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...

Full description

Bibliographic Details
Main Authors: Fouragnan, E, Queirazza, F, Retzler, C, Mullinger, KJ, Philiastides, MG
Format: Journal article
Language:English
Published: Springer Nature 2017
_version_ 1797083465220358144
author Fouragnan, E
Queirazza, F
Retzler, C
Mullinger, KJ
Philiastides, MG
author_facet Fouragnan, E
Queirazza, F
Retzler, C
Mullinger, KJ
Philiastides, MG
author_sort Fouragnan, E
collection OXFORD
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 2024-03-07T01:42:06Z
format Journal article
id oxford-uuid:973924b3-f9e4-4642-a428-b02f7b10321e
institution University of Oxford
language English
last_indexed 2024-03-07T01:42:06Z
publishDate 2017
publisher Springer Nature
record_format dspace
spelling oxford-uuid:973924b3-f9e4-4642-a428-b02f7b10321e2022-03-26T23:57:59ZSpatiotemporal neural characterization of prediction error valence and surprise during reward learning in humansJournal articlehttp://purl.org/coar/resource_type/c_dcae04bcuuid:973924b3-f9e4-4642-a428-b02f7b10321eEnglishSymplectic Elements at OxfordSpringer Nature2017Fouragnan, EQueirazza, FRetzler, CMullinger, KJPhiliastides, MGReward 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.
spellingShingle Fouragnan, E
Queirazza, F
Retzler, C
Mullinger, KJ
Philiastides, MG
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
work_keys_str_mv AT fouragnane spatiotemporalneuralcharacterizationofpredictionerrorvalenceandsurpriseduringrewardlearninginhumans
AT queirazzaf spatiotemporalneuralcharacterizationofpredictionerrorvalenceandsurpriseduringrewardlearninginhumans
AT retzlerc spatiotemporalneuralcharacterizationofpredictionerrorvalenceandsurpriseduringrewardlearninginhumans
AT mullingerkj spatiotemporalneuralcharacterizationofpredictionerrorvalenceandsurpriseduringrewardlearninginhumans
AT philiastidesmg spatiotemporalneuralcharacterizationofpredictionerrorvalenceandsurpriseduringrewardlearninginhumans