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The Journal of Neuroscience, September 9, 2009, 29(36):11330-11338; doi:10.1523/JNEUROSCI.1639-09.2009

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Behavioral/Systems/Cognitive
Differential Engagement of the Ventromedial Prefrontal Cortex by Goal-Directed and Habitual Behavior toward Food Pictures in Humans

Sanne de Wit,^1,2 Philip R. Corlett,^2,3 Mike R. Aitken,⁴ Anthony Dickinson,⁴ and Paul C. Fletcher²

¹Amsterdam Center for the Study of Adaptive Control in Brain and Behavior (Acacia), Department of Psychology, University of Amsterdam, 1018 WB Amsterdam, The Netherlands, ²Department of Psychiatry, University of Cambridge, Cambridge CB2 2QQ, United Kingdom, ³Department of Psychiatry, Connecticut Mental Health Center, Yale University, New Haven, Connecticut 06510, and ⁴Department of Experimental Psychology, University of Cambridge, Cambridge CB2 3EB, United Kingdom

Correspondence should be addressed to Sanne de Wit, Amsterdam Center for the Study of Adaptive Control in Brain and Behavior (Acacia), Department of Psychology, University of Amsterdam, Roeterstraat 15, 1018 WB Amsterdam, The Netherlands. Email: s.dewit{at}uva.nl

According to dual-system accounts, instrumental learning is supported by both a goal-directed and a habitual system. Although behavioral control by the goal-directed system, through outcome–action associations, dominates with moderate training, stimulus–response associations are thought to form concurrently in the habit system. It is therefore challenging to isolate the neural substrate of the goal-directed system in neuroimaging research with healthy human volunteers. Recently, however, de Wit et al. (2007) developed an instrumental discrimination task that distinguishes between goal-directed and habit-based responding. In this task, cues are congruent, unrelated, or incongruent with subsequent outcomes. Whereas performance on congruent and control trials can be supported by both the goal-directed and habitual system, performance on the incongruent discrimination relies solely on the habit system. In the present study, we used this task with healthy participants undergoing functional magnetic resonance imaging to demonstrate that engagement of the goal-directed system during learning is reflected in increased activity in the ventromedial prefrontal cortex. Moreover, using a subsequent outcome devaluation manipulation, we show that this area is involved in guiding decision making when goal values change, even in the absence of external cues to guide performance. We can therefore exclude a purely Pavlovian account of ventromedial prefrontal function and unequivocally demonstrate its involvement in the acquisition as well as deployment of goal-directed knowledge.

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Received April 6, 2009; revised July 7, 2009; accepted Aug. 3, 2009.

Correspondence should be addressed to Sanne de Wit, Amsterdam Center for the Study of Adaptive Control in Brain and Behavior (Acacia), Department of Psychology, University of Amsterdam, Roeterstraat 15, 1018 WB Amsterdam, The Netherlands. Email: s.dewit{at}uva.nl

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