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Non-invasive stimulation reveals ventromedial prefrontal cortex function in reward prediction and reward processing

INTRODUCTION: Studies suggest an involvement of the ventromedial prefrontal cortex (vmPFC) in reward prediction and processing, with reward-based learning relying on neural activity in response to unpredicted rewards or non-rewards (reward prediction error, RPE). Here, we investigated the causal rol...

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Autores principales: Rehbein, Maimu Alissa, Kroker, Thomas, Winker, Constantin, Ziehfreund, Lena, Reschke, Anna, Bölte, Jens, Wyczesany, Miroslaw, Roesmann, Kati, Wessing, Ida, Junghöfer, Markus
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10465130/
https://www.ncbi.nlm.nih.gov/pubmed/37650099
http://dx.doi.org/10.3389/fnins.2023.1219029
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author Rehbein, Maimu Alissa
Kroker, Thomas
Winker, Constantin
Ziehfreund, Lena
Reschke, Anna
Bölte, Jens
Wyczesany, Miroslaw
Roesmann, Kati
Wessing, Ida
Junghöfer, Markus
author_facet Rehbein, Maimu Alissa
Kroker, Thomas
Winker, Constantin
Ziehfreund, Lena
Reschke, Anna
Bölte, Jens
Wyczesany, Miroslaw
Roesmann, Kati
Wessing, Ida
Junghöfer, Markus
author_sort Rehbein, Maimu Alissa
collection PubMed
description INTRODUCTION: Studies suggest an involvement of the ventromedial prefrontal cortex (vmPFC) in reward prediction and processing, with reward-based learning relying on neural activity in response to unpredicted rewards or non-rewards (reward prediction error, RPE). Here, we investigated the causal role of the vmPFC in reward prediction, processing, and RPE signaling by transiently modulating vmPFC excitability using transcranial Direct Current Stimulation (tDCS). METHODS: Participants received excitatory or inhibitory tDCS of the vmPFC before completing a gambling task, in which cues signaled varying reward probabilities and symbols provided feedback on monetary gain or loss. We collected self-reported and evaluative data on reward prediction and processing. In addition, cue-locked and feedback-locked neural activity via magnetoencephalography (MEG) and pupil diameter using eye-tracking were recorded. RESULTS: Regarding reward prediction (cue-locked analysis), vmPFC excitation (versus inhibition) resulted in increased prefrontal activation preceding loss predictions, increased pupil dilations, and tentatively more optimistic reward predictions. Regarding reward processing (feedback-locked analysis), vmPFC excitation (versus inhibition) resulted in increased pleasantness, increased vmPFC activation, especially for unpredicted gains (i.e., gain RPEs), decreased perseveration in choice behavior after negative feedback, and increased pupil dilations. DISCUSSION: Our results support the pivotal role of the vmPFC in reward prediction and processing. Furthermore, they suggest that transient vmPFC excitation via tDCS induces a positive bias into the reward system that leads to enhanced anticipation and appraisal of positive outcomes and improves reward-based learning, as indicated by greater behavioral flexibility after losses and unpredicted outcomes, which can be seen as an improved reaction to the received feedback.
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spelling pubmed-104651302023-08-30 Non-invasive stimulation reveals ventromedial prefrontal cortex function in reward prediction and reward processing Rehbein, Maimu Alissa Kroker, Thomas Winker, Constantin Ziehfreund, Lena Reschke, Anna Bölte, Jens Wyczesany, Miroslaw Roesmann, Kati Wessing, Ida Junghöfer, Markus Front Neurosci Neuroscience INTRODUCTION: Studies suggest an involvement of the ventromedial prefrontal cortex (vmPFC) in reward prediction and processing, with reward-based learning relying on neural activity in response to unpredicted rewards or non-rewards (reward prediction error, RPE). Here, we investigated the causal role of the vmPFC in reward prediction, processing, and RPE signaling by transiently modulating vmPFC excitability using transcranial Direct Current Stimulation (tDCS). METHODS: Participants received excitatory or inhibitory tDCS of the vmPFC before completing a gambling task, in which cues signaled varying reward probabilities and symbols provided feedback on monetary gain or loss. We collected self-reported and evaluative data on reward prediction and processing. In addition, cue-locked and feedback-locked neural activity via magnetoencephalography (MEG) and pupil diameter using eye-tracking were recorded. RESULTS: Regarding reward prediction (cue-locked analysis), vmPFC excitation (versus inhibition) resulted in increased prefrontal activation preceding loss predictions, increased pupil dilations, and tentatively more optimistic reward predictions. Regarding reward processing (feedback-locked analysis), vmPFC excitation (versus inhibition) resulted in increased pleasantness, increased vmPFC activation, especially for unpredicted gains (i.e., gain RPEs), decreased perseveration in choice behavior after negative feedback, and increased pupil dilations. DISCUSSION: Our results support the pivotal role of the vmPFC in reward prediction and processing. Furthermore, they suggest that transient vmPFC excitation via tDCS induces a positive bias into the reward system that leads to enhanced anticipation and appraisal of positive outcomes and improves reward-based learning, as indicated by greater behavioral flexibility after losses and unpredicted outcomes, which can be seen as an improved reaction to the received feedback. Frontiers Media S.A. 2023-08-15 /pmc/articles/PMC10465130/ /pubmed/37650099 http://dx.doi.org/10.3389/fnins.2023.1219029 Text en Copyright © 2023 Rehbein, Kroker, Winker, Ziehfreund, Reschke, Bölte, Wyczesany, Roesmann, Wessing and Junghöfer. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Neuroscience
Rehbein, Maimu Alissa
Kroker, Thomas
Winker, Constantin
Ziehfreund, Lena
Reschke, Anna
Bölte, Jens
Wyczesany, Miroslaw
Roesmann, Kati
Wessing, Ida
Junghöfer, Markus
Non-invasive stimulation reveals ventromedial prefrontal cortex function in reward prediction and reward processing
title Non-invasive stimulation reveals ventromedial prefrontal cortex function in reward prediction and reward processing
title_full Non-invasive stimulation reveals ventromedial prefrontal cortex function in reward prediction and reward processing
title_fullStr Non-invasive stimulation reveals ventromedial prefrontal cortex function in reward prediction and reward processing
title_full_unstemmed Non-invasive stimulation reveals ventromedial prefrontal cortex function in reward prediction and reward processing
title_short Non-invasive stimulation reveals ventromedial prefrontal cortex function in reward prediction and reward processing
title_sort non-invasive stimulation reveals ventromedial prefrontal cortex function in reward prediction and reward processing
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10465130/
https://www.ncbi.nlm.nih.gov/pubmed/37650099
http://dx.doi.org/10.3389/fnins.2023.1219029
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