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: 6.13). 03/2010; 51(4):1459-67. DOI: 10.1016/j.neuroimage.2010.03.036
Source: PubMed

ABSTRACT 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.

Download full-text


Available from: Oliver J Robinson, Jun 24, 2015
  • [Show abstract] [Hide abstract]
    ABSTRACT: This focussed narrative review examines neurobiological and psychophysiological evidence supporting a role for altered reward processes in the development and maintenance of anorexia nervosa (AN). In AN, there does not appear to be a generalised inability to experience reward. Rather, data suggest that a reluctance to gain weight leads to an aversive appraisal of food- and taste-related stimuli. As a result, cues compatible with this aberrant mode of thinking become rewarding for the individual. Evidence also suggests that attribution of motivational salience to such cues promotes anorectic behaviours. These findings are consistent with models in which interactions between cognition and reward are important in eliciting the anorectic "habit". A model is proposed which is consistent with elements of other theoretical frameworks, but differs in that its emphasis is towards neural overlaps between AN and addiction. It is consistent with AN being a reward-based learned behaviour in which aberrant cognitions related to eating and shape alter functioning of central reward systems. It proposes that the primary neural problem responsible for the development, maintenance, and treatment resistance is centred in the striatal reward system. This helps shift the emphasis of aetiological models towards reward processing, particularly in the context of illness-compatible cues. Furthermore, it suggests that continuing to explore the utility and valued nature of AN in the patient's life would be a useful inclusion in treatment and prevention models. Copyright © 2015. Published by Elsevier Ltd.
    Neuroscience & Biobehavioral Reviews 02/2015; 52. DOI:10.1016/j.neubiorev.2015.02.012 · 10.28 Impact Factor
  • [Show abstract] [Hide abstract]
    ABSTRACT: Feedback-related negativity (FRN) is an event-related brain potential (ERP) component elicited by errors and negative outcomes. Previous studies proposed that FRN reflects the activity of a general error-processing system that incorporates reward prediction error (RPE). However, other studies reported inconsistent results on this issue - namely, that FRN only reflects the valence of feedback and that the magnitude of RPE is reflected by the other ERP component called P300. The present study focused on the relationship between the FRN amplitude and RPE. ERPs were recorded during a reversal learning task performed by the participants, and a computational model was used to estimate trial-by-trial RPEs, which we correlated with the ERPs. The results indicated that FRN and P300 reflected the magnitude of RPE in negative outcomes and positive outcomes, respectively. In addition, the correlation between RPE and the P300 amplitude was stronger than the correlation between RPE and the FRN amplitude. These differences in the correlation between ERP and RPE components may explain the inconsistent results reported by previous studies; the asymmetry in the correlations might make it difficult to detect the effect of the RPE magnitude on the FRN and makes it appear that the FRN only reflects the valence of feedback.
    Neuroreport 02/2015; 26(3):157-62. DOI:10.1097/WNR.0000000000000318 · 1.64 Impact Factor
  • [Show abstract] [Hide abstract]
    ABSTRACT: A common assumption regarding error-based motor learning (motor adaptation) in humans is that its underlying mechanism is automatic and insensitive to reward- or punishment-based feedback. Contrary to this hypothesis, we show in a double dissociation that the two have independent effects on the learning and retention components of motor adaptation. Negative feedback, whether graded or binary, accelerated learning. While it was not necessary for the negative feedback to be coupled to monetary loss, it had to be clearly related to the actual performance on the preceding movement. Positive feedback did not speed up learning, but it increased retention of the motor memory when performance feedback was withdrawn. These findings reinforce the view that independent mechanisms underpin learning and retention in motor adaptation, reject the assumption that motor adaptation is independent of motivational feedback, and raise new questions regarding the neural basis of negative and positive motivational feedback in motor learning.
    Nature Neuroscience 02/2015; DOI:10.1038/nn.3956 · 14.98 Impact Factor