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J Neurophysiol 101: 3284-3293, 2009. First published April 1, 2009; doi:10.1152/jn.90909.2008
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Segregated and Integrated Coding of Reward and Punishment in the Cingulate Cortex

Juri Fujiwara1, Philippe N. Tobler4, Masato Taira2,3, Toshio Iijima1 and Ken-Ichiro Tsutsui1

1Division of Systems Neuroscience, Tohoku University Graduate School of Life Sciences, Sendai; 2Advanced Research Institute for the Sciences and Humanities, Nihon University; 3Division of Applied System Neuroscience, Nihon University Graduate School of Medical Science, Tokyo, Japan; and 4Department of Physiology, Development and Neuroscience, University of Cambridge, Cambridge, United Kingdom

Submitted 8 January 2009; accepted in final form 29 March 2009

Reward and punishment have opposite affective value but are both processed by the cingulate cortex. However, it is unclear whether the positive and negative affective values of monetary reward and punishment are processed by separate or common subregions of the cingulate cortex. We performed a functional magnetic resonance imaging study using a free-choice task and compared cingulate activations for different levels of monetary gain and loss. Gain-specific activation (increasing activation for increasing gain, but no activation change in relation to loss) occurred mainly in the anterior part of the anterior cingulate and in the posterior cingulate cortex. Conversely, loss-specific activation (increasing activation for increasing loss, but no activation change in relation to gain) occurred between these areas, in the middle and posterior part of the anterior cingulate. Integrated coding of gain and loss (increasing activation throughout the full range, from biggest loss to biggest gain) occurred in the dorsal part of the anterior cingulate, at the border with the medial prefrontal cortex. Finally, unspecific activation increases to both gains and losses (increasing activation to increasing gains and increasing losses, possibly reflecting attention) occurred in dorsal and middle regions of the cingulate cortex. Together, these results suggest separate and common coding of monetary reward and punishment in distinct subregions of the cingulate cortex. Further meta-analysis suggested that the presently found reward- and punishment-specific areas overlapped with those processing positive and negative emotions, respectively.


Address for reprint requests and other correspondence: K.-I. Tsutsui, Division of Systems Neuroscience, Tohoku University Graduate School of Life Sciences, 2-1-1 Katahira, Aoba-ku, Sendai 980-8577, Japan (E-mail: tsutsui{at}m.tains.tohoku.ac.jp)







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