Advanced search
1 file | 960.34 KB Add to list

Unravelling the origin of the reward positivity : a human intracranial event-related brain potential study

Joyce Oerlemans (UGent) , Ricardo Alejandro Benavides (UGent) , Dirk Van Roost (UGent) , Paul Boon (UGent) , Veerle De Herdt (UGent) , Alfred Meurs (UGent) and Clay Holroyd (UGent)
(2025) BRAIN. 148(1). p.199-211
Author
Organization
Project
  • SEE-ACC (Cracking the Anterior Cingulate Cortex Code: Toward a Unified Theory of ACC Function)
Abstract
The reward positivity (RewP) is an event-related brain potential (ERP) component that emerges approximately 250 to 350 milliseconds (ms) after receiving reward-related feedback stimuli and is believed to be important for reinforcement learning and reward processing. Although numerous localization studies have indicated that the anterior cingulate cortex (ACC) is the neural generator of this component, other studies have identified sources outside of the ACC, fuelling a debate about its origin. Because the results of EEG and MEG source localization studies are severely limited by the inverse problem, we addressed this question by leveraging the high spatial and temporal resolution of intracranial EEG. We predicted that we would identify a neural generator of the RewP in the caudal ACC. We recorded intracranial EEG in 19 refractory epilepsy patients who underwent invasive video-EEG monitoring at Ghent University Hospital, Belgium. Participants engaged in the virtual T-maze task (vTMT), a trial-and-error task known to elicit a canonical RewP, while scalp and intracranial EEG were simultaneously recorded. The RewP was identified using a difference wave approach for both scalp and intracranial EEG. The data were aggregated across participants to create a virtual “meta-participant” that contained all the recorded intracranial ERPs (iERPs) with respect to their intracranial contact locations. We used both a hypothesis-driven (focused on ACC) and exploratory (whole-brain analysis) approach to segment the brain into regions of interest (ROI). For each ROI, we evaluated the degree to which the time course of the absolute current density (ACD) activity mirrored the time course of the RewP, and confirmed the statistical significance of the results using permutation analysis. The grand average waveform of the scalp data revealed a RewP at 309 ms after reward feedback with a frontocentral scalp distribution, consistent with the identification of this component as the RewP. The meta-participant contained iERPs recorded from 582 intracranial contacts in total. The ACD activity of the aggregated iERPs were most similar to the RewP in left caudal ACC, left dorsolateral prefrontal cortex, left frontomedial cortex, and left white matter, with the highest score attributed to caudal ACC, as predicted. To our knowledge, this is the first study that uses intracranial EEG aggregated across multiple human epilepsy patients and current source density analysis to identify the neural generator(s) of the RewP. These results provide direct evidence that the ACC is a neural generator of the RewP.
Keywords
reward positivity, anterior cingulate cortex, intracranial EEG, current density maps, FEEDBACK-RELATED NEGATIVITY, MEDIAL FRONTAL-CORTEX, CINGULATE CORTEX, INDIVIDUAL-DIFFERENCES, PREFRONTAL CORTEX, DECISION-MAKING, NEURAL REWARD, INFORMATION, SENSITIVITY, ACTIVATION

Downloads

  • (...).pdf
    • full text (Published version)
    • |
    • UGent only
    • |
    • PDF
    • |
    • 960.34 KB

Citation

Please use this url to cite or link to this publication:

