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The Journal of Neuroscience, September 24, 2008, 28(39):9619-9631; doi:10.1523/JNEUROSCI.0255-08.2008

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Behavioral/Systems/Cognitive
Tripartite Mechanism of Extinction Suggested by Dopamine Neuron Activity and Temporal Difference Model

Wei-Xing Pan,¹ Robert Schmidt,² Jeffery R. Wickens,^2,3 and Brian I. Hyland¹

Departments of ¹Physiology and ²Anatomy and Structural Biology, School of Medical Sciences, University of Otago, Dunedin 9054, New Zealand, and ³Okinawa Institute of Science and Technology, Okinawa 904-2234, Japan

Correspondence should be addressed to Brian I. Hyland, Department of Physiology, School of Medical Sciences, University of Otago, Dunedin 9054, New Zealand. Email: brian.hyland{at}otago.ac.nz

Extinction of behavior enables adaptation to a changing world and is crucial for recovery from disorders such as phobias and drug addiction. However, the brain mechanisms underlying behavioral extinction remain poorly understood. Midbrain dopamine (DA) neurons appear to play a central role in most acquisition processes of appetitive conditioning. Here, we show that the responses of putative DA neurons to conditioned reward predicting cues also dynamically encode two classical features of extinction: decrement in amplitude of previously learned excitatory responses and rebound of responding on subsequent retesting (spontaneous recovery). Crucially, this encoding involves development of inhibitory responses in the DA neurons, reflecting new, extinction-specific learning in the brain. We explored the implications of this finding by adding such inhibitory inputs to a standard temporal difference model of DA cell activity. We found that combining extinction-triggered plasticity of these inputs with a time-dependent spontaneous decay of weights, equivalent to a forgetting process as described in classical behavioral extinction literature, enabled the model to simulate several classical features of extinction. A key requirement to achieving spontaneous recovery was differential rates of spontaneous decay for weights representing original conditioning and for subsequent extinction learning. A testable prediction of the model is thus that differential decay properties exist within the wider circuits regulating DA cell activity. These findings are consistent with the hypothesis that extinction processes at both cellular and behavioral levels involve a dynamic interaction between new (inhibitory) learning, forgetting, and unlearning.

Key words: dopaminergic neuron; extinction; classical conditioning; extracellular recording; temporal difference model; reward learning

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Received Jan. 18, 2008; revised Aug. 14, 2008; accepted Aug. 18, 2008.

Correspondence should be addressed to Brian I. Hyland, Department of Physiology, School of Medical Sciences, University of Otago, Dunedin 9054, New Zealand. Email: brian.hyland{at}otago.ac.nz

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