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The Journal of Neuroscience, April 11, 2007, 27(15):4019-4026; doi:10.1523/JNEUROSCI.0564-07.2007

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Behavioral/Systems/Cognitive
Determining the Neural Substrates of Goal-Directed Learning in the Human Brain

Vivian V. Valentin,^1,2 Anthony Dickinson,³ and John P. O'Doherty^1,2

¹Division of Humanities and Social Sciences and ²Computation and Neural Systems Program, California Institute of Technology, Pasadena, California 91125, and ³Department of Experimental Psychology, University of Cambridge, Cambridge CB2 3EB, United Kingdom

Correspondence should be addressed to John P. O'Doherty, Division of Humanities and Social Sciences, California Institute of Technology, 1200 East California Boulevard, Mail Code 228-77, Pasadena, CA 91125. Email: jdoherty{at}hss.caltech.edu

Instrumental conditioning is considered to involve at least two distinct learning systems: a goal-directed system that learns associations between responses and the incentive value of outcomes, and a habit system that learns associations between stimuli and responses without any link to the outcome that that response engendered. Lesion studies in rodents suggest that these two distinct components of instrumental conditioning may be mediated by anatomically distinct neural systems. The aim of the present study was to determine the neural substrates of the goal-directed component of instrumental learning in humans. Nineteen human subjects were scanned with functional magnetic resonance imaging while they learned to choose instrumental actions that were associated with the subsequent delivery of different food rewards (tomato juice, chocolate milk, and orange juice). After training, one of these foods was devalued by feeding the subject to satiety on that food. The subjects were then scanned again, while being re-exposed to the instrumental choice procedure (in extinction). We hypothesized that regions of the brain involved in goal-directed learning would show changes in their activity as a function of outcome devaluation. Our results indicate that neural activity in one brain region in particular, the orbitofrontal cortex, showed a strong modulation in its activity during selection of a devalued compared with a nondevalued action. These results suggest an important contribution of orbitofrontal cortex in guiding goal-directed instrumental choices in humans.

Key words: decision making; habit learning; instrumental conditioning; orbitofrontal cortex; outcome devaluation; reinforcement learning; fMRI; reward

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Received Nov. 21, 2006; revised March 5, 2007; accepted March 6, 2007.

Correspondence should be addressed to John P. O'Doherty, Division of Humanities and Social Sciences, California Institute of Technology, 1200 East California Boulevard, Mail Code 228-77, Pasadena, CA 91125. Email: jdoherty{at}hss.caltech.edu

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