Dissociable responses to punishment in distinct striatal regions during reversal learning

Department of Psychiatry and Behavioural and Clinical Neuroscience Institute, University of Cambridge, Cambridge, Addenbrooke's Hospital, P. O. Box 189, Level E4, Hills Road, Cambridge, CB2 2QQ, UK.
NeuroImage (Impact Factor: 6.36). 03/2010; 51(4):1459-67. DOI: 10.1016/j.neuroimage.2010.03.036
Source: PubMed


Adaptive behavior depends on the ability to flexibly alter our choices in response to changes in reward and punishment contingencies. One brain region frequently implicated in such behavior is the striatum. However, this region is functionally diverse and there are a number of apparent inconsistencies across previous studies. For instance, how can significant BOLD responses in the ventral striatum during punishment-based reversal learning be reconciled with the frequently demonstrated role of the ventral striatum in reward processing? Here we attempt to address this question by separately examining BOLD responses during reversal learning driven by reward and during reversal learning driven by punishment. We demonstrate simultaneous valence-specific and valence-nonspecific signals in the striatum, with the posterior dorsal striatum responding only to unexpected reward, and the anterior ventral striatum responding to both unexpected punishment as well as unexpected reward. These data help to reconcile conflicting findings from previous studies by showing that distinct regions of the striatum exhibit dissociable responses to punishment during reversal learning.

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    • "Results further demonstrate that aversive prediction error-related activity was enhanced in the hippocampus, insula and ventral striatum (Fig. 2/B1). The involvement of both striatum and insula is consistent with previous studies, where they have repeatedly been implicated as the neural correlates of aversive prediction errors (Delgado et al., 2008a; Metereau and Dreher, 2013; Robinson et al., 2010; Schiller et al., 2008; Seymour et al., 2004, 2007; Spoormaker et al., 2011). The strongest enhancement of aversive prediction error-related activity, however, was found in the right hippocampus (Fig. 2/B1; Table 2). "
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    • "Previous studies on reinforcement learning have found distinct neural mechanisms for learning by reward and that by punishment [36], [37], [39], [73]. In particular, although several studies on reward and punishment reinforcement learning also used a reversal learning paradigm [37], [73], these studies focused on prediction error and the dopamine system in the striatum, which is very different from the way we analyzed the data. Similarly, although lesion studies have suggested that the ventromedial PFC was responsible for reversal learning [17], [74], especially that driven by negative feedback [35], these studies did not directly compare reversal learning by reward and punishment. "
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