Herrero Jose L, Khuvis Simon, Yeagle Erin, Cerf Moran, Mehta Ashesh D
The Feinstein Institute for Medical Research, Manhasset, New York.
Department of Neurosurgery, Hofstra Northwell School of Medicine, Manhasset, New York.
J Neurophysiol. 2018 Jan 1;119(1):145-159. doi: 10.1152/jn.00551.2017. Epub 2017 Sep 27.
Whereas the neurophysiology of respiration has traditionally focused on automatic brain stem processes, higher brain mechanisms underlying the cognitive aspects of breathing are gaining increasing interest. Therapeutic techniques have used conscious control and awareness of breathing for millennia with little understanding of the mechanisms underlying their efficacy. Using direct intracranial recordings in humans, we correlated cortical and limbic neuronal activity as measured by the intracranial electroencephalogram (iEEG) with the breathing cycle. We show this to be the direct result of neuronal activity, as demonstrated by both the specificity of the finding to the cortical gray matter and the tracking of breath by the gamma-band (40-150 Hz) envelope in these structures. We extend prior observations by showing the iEEG signal to track the breathing cycle across a widespread network of cortical and limbic structures. We further demonstrate a sensitivity of this tracking to cognitive factors by using tasks adapted from cognitive behavioral therapy and meditative practice. Specifically, volitional control and awareness of breathing engage distinct but overlapping brain circuits. During volitionally paced breathing, iEEG-breath coherence increases in a frontotemporal-insular network, and during attention to breathing, we demonstrate increased coherence in the anterior cingulate, premotor, insular, and hippocampal cortices. Our findings suggest that breathing can act as an organizing hierarchical principle for neuronal oscillations throughout the brain and detail mechanisms of how cognitive factors impact otherwise automatic neuronal processes during interoceptive attention. NEW & NOTEWORTHY Whereas the link between breathing and brain activity has a long history of application to therapy, its neurophysiology remains unexplored. Using intracranial recordings in humans, we show neuronal activity to track the breathing cycle throughout widespread cortical/limbic sites. Volitional pacing of the breath engages frontotemporal-insular cortices, whereas attention to automatic breathing modulates the cingulate cortex. Our findings imply a fundamental role of breathing-related oscillations in driving neuronal activity and provide insight into the neuronal mechanisms of interoceptive attention.
传统上，呼吸的神经生理学主要关注脑干的自动过程，而呼吸认知方面的高级脑机制正越来越受到关注。数千年来，治疗技术一直使用对呼吸的有意识控制和感知，但对其疗效背后的机制了解甚少。通过对人类进行直接颅内记录，我们将颅内脑电图（iEEG）测量的皮质和边缘神经元活动与呼吸周期相关联。我们证明这是神经元活动的直接结果，这一发现对皮质灰质的特异性以及这些结构中伽马波段（40 - 150赫兹）包络对呼吸的追踪都证明了这一点。我们通过展示iEEG信号在广泛的皮质和边缘结构网络中追踪呼吸周期，扩展了先前的观察结果。我们还通过使用源自认知行为疗法和冥想练习的任务，进一步证明了这种追踪对认知因素的敏感性。具体而言，呼吸的意志控制和感知涉及不同但重叠的脑回路。在自主控制呼吸时，iEEG与呼吸的相干性在额颞 - 岛叶网络中增加，而在关注呼吸时，我们证明前扣带回、运动前区、岛叶和海马皮质的相干性增加。我们的研究结果表明，呼吸可以作为整个大脑神经元振荡的组织层次原则，并详细说明了认知因素在本体感受性注意期间如何影响原本自动的神经元过程。新发现与值得注意之处：尽管呼吸与脑活动之间的联系在治疗应用方面有着悠久的历史，但其神经生理学仍未得到探索。通过对人类进行颅内记录，我们显示神经元活动在广泛的皮质/边缘部位追踪呼吸周期。呼吸的自主控制涉及额颞 - 岛叶皮质，而对自动呼吸的关注则调节扣带回皮质。我们的研究结果暗示与呼吸相关的振荡在驱动神经元活动中具有基本作用，并为本体感受性注意的神经元机制提供了见解。
