Spatiotemporal neural characterization of prediction error valence and surprise during reward learning in humans

Fouragnan, E., Queirazza, F., Retzler, C. , Mullinger, K. J. and Philiastides, M. G. (2017) Spatiotemporal neural characterization of prediction error valence and surprise during reward learning in humans. Scientific Reports, 7, 4762. (doi:10.1038/s41598-017-04507-w) (PMID:28684734) (PMCID:PMC5500565)

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Abstract

Reward learning depends on accurate reward associations with potential choices. These associations can be attained with reinforcement learning mechanisms using a reward prediction error (RPE) signal (the difference between actual and expected rewards) for updating future reward expectations. Despite an extensive body of literature on the influence of RPE on learning, little has been done to investigate the potentially separate contributions of RPE valence (positive or negative) and surprise (absolute degree of deviation from expectations). Here, we coupled single-trial electroencephalography with simultaneously acquired fMRI, during a probabilistic reversal-learning task, to offer evidence of temporally overlapping but largely distinct spatial representations of RPE valence and surprise. Electrophysiological variability in RPE valence correlated with activity in regions of the human reward network promoting approach or avoidance learning. Electrophysiological variability in RPE surprise correlated primarily with activity in regions of the human attentional network controlling the speed of learning. Crucially, despite the largely separate spatial extend of these representations our EEG-informed fMRI approach uniquely revealed a linear superposition of the two RPE components in a smaller network encompassing visuo-mnemonic and reward areas. Activity in this network was further predictive of stimulus value updating indicating a comparable contribution of both signals to reward learning.

Item Type:Articles
Status:Published
Refereed:Yes
Glasgow Author(s) Enlighten ID:Retzler, Mr Christopher and Queirazza, Dr Filippo and Fouragnan, Dr Elsa and Philiastides, Dr Marios
Authors: Fouragnan, E., Queirazza, F., Retzler, C., Mullinger, K. J., and Philiastides, M. G.
College/School:College of Medical Veterinary and Life Sciences > Institute of Health and Wellbeing > Mental Health and Wellbeing
College of Medical Veterinary and Life Sciences > Institute of Neuroscience and Psychology
Journal Name:Scientific Reports
Publisher:Nature Publishing Group
ISSN:2045-2322
ISSN (Online):2045-2322
Copyright Holders:Copyright © 2017 The Authors
First Published:First published in Scientific Reports 7:4762
Publisher Policy:Reproduced under a Creative Commons License

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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