A new framework for cortico-striatal plasticity: behavioural theory meets In vitro data at the reinforcement-action interface
Operant learning requires that reinforcement signals interact with action representations at a suitable neural interface. Much evidence suggests that this occurs when phasic dopamine, acting as a reinforcement prediction error, gates plasticity at cortico-striatal synapses, and thereby changes the f...
| Main Authors: | , , , |
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| Format: | Article |
| Language: | English |
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Public Library of Science
2015
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| Online Access: | https://eprints.nottingham.ac.uk/53579/ |
| _version_ | 1848798960597073920 |
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| author | Dayan, Peter Gurney, Kevin N. Humphries, Mark D. Redgrave, Peter |
| author_facet | Dayan, Peter Gurney, Kevin N. Humphries, Mark D. Redgrave, Peter |
| author_sort | Dayan, Peter |
| building | Nottingham Research Data Repository |
| collection | Online Access |
| description | Operant learning requires that reinforcement signals interact with action representations at a suitable neural interface. Much evidence suggests that this occurs when phasic dopamine, acting as a reinforcement prediction error, gates plasticity at cortico-striatal synapses, and thereby changes the future likelihood of selecting the action(s) coded by striatal neurons. But this hypothesis faces serious challenges. First, cortico-striatal plasticity is inexplicably complex, depending on spike timing, dopamine level, and dopamine receptor type. Second, there is a credit assignment problem—action selection signals occur long before the consequent dopamine reinforcement signal. Third, the two types of striatal output neuron have apparently opposite effects on action selection. Whether these factors rule out the interface hypothesis and how they interact to produce reinforcement learning is unknown. We present a computational framework that addresses these challenges. We first predict the expected activity changes over an operant task for both types of action-coding striatal neuron, and show they co-operate to promote action selection in learning and compete to promote action suppression in extinction. Separately, we derive a complete model of dopamine and spike-timing dependent cortico-striatal plasticity from in vitro data. We then show this model produces the predicted activity changes necessary for learning and extinction in an operant task, a remarkable convergence of a bottom-up data-driven plasticity model with the top-down behavioural requirements of learning theory. Moreover, we show the complex dependencies of cortico-striatal plasticity are not only sufficient but necessary for learning and extinction. Validating the model, we show it can account for behavioural data describing extinction, renewal, and reacquisition, and replicate in vitro experimental data on cortico-striatal plasticity. By bridging the levels between the single synapse and behaviour, our model shows how striatum acts as the action-reinforcement interface. |
| first_indexed | 2025-11-14T20:28:04Z |
| format | Article |
| id | nottingham-53579 |
| institution | University of Nottingham Malaysia Campus |
| institution_category | Local University |
| language | English |
| last_indexed | 2025-11-14T20:28:04Z |
| publishDate | 2015 |
| publisher | Public Library of Science |
| recordtype | eprints |
| repository_type | Digital Repository |
| spelling | nottingham-535792018-08-31T10:21:41Z https://eprints.nottingham.ac.uk/53579/ A new framework for cortico-striatal plasticity: behavioural theory meets In vitro data at the reinforcement-action interface Dayan, Peter Gurney, Kevin N. Humphries, Mark D. Redgrave, Peter Operant learning requires that reinforcement signals interact with action representations at a suitable neural interface. Much evidence suggests that this occurs when phasic dopamine, acting as a reinforcement prediction error, gates plasticity at cortico-striatal synapses, and thereby changes the future likelihood of selecting the action(s) coded by striatal neurons. But this hypothesis faces serious challenges. First, cortico-striatal plasticity is inexplicably complex, depending on spike timing, dopamine level, and dopamine receptor type. Second, there is a credit assignment problem—action selection signals occur long before the consequent dopamine reinforcement signal. Third, the two types of striatal output neuron have apparently opposite effects on action selection. Whether these factors rule out the interface hypothesis and how they interact to produce reinforcement learning is unknown. We present a computational framework that addresses these challenges. We first predict the expected activity changes over an operant task for both types of action-coding striatal neuron, and show they co-operate to promote action selection in learning and compete to promote action suppression in extinction. Separately, we derive a complete model of dopamine and spike-timing dependent cortico-striatal plasticity from in vitro data. We then show this model produces the predicted activity changes necessary for learning and extinction in an operant task, a remarkable convergence of a bottom-up data-driven plasticity model with the top-down behavioural requirements of learning theory. Moreover, we show the complex dependencies of cortico-striatal plasticity are not only sufficient but necessary for learning and extinction. Validating the model, we show it can account for behavioural data describing extinction, renewal, and reacquisition, and replicate in vitro experimental data on cortico-striatal plasticity. By bridging the levels between the single synapse and behaviour, our model shows how striatum acts as the action-reinforcement interface. Public Library of Science 2015-01-06 Article PeerReviewed application/pdf en cc_by https://eprints.nottingham.ac.uk/53579/1/Gurney2015.pdf Dayan, Peter, Gurney, Kevin N., Humphries, Mark D. and Redgrave, Peter (2015) A new framework for cortico-striatal plasticity: behavioural theory meets In vitro data at the reinforcement-action interface. PLoS Biology, 13 (1). e1002034. ISSN 1545-7885 http://journals.plos.org/plosbiology/article?id=10.1371/journal.pbio.1002034 doi:10.1371/journal.pbio.1002034 doi:10.1371/journal.pbio.1002034 |
| spellingShingle | Dayan, Peter Gurney, Kevin N. Humphries, Mark D. Redgrave, Peter A new framework for cortico-striatal plasticity: behavioural theory meets In vitro data at the reinforcement-action interface |
| title | A new framework for cortico-striatal plasticity: behavioural theory meets In vitro data at the reinforcement-action interface |
| title_full | A new framework for cortico-striatal plasticity: behavioural theory meets In vitro data at the reinforcement-action interface |
| title_fullStr | A new framework for cortico-striatal plasticity: behavioural theory meets In vitro data at the reinforcement-action interface |
| title_full_unstemmed | A new framework for cortico-striatal plasticity: behavioural theory meets In vitro data at the reinforcement-action interface |
| title_short | A new framework for cortico-striatal plasticity: behavioural theory meets In vitro data at the reinforcement-action interface |
| title_sort | new framework for cortico-striatal plasticity: behavioural theory meets in vitro data at the reinforcement-action interface |
| url | https://eprints.nottingham.ac.uk/53579/ https://eprints.nottingham.ac.uk/53579/ https://eprints.nottingham.ac.uk/53579/ |