MLA
Oerlemans, Joyce, et al. “Unravelling the Origin of the Reward Positivity : A Human Intracranial Event-Related Brain Potential Study.” BRAIN, vol. 148, no. 1, 2025, pp. 199–211, doi:10.1093/brain/awae259.
APA
Oerlemans, J., Alejandro Benavides, R., Van Roost, D., Boon, P., De Herdt, V., Meurs, A., & Holroyd, C. (2025). Unravelling the origin of the reward positivity : a human intracranial event-related brain potential study. BRAIN, 148(1), 199–211. https://doi.org/10.1093/brain/awae259
Chicago author-date
Oerlemans, Joyce, Ricardo Alejandro Benavides, Dirk Van Roost, Paul Boon, Veerle De Herdt, Alfred Meurs, and Clay Holroyd. 2025. “Unravelling the Origin of the Reward Positivity : A Human Intracranial Event-Related Brain Potential Study.” BRAIN 148 (1): 199–211. https://doi.org/10.1093/brain/awae259.
Chicago author-date (all authors)
Oerlemans, Joyce, Ricardo Alejandro Benavides, Dirk Van Roost, Paul Boon, Veerle De Herdt, Alfred Meurs, and Clay Holroyd. 2025. “Unravelling the Origin of the Reward Positivity : A Human Intracranial Event-Related Brain Potential Study.” BRAIN 148 (1): 199–211. doi:10.1093/brain/awae259.
Vancouver
1.
Oerlemans J, Alejandro Benavides R, Van Roost D, Boon P, De Herdt V, Meurs A, et al. Unravelling the origin of the reward positivity : a human intracranial event-related brain potential study. BRAIN. 2025;148(1):199–211.
IEEE
[1]
J. Oerlemans et al., “Unravelling the origin of the reward positivity : a human intracranial event-related brain potential study,” BRAIN, vol. 148, no. 1, pp. 199–211, 2025.
@article{01JA31VW1PB8YX56SSY6E45HCK,
  abstract     = {{The reward positivity (RewP) is an event-related brain potential (ERP) component that emerges approximately 250 to 350 milliseconds (ms) after receiving reward-related feedback stimuli and is believed to be important for reinforcement learning and reward processing. Although numerous localization studies have indicated that the anterior cingulate cortex (ACC) is the neural generator of this component, other studies have identified sources outside of the ACC, fuelling a debate about its origin. Because the results of EEG and MEG source localization studies are severely limited by the inverse problem, we addressed this question by leveraging the high spatial and temporal resolution of intracranial EEG. We predicted that we would identify a neural generator of the RewP in the caudal ACC.

We recorded intracranial EEG in 19 refractory epilepsy patients who underwent invasive video-EEG monitoring at Ghent University Hospital, Belgium. Participants engaged in the virtual T-maze task (vTMT), a trial-and-error task known to elicit a canonical RewP, while scalp and intracranial EEG were simultaneously recorded. The RewP was identified using a difference wave approach for both scalp and intracranial EEG. The data were aggregated across participants to create a virtual “meta-participant” that contained all the recorded intracranial ERPs (iERPs) with respect to their intracranial contact locations. We used both a hypothesis-driven (focused on ACC) and exploratory (whole-brain analysis) approach to segment the brain into regions of interest (ROI). For each ROI, we evaluated the degree to which the time course of the absolute current density (ACD) activity mirrored the time course of the RewP, and confirmed the statistical significance of the results using permutation analysis.

The grand average waveform of the scalp data revealed a RewP at 309 ms after reward feedback with a frontocentral scalp distribution, consistent with the identification of this component as the RewP. The meta-participant contained iERPs recorded from 582 intracranial contacts in total. The ACD activity of the aggregated iERPs were most similar to the RewP in left caudal ACC, left dorsolateral prefrontal cortex, left frontomedial cortex, and left white matter, with the highest score attributed to caudal ACC, as predicted.

To our knowledge, this is the first study that uses intracranial EEG aggregated across multiple human epilepsy patients and current source density analysis to identify the neural generator(s) of the RewP. These results provide direct evidence that the ACC is a neural generator of the RewP.}},
  author       = {{Oerlemans, Joyce and Alejandro Benavides, Ricardo and Van Roost, Dirk and Boon, Paul and De Herdt, Veerle and Meurs, Alfred and Holroyd, Clay}},
  issn         = {{0006-8950}},
  journal      = {{BRAIN}},
  keywords     = {{reward positivity,anterior cingulate cortex,intracranial EEG,current density maps,FEEDBACK-RELATED NEGATIVITY,MEDIAL FRONTAL-CORTEX,CINGULATE CORTEX,INDIVIDUAL-DIFFERENCES,PREFRONTAL CORTEX,DECISION-MAKING,NEURAL REWARD,INFORMATION,SENSITIVITY,ACTIVATION}},
  language     = {{eng}},
  number       = {{1}},
  pages        = {{199--211}},
  title        = {{Unravelling the origin of the reward positivity : a human intracranial event-related brain potential study}},
  url          = {{http://doi.org/10.1093/brain/awae259}},
  volume       = {{148}},
  year         = {{2025}},
}

Altmetric
View in Altmetric
Web of Science
Times cited: