Social feedback can selectively enhance learning in diverse domains. Relevant neurocognitive mechanisms have been studied mainly in healthy persons, yielding correlational findings. Neurodegenerative lesion models, coupled with multimodal brain measures, can complement standard approaches by revealing direct multidimensional correlates of the phenomenon. To this end, we assessed socially reinforced and non-socially reinforced learning in 40 healthy participants as well as persons with behavioral variant frontotemporal dementia (n = 21), Parkinson’s disease (n = 31), and Alzheimer’s disease (n = 20). These conditions are typified by predominant deficits in social cognition, feedback-based learning, and associative learning respectively, although all three domains may be partly compromised in the other conditions. We combined a validated behavioral task with ongoing electroencephalographic (EEG) signatures of implicit learning (medial frontal negativity) and offline magnetic resonance imaging (MRI) measures (voxel-based morphometry). In healthy participants, learning was facilitated by social feedback relative to non-social feedback. In comparison with controls, this effect was specifically impaired in behavioral variant frontotemporal dementia and Parkinson’s disease, while unspecific learning deficits (across social and non-social conditions) were observed in Alzheimer’s disease. EEG results showed increased medial frontal negativity in healthy controls during social feedback and learning. Such a modulation was selectively disrupted in behavioral variant frontotemporal dementia. Neuroanatomical results revealed extended temporo-parietal and fronto-limbic correlates of socially reinforced learning, with specific temporo-parietal associations in behavioral variant frontotemporal dementia, and predominantly fronto-limbic regions in Alzheimer’s disease. In contrast, non-socially reinforced learning was consistently linked to medial temporal/hippocampal regions. No associations with cortical volume were found in Parkinson’s disease. Results are consistent with core social deficits in behavioral variant frontotemporal dementia, subtle disruptions in ongoing feedback-mechanisms and social processes in Parkinson’s disease, and generalized learning alterations in Alzheimer’s disease. This multimodal approach highlights the impact of different neurodegenerative profiles on learning and social feedback. Our findings inform a promising theoretical and clinical agenda in the fields of social learning, socially-reinforced learning and neurodegeneration.

中文翻译：

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跨神经退行性疾病的人类社会强化学习的多模式机制

社会反馈可以选择性地增强不同领域的学习。相关的神经认知机制主要在健康人中进行了研究，得出了相关的发现。神经退行性病变模型与多模态大脑测量相结合，可以通过揭示该现象的直接多维相关性来补充标准方法。为此，我们评估了 40 名健康参与者以及行为变异型额颞叶痴呆 (n = 21)、帕金森病 (n = 31) 和阿尔茨海默病 (n = 20) 的社会强化和非社会强化学习。这些情况的典型特征分别是社会认知、基于反馈的学习和联想学习方面的主要缺陷，尽管所有三个领域都可能在其他情况下部分受损。我们将经过验证的行为任务与内隐学习（内侧额叶负性）和离线磁共振成像（MRI）测量（基于体素的形态测量）的持续脑电图（EEG）特征相结合。在健康的参与者中，相对于非社会反馈，社会反馈促进了学习。与对照组相比，这种效应在行为变异额颞叶痴呆和帕金森病中特别受损，而在阿尔茨海默病中观察到非特异性学习缺陷（跨越社会和非社会条件）。脑电图结果显示，在社会反馈和学习过程中，健康对照组的正面正面负性增加。这种调节在行为变异额颞叶痴呆中被选择性地破坏。神经解剖学结果揭示了社会强化学习的扩展的颞顶叶和额叶边缘相关性，在行为变异额颞叶痴呆中具有特定的颞顶叶关联，在阿尔茨海默病中主要是额叶边缘区域。相比之下，非社会强化学习始终与内侧颞叶/海马区域相关联。在帕金森病中未发现与皮质体积相关。结果与行为变异额颞叶痴呆的核心社会缺陷、帕金森病持续反馈机制和社会过程的微妙破坏以及阿尔茨海默病的普遍学习改变一致。这种多模式方法突出了不同神经退行性特征对学习和社会反馈的影响。