Zeng Yimeng, Xiong Bingsen, Gao Hongyao, Liu Chao, Chen Changming, Wu Jianhui, Qin Shaozheng
School of Management, Beijing University of Chinese Medicine, Beijing 100029, China.
State Key Laboratory of Cognitive Neuroscience and Learning & International Data Group/McGovern Institute for Brain Research, Beijing Normal University, Beijing 100875, China.
Proc Natl Acad Sci U S A. 2024 Dec 24;121(52):e2405850121. doi: 10.1073/pnas.2405850121. Epub 2024 Dec 16.
Emotion and cognition involve an intricate crosstalk of neural and endocrine systems that support dynamic reallocation of neural resources and optimal adaptation for upcoming challenges, an active process analogous to allostasis. As a hallmark of human endocrine activity, the cortisol awakening response (CAR) is recognized to play a critical role in proactively modulating emotional and executive functions. Yet, the underlying mechanisms of such proactive effects remain elusive. By leveraging pharmacological neuroimaging and hidden Markov modeling of brain state dynamics, we show that the CAR proactively modulates rapid spatiotemporal reconfigurations (state) of large-scale brain networks involved in emotional and executive functions. Behaviorally, suppression of CAR proactively impaired performance of emotional discrimination but not working memory (WM), while individuals with higher CAR exhibited better performance for both emotional and WM tasks. Neuronally, suppression of CAR led to a decrease in fractional occupancy and mean lifetime of task-related brain states dominant to emotional and WM processing. Further information-theoretic analyses on sequence complexity of state transitions revealed that a suppressed or lower CAR led to higher transition complexity among states primarily anchored in visual-sensory and salience networks during emotional task. Conversely, an opposite pattern of transition complexity was observed among states anchored in executive control and visuospatial networks during WM, indicating that CAR distinctly modulates neural resources allocated to emotional and WM processing. Our findings establish a causal link of CAR with brain network dynamics across emotional and executive functions, suggesting a neuroendocrine account for CAR proactive effects on human emotion and cognition.
情绪和认知涉及神经和内分泌系统之间复杂的相互作用，这些系统支持神经资源的动态重新分配以及对即将到来的挑战的最佳适应，这是一个类似于动态平衡的积极过程。作为人类内分泌活动的一个标志，皮质醇觉醒反应（CAR）被认为在主动调节情绪和执行功能方面起着关键作用。然而，这种主动作用的潜在机制仍然难以捉摸。通过利用药理学神经影像学和脑状态动力学的隐马尔可夫模型，我们表明CAR主动调节参与情绪和执行功能的大规模脑网络的快速时空重构（状态）。在行为上，抑制CAR会主动损害情绪辨别能力，但不会损害工作记忆（WM），而CAR较高的个体在情绪和WM任务中表现更好。在神经元层面，抑制CAR会导致在情绪和WM处理中占主导地位的与任务相关的脑状态的分数占有率和平均寿命下降。对状态转换序列复杂性的进一步信息论分析表明，在情绪任务中，抑制或较低的CAR会导致主要锚定在视觉感觉和突显网络中的状态之间的转换复杂性增加。相反，在WM期间，在锚定在执行控制和视觉空间网络中的状态之间观察到相反的转换复杂性模式，这表明CAR对分配给情绪和WM处理的神经资源有明显的调节作用。我们的研究结果建立了CAR与跨情绪和执行功能的脑网络动力学之间的因果联系，为CAR对人类情绪和认知的主动作用提供了一种神经内分泌解释。
