, Chicago, United StatesIntramural Research Program, National Institute on Drug Abuse, National Institutes of Health, Baltimore, United States; Department of Anatomy and Neurobiology, University of Maryland School of Medicine, Baltimore, United States; Department of Neuroscience, Johns Hopkins School of Medicine, Baltimore, United StatesDopamine neurons respond to errors in predicting value-neutral sensory information. These data, combined with causal evidence that dopamine transients support sensory-based associative learning, suggest that the dopamine system signals a multidimensional prediction error. Yet such complexity is not evident in the activity of individual neurons or population averages. How then do downstream areas know what to learn in response to these signals? One possibility is that information about content is contained in the pattern of firing across many dopamine neurons. Consistent with this, here we show that the pattern of firing across a small group of dopamine neurons recorded in rats signals the identity of a mis-predicted sensory event. Further, this same information is reflected in the BOLD response elicited by sensory prediction errors in human midbrain. These data provide evidence that ensembles of dopamine neurons provide highly specific teaching signals, opening new possibilities for how this system might contribute to learning.https://elifesciences.org/articles/49315dopamineprediction errorlearningrathuman |
| spellingShingle | Thomas A Stalnaker James D Howard Yuji K Takahashi Samuel J Gershman Thorsten Kahnt Geoffrey Schoenbaum Dopamine neuron ensembles signal the content of sensory prediction errors eLife dopamine prediction error learning rat human |
| title | Dopamine neuron ensembles signal the content of sensory prediction errors |
| title_full | Dopamine neuron ensembles signal the content of sensory prediction errors |
| title_fullStr | Dopamine neuron ensembles signal the content of sensory prediction errors |
| title_full_unstemmed | Dopamine neuron ensembles signal the content of sensory prediction errors |
| title_short | Dopamine neuron ensembles signal the content of sensory prediction errors |
| title_sort | dopamine neuron ensembles signal the content of sensory prediction errors |
| topic | dopamine prediction error learning rat human |
| url | https://elifesciences.org/articles/49315 |
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