Spatiotemporal neural characterization of prediction error valence and surprise during reward learning in humans
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...
| Main Authors: | , , , , |
|---|---|
| Format: | Article |
| Published: |
Nature Publishing Group
2017
|
| Subjects: | |
| Online Access: | https://eprints.nottingham.ac.uk/43507/ |
| _version_ | 1848796703542476800 |
|---|---|
| author | Fouragnan, Elsa Queirazza, Filippo Retzler, Chris Mullinger, Karen J. Philiastides, Marios G. |
| author_facet | Fouragnan, Elsa Queirazza, Filippo Retzler, Chris Mullinger, Karen J. Philiastides, Marios G. |
| author_sort | Fouragnan, Elsa |
| building | Nottingham Research Data Repository |
| collection | Online Access |
| description | 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. |
| first_indexed | 2025-11-14T19:52:12Z |
| format | Article |
| id | nottingham-43507 |
| institution | University of Nottingham Malaysia Campus |
| institution_category | Local University |
| last_indexed | 2025-11-14T19:52:12Z |
| publishDate | 2017 |
| publisher | Nature Publishing Group |
| recordtype | eprints |
| repository_type | Digital Repository |
| spelling | nottingham-435072020-05-04T18:54:36Z https://eprints.nottingham.ac.uk/43507/ 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. 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. Nature Publishing Group 2017-07-06 Article PeerReviewed Fouragnan, Elsa, Queirazza, Filippo, Retzler, Chris, Mullinger, Karen J. and Philiastides, Marios G. (2017) Spatiotemporal neural characterization of prediction error valence and surprise during reward learning in humans. Scientific Reports, 7 . 4762/1-4762/18. ISSN 2045-2322 Reward learning prediction error valence surprise EEG fMRI http://www.nature.com/articles/s41598-017-04507-w doi:10.1038/s41598-017-04507-w doi:10.1038/s41598-017-04507-w |
| spellingShingle | Reward learning prediction error valence surprise EEG fMRI Fouragnan, Elsa Queirazza, Filippo Retzler, Chris Mullinger, Karen J. Philiastides, Marios G. Spatiotemporal neural characterization of prediction error valence and surprise during reward learning in humans |
| title | Spatiotemporal neural characterization of prediction error valence and surprise during reward learning in humans |
| title_full | Spatiotemporal neural characterization of prediction error valence and surprise during reward learning in humans |
| title_fullStr | Spatiotemporal neural characterization of prediction error valence and surprise during reward learning in humans |
| title_full_unstemmed | Spatiotemporal neural characterization of prediction error valence and surprise during reward learning in humans |
| title_short | Spatiotemporal neural characterization of prediction error valence and surprise during reward learning in humans |
| title_sort | spatiotemporal neural characterization of prediction error valence and surprise during reward learning in humans |
| topic | Reward learning prediction error valence surprise EEG fMRI |
| url | https://eprints.nottingham.ac.uk/43507/ https://eprints.nottingham.ac.uk/43507/ https://eprints.nottingham.ac.uk/43507/ |