Dlouhy Brian, Mowla Md Rakibul, Rhone Ariane, Kumar Sukhbinder, Kovach Christopher, Liu Junjie, Chan Aubrey, Kawasaki Hiroto, Mueller Rashmi, Kuhn Justin, Frede Ryan, Ciliberto Michael, Czech Theresa, Ganganna Sreenath, Owens James, Dabrowski Ania, Sprigg Brittany, Granner Mark, Simonyan Kristina, Nourski Kirill, Krause Bryan, Banks Matthew, Howard Matthew, Davenport Paul, Pattinson Kyle, Richerson George, Wemmie John
University of Iowa,Roy J and Lucille A Carver College of Medicine.
University of Iowa.
Res Sq. 2025 May 14:rs.3.rs-6568046. doi: 10.21203/rs.3.rs-6568046/v1.
The ability of the forebrain to track and integrate respiratory signals, a process known as breathing interoception, is critical for detecting respiratory threats and ensuring survival, yet its neural mechanisms remain largely unknown. Using human intracranial recordings, we identified widespread synchronization between forebrain neural oscillations and breathing rhythms across wakefulness, sleep, and external mechanical ventilation. During wakefulness, localized sites within known interoceptive regions such as insula, somatosensory cortex, anterior cingulate cortex, and amygdala robustly synchronized with breathing, highlighting their critical roles in breathing interoception. During sleep, forebrain synchronization shifted from cortex to amygdala and hippocampus, suggesting redistributed processing that may support vigilance and memory consolidation. In contrast to rodents, nasal airflow was not required for this synchronization, implicating multiple afferent pathways in respiratory interoception and possible unique evolutionary changes in humans. When breathing was driven by an external mechanical ventilator, the imposed breathing rhythm directly entrained forebrain activity, indicating a causal link. Notably, ventilator-driven slow, deep breathing entrained more forebrain sites, suggesting a potential mechanism through which breath-based practices might influence emotion and cognition. Together, these findings redefine breathing interoception as a pervasive influence within the forebrain, with implications for understanding disorders of respiratory awareness, emotional regulation, and cognitive health.
前脑追踪和整合呼吸信号的能力，即所谓的呼吸内感受过程，对于检测呼吸威胁和确保生存至关重要，但其神经机制仍 largely 未知。通过人类颅内记录，我们发现在清醒、睡眠和外部机械通气过程中，前脑神经振荡与呼吸节律之间存在广泛同步。在清醒状态下，已知内感受区域（如岛叶、体感皮层、前扣带回皮层和杏仁核）内的局部位点与呼吸强烈同步，突出了它们在呼吸内感受中的关键作用。在睡眠期间，前脑同步从皮层转移到杏仁核和海马体，表明处理过程重新分布，这可能支持警觉和记忆巩固。与啮齿动物不同，这种同步不需要鼻气流，这意味着呼吸内感受中有多种传入途径，以及人类可能存在独特的进化变化。当呼吸由外部机械通气驱动时，施加的呼吸节律直接带动前脑活动，表明存在因果联系。值得注意的是，通气机驱动的缓慢、深呼吸带动了更多前脑位点，提示基于呼吸的练习可能影响情绪和认知的潜在机制。总之，这些发现将呼吸内感受重新定义为在前脑内具有普遍影响，对理解呼吸意识障碍、情绪调节和认知健康具有重要意义。
