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The Journal of Neuroscience, November 18, 2009, 29(46):14617-14626; doi:10.1523/JNEUROSCI.2026-09.2009

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Behavioral/Systems/Cognitive
How Humans Integrate the Prospects of Pain and Reward during Choice

Deborah Talmi,¹ Peter Dayan,² Stefan J. Kiebel,¹ Chris D. Frith,^1,3 and Raymond J. Dolan¹

¹Wellcome Trust Centre for Neuroimaging, University College London (UCL), London WC1N 3BG, United Kingdom, ²The Gatsby Computational Neuroscience Unit, UCL, London WC1N 3AR, United Kingdom, and ³Center for Functionally Integrative Neuroscience, Aarhus University Hospital, DK-8000 Aarhus, Denmark

Correspondence should be addressed to Deborah Talmi at her present address: School of Psychological Sciences, University of Manchester, Manchester M13 9PL, UK. Email: deborah.talmi{at}manchester.ac.uk

The maxim "no pain, no gain" summarizes scenarios in which an action leading to reward also entails a cost. Although we know a substantial amount about how the brain represents pain and reward separately, we know little about how they are integrated during goal-directed behavior. Two theoretical models might account for the integration of reward and pain. An additive model specifies that the disutility of costs is summed linearly with the utility of benefits, whereas an interactive model suggests that cost and benefit utilities interact so that the sensitivity to benefits is attenuated as costs become increasingly aversive. Using a novel task that required integration of physical pain and monetary reward, we examined the mechanism underlying cost–benefit integration in humans. We provide evidence in support of an interactive model in behavioral choice. Using functional neuroimaging, we identify a neural signature for this interaction such that, when the consequences of actions embody a mixture of reward and pain, there is an attenuation of a predictive reward signal in both ventral anterior cingulate cortex and ventral striatum. We conclude that these regions subserve integration of action costs and benefits in humans, a finding that suggests a cross-species similarity in neural substrates that implement this function and illuminates mechanisms that underlie altered decision making under aversive conditions.

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Received April 28, 2009; revised Sept. 9, 2009; accepted Sept. 15, 2009.

Correspondence should be addressed to Deborah Talmi at her present address: School of Psychological Sciences, University of Manchester, Manchester M13 9PL, UK. Email: deborah.talmi{at}manchester.ac.uk

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