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

Fouragnan, Elsa; Queirazza, Filippo; Retzler, Chris; Mullinger, Karen J.; Philiastides, Marios G.

Authors

Elsa Fouragnan

Filippo Queirazza

Chris Retzler

Karen J. Mullinger karen.mullinger@nottingham.ac.uk

Marios G. Philiastides



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.

Journal Article Type Article
Journal Scientific Reports
Print ISSN 2045-2322
Electronic ISSN 2045-2322
Publisher Nature Publishing Group
Peer Reviewed Peer Reviewed
Volume 7
Article Number 4762
APA6 Citation Fouragnan, E., Queirazza, F., Retzler, C., Mullinger, K. J., & Philiastides, M. G. (in press). Spatiotemporal neural characterization of prediction error valence and surprise during reward learning in humans. Scientific Reports, 7, https://doi.org/10.1038/s41598-017-04507-w
DOI https://doi.org/10.1038/s41598-017-04507-w
Keywords Reward, learning, prediction error, valence, surprise, EEG, fMRI
Publisher URL http://www.nature.com/articles/s41598-017-04507-w
Copyright Statement Copyright information regarding this work can be found at the following address: http://creativecommons.org/licenses/by/4.0

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Copyright Statement
Copyright information regarding this work can be found at the following address: http://creativecommons.org/licenses/by/4.0





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