Oerlemans Joyce, Alejandro Ricardo J, Van Roost Dirk, Boon Paul, De Herdt Veerle, Meurs Alfred, Holroyd Clay B
4BRAIN, Department of Head and Skin, Ghent University, 9000 Ghent, Belgium.
Department of Experimental Psychology, Ghent University, 9000 Ghent, Belgium.
Brain. 2025 Jan 7;148(1):199-211. doi: 10.1093/brain/awae259.
Reward positivity (RewP) is an event-related brain potential component that emerges ∼250-350 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 magnetoencephalography 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 rthe RewP in the caudal ACC. We recorded intracranial EEG in 19 patients with refractory epilepsy who underwent invasive video-EEG monitoring at Ghent University Hospital, Belgium. Participants engaged in the virtual T-maze task, a trial-and-error task known to elicit a canonical RewP, while scalp and intracranial EEG were recorded simultaneously. 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 event-related brain potentials with respect to their intracranial contact locations. We used both hypothesis-driven (focused on ACC) and exploratory (whole-brain analysis) approaches to segment the brain into regions of interest. For each region of interest, we evaluated the degree to which the time course of the absolute current density (ACD) activity mirrored the time course of the RewP, and we 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 intracranial event-related brain potentials recorded from 582 intracranial contacts in total. The ACD activity of the aggregated intracranial event-related brain potentials was most similar to the RewP in the 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 to use 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.
奖赏正性波（RewP）是一种与事件相关的脑电成分，在接收到与奖赏相关的反馈刺激后约250 - 350毫秒出现，被认为对强化学习和奖赏处理很重要。尽管众多定位研究表明前扣带回皮质（ACC）是该成分的神经发生器，但其他研究也在ACC之外发现了其来源，引发了关于其起源的争论。由于脑电图（EEG）和脑磁图（MEG）源定位研究的结果受到逆问题的严重限制，我们利用颅内EEG的高空间和时间分辨率来解决这个问题。我们预测会在尾侧ACC中识别出RewP的神经发生器。我们记录了19例难治性癫痫患者的颅内EEG，这些患者在比利时根特大学医院接受了侵入性视频EEG监测。参与者进行虚拟T型迷宫任务，这是一种已知能引发典型RewP的试错任务，同时记录头皮和颅内EEG。通过差异波方法识别头皮和颅内EEG的RewP。将参与者的数据汇总以创建一个虚拟的“元参与者”，其中包含所有记录的颅内事件相关脑电及其颅内接触位置。我们使用假设驱动（聚焦于ACC）和探索性（全脑分析）方法将大脑划分为感兴趣区域。对于每个感兴趣区域，我们评估绝对电流密度（ACD）活动的时间进程反映RewP时间进程的程度，并使用置换分析确认结果的统计学意义。头皮数据的总体平均波形显示，在奖赏反馈后309毫秒出现RewP，头皮分布为额中央，这与该成分被识别为RewP一致。元参与者总共包含从582个颅内接触点记录的颅内事件相关脑电。汇总的颅内事件相关脑电的ACD活动在左尾侧ACC、左背外侧前额叶皮质、左额内侧皮质和左白质中与RewP最为相似，如预测的那样，尾侧ACC得分最高。据我们所知，这是第一项使用跨多例人类癫痫患者汇总的颅内EEG和电流源密度分析来识别RewP神经发生器的研究。这些结果提供了直接证据，表明ACC是RewP的神经发生器。
