Expectancy-related changes in firing of dopamine neurons depend on orbitofrontal cortex

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Abstract
The orbitofrontal cortex (OFC) has been hypothesized to carry information regarding the value of expected rewards. Such information could be used for generating instructive error signals conveyed by dopamine neurons. Here the authors report that this is indeed the case. However, contrary to the simplest hypothesis, OFC lesions did not result in the loss of all value information. Instead, lesions caused the loss of value information derived from model-based representations. The orbitofrontal cortex has been hypothesized to carry information regarding the value of expected rewards. Such information is essential for associative learning, which relies on comparisons between expected and obtained reward for generating instructive error signals. These error signals are thought to be conveyed by dopamine neurons. To test whether orbitofrontal cortex contributes to these error signals, we recorded from dopamine neurons in orbitofrontal-lesioned rats performing a reward learning task. Lesions caused marked changes in dopaminergic error signaling. However, the effect of lesions was not consistent with a simple loss of information regarding expected value. Instead, without orbitofrontal input, dopaminergic error signals failed to reflect internal information about the impending response that distinguished externally similar states leading to differently valued future rewards. These results are consistent with current conceptualizations of orbitofrontal cortex as supporting model-based behavior and suggest an unexpected role for this information in dopaminergic error signaling.