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A new framework for cortico-striatal plasticity: behavioural theory meets In vitro data at the reinforcement-action interface

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 Thumbnail


Authors

Kevin N. Gurney

MARK HUMPHRIES Mark.Humphries@nottingham.ac.uk
Professor of Computational Neuroscience

Peter Redgrave



Abstract

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.

Citation

Gurney, K. N., Humphries, M. D., & Redgrave, P. (2015). A new framework for cortico-striatal plasticity: behavioural theory meets In vitro data at the reinforcement-action interface. PLoS Biology, 13(1), Article e1002034. https://doi.org/10.1371/journal.pbio.1002034

Journal Article Type Article
Acceptance Date Nov 20, 2014
Online Publication Date Jan 6, 2015
Publication Date Jan 6, 2015
Deposit Date Aug 6, 2018
Publicly Available Date Aug 6, 2018
Journal PLoS Biology
Print ISSN 1544-9173
Electronic ISSN 1545-7885
Publisher Public Library of Science
Peer Reviewed Peer Reviewed
Volume 13
Issue 1
Article Number e1002034
DOI https://doi.org/10.1371/journal.pbio.1002034
Public URL https://nottingham-repository.worktribe.com/output/952471
Publisher URL http://journals.plos.org/plosbiology/article?id=10.1371/journal.pbio.1002034
Contract Date Aug 6, 2018

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