Separate neural representations of prediction error valence and surprise: evidence from an fMRI meta‐analysis

Fouragnan, E., Retzler, C. and Philiastides, M. G. (2018) Separate neural representations of prediction error valence and surprise: evidence from an fMRI meta‐analysis. Human Brain Mapping, 39(7), pp. 2887-2906. (doi:10.1002/hbm.24047) (PMID:29575249)

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Abstract

Learning occurs when an outcome differs from expectations, generating a reward prediction error signal (RPE). The RPE signal has been hypothesized to simultaneously embody the valence of an outcome (better or worse than expected) and its surprise (how far from expectations). Nonetheless, growing evidence suggests that separate representations of the two RPE components exist in the human brain. Meta‐analyses provide an opportunity to test this hypothesis and directly probe the extent to which the valence and surprise of the error signal are encoded in separate or overlapping networks. We carried out several meta‐analyses on a large set of fMRI studies investigating the neural basis of RPE, locked at decision outcome. We identified two valence learning systems by pooling studies searching for differential neural activity in response to categorical positive‐versus‐negative outcomes. The first valence network (negative > positive) involved areas regulating alertness and switching behaviours such as the midcingulate cortex, the thalamus and the dorsolateral prefrontal cortex whereas the second valence network (positive > negative) encompassed regions of the human reward circuitry such as the ventral striatum and the ventromedial prefrontal cortex. We also found evidence of a largely distinct surprise‐encoding network including the anterior cingulate cortex, anterior insula and dorsal striatum. Together with recent animal and electrophysiological evidence this meta‐analysis points to a sequential and distributed encoding of different components of the RPE signal, with potentially distinct functional roles.

Item Type:Articles
Status:Published
Refereed:Yes
Glasgow Author(s) Enlighten ID:Philiastides, Dr Marios and Fouragnan, Dr Elsa and Retzler, Mr Christopher
Authors: Fouragnan, E., Retzler, C., and Philiastides, M. G.
College/School:College of Medical Veterinary and Life Sciences > Institute of Neuroscience and Psychology
Journal Name:Human Brain Mapping
Publisher:Wiley
ISSN:1065-9471
ISSN (Online):1097-0193
Published Online:25 March 2018
Copyright Holders:Copyright © 2018 Wiley Periodicals, Inc.
First Published:First published in Human Brain Mapping 39(7):2887-2906
Publisher Policy:Reproduced in accordance with the copyright policy of the publisher

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Project CodeAward NoProject NamePrincipal InvestigatorFunder's NameFunder RefLead Dept
653861Spatiotemporal characterization of value judgments and reward processing in the human brainMarios PhiliastidesBiotechnology and Biological Sciences Research Council (BBSRC)BB/J015393/2INP - CENTRE FOR COGNITIVE NEUROIMAGING
654411Neural correlates of learning and confidence during decision making and their utility in developing "intelligent technologies".Marios PhiliastidesEconomic and Social Research Council (ESRC)ES/L012995/1INP - CENTRE FOR COGNITIVE NEUROIMAGING