Neural Mechanisms of Feedback Processing and Regulation Recalibration During Neurofeedback Training

IF 3.5 2区 医学 Q1 NEUROIMAGING
Gustavo S. P. Pamplona, Jana Zweerings, Cindy S. Lor, Lindsay deErney, Erik Roecher, Arezoo Taebi, Lydia Hellrung, Kaoru Amano, Dustin Scheinost, Florian Krause, Monica D. Rosenberg, Silvio Ionta, Silvia Brem, Erno J. Hermans, Klaus Mathiak, Frank Scharnowski
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Abstract

The acquisition of new skills is facilitated by providing individuals with feedback that reflects their performance. This process creates a closed loop that involves feedback processing and regulation recalibration to promote effective training. Functional magnetic resonance imaging (fMRI)-based neurofeedback is unique in applying this principle by delivering direct feedback on the self-regulation of brain activity. Understanding how feedback-driven learning occurs requires examining how feedback is evaluated and how regulation adjusts in response to feedback signals. In this pre-registered mega-analysis, we re-analyzed data from eight intermittent fMRI neurofeedback studies (N = 153 individuals) to investigate brain regions where activity and connectivity are linked to feedback processing and regulation recalibration (i.e., regulation after feedback) during training. We harmonized feedback scores presented during training in these studies and computed their linear associations with brain activity and connectivity using parametric general linear model analyses. We observed that, during feedback processing, feedback scores were positively associated with (1) activity in the reward system, dorsal attention network, default mode network, and cerebellum; and with (2) reward system-related connectivity within the salience network. During regulation recalibration, no significant associations were observed between feedback scores and either activity or associative learning-related connectivity. Our results suggest that neurofeedback is processed in the reward system, supporting the theory that reinforcement learning shapes this form of brain training. In addition, the involvement of large-scale networks in feedback processing, continuously transitioning between evaluating external feedback and internally assessing the adopted cognitive state, suggests that higher-level processing is integral to neurofeedback learning, which usually occurs over a short time span. Our findings highlight the pivotal role of performance-related feedback as a driving force in learning, potentially extending beyond neurofeedback training to other feedback-based processes.

Abstract Image

反馈加工的神经机制与神经反馈训练中的调节再校准
通过向个人提供反映其表现的反馈,可以促进新技能的获得。这个过程创造了一个闭环,包括反馈处理和规则再校准,以促进有效的培训。基于功能磁共振成像(fMRI)的神经反馈在应用这一原理方面是独一无二的,它通过对大脑活动的自我调节提供直接反馈。理解反馈驱动的学习是如何发生的,需要研究反馈是如何被评估的,以及调节是如何响应反馈信号的。在这项预先注册的大型分析中,我们重新分析了8项间歇fMRI神经反馈研究(N = 153人)的数据,以调查训练期间与反馈处理和调节再校准(即反馈后的调节)相关的大脑区域的活动和连通性。在这些研究中,我们统一了训练期间的反馈分数,并使用参数化一般线性模型分析计算了它们与大脑活动和连通性的线性关联。我们观察到,在反馈处理过程中,反馈得分与(1)奖励系统、背侧注意网络、默认模式网络和小脑的活动呈正相关;(2)突出性网络内与奖励系统相关的连通性。在调节重新校准期间,没有观察到反馈分数与活动或联想学习相关连通性之间的显著关联。我们的研究结果表明,神经反馈是在奖励系统中处理的,这支持了强化学习形成这种大脑训练形式的理论。此外,大规模网络参与反馈加工,在评估外部反馈和内部评估所采用的认知状态之间不断转换,表明更高水平的加工是神经反馈学习的组成部分,通常发生在短时间内。我们的研究结果强调了与表现相关的反馈作为学习驱动力的关键作用,它有可能从神经反馈训练扩展到其他基于反馈的过程。
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来源期刊
Human Brain Mapping
Human Brain Mapping 医学-核医学
CiteScore
8.30
自引率
6.20%
发文量
401
审稿时长
3-6 weeks
期刊介绍: Human Brain Mapping publishes peer-reviewed basic, clinical, technical, and theoretical research in the interdisciplinary and rapidly expanding field of human brain mapping. The journal features research derived from non-invasive brain imaging modalities used to explore the spatial and temporal organization of the neural systems supporting human behavior. Imaging modalities of interest include positron emission tomography, event-related potentials, electro-and magnetoencephalography, magnetic resonance imaging, and single-photon emission tomography. Brain mapping research in both normal and clinical populations is encouraged. Article formats include Research Articles, Review Articles, Clinical Case Studies, and Technique, as well as Technological Developments, Theoretical Articles, and Synthetic Reviews. Technical advances, such as novel brain imaging methods, analyses for detecting or localizing neural activity, synergistic uses of multiple imaging modalities, and strategies for the design of behavioral paradigms and neural-systems modeling are of particular interest. The journal endorses the propagation of methodological standards and encourages database development in the field of human brain mapping.
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