Neural underpinning of a respiration-associated resting-state fMRI network.
Neural underpinning of a respiration-associated resting-state fMRI network.
复制标题
呼吸相关静息状态fMRI网络的神经基础。
DOI：
10.7554/elife.81555
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发表时间：
2022-10-20
期刊：
影响因子：
7.7
通讯作者：
Zhang N
中科院分区：
文献类型：
--
作者：
Tu W;Zhang N
在静息态 fMRI (rsfMRI) 扫描期间，呼吸会引起运动和 CO2 波动，这将导致 rsfMRI 信号中出现非神经伪影。同时，呼吸作为一个重要的生理过程，可以直接驱动大脑神经活动的变化，从而调节rsfMRI信号。尽管如此，呼吸与功能磁共振成像关系中的这种潜在神经成分在很大程度上尚未被探索。为了阐明这个问题，我们同时记录了大鼠的电生理学、rsfMRI 和呼吸信号。我们的数据表明，呼吸确实与神经活动变化相关，慢呼吸变化与前扣带皮层记录的电生理信号的伽马带功率之间的锁相关系证明了这一点。有趣的是，缓慢的呼吸变化也与特征性的 rsfMRI 网络有关，该网络由伽马带神经活动介导。此外，当全脑神经活动在等电状态下沉默时，这种与呼吸相关的大脑网络就会消失，而呼吸却得以维持，这进一步证实了神经活动在该网络中的必要作用。总而言之，这项研究确定了一个由神经活动支撑的与呼吸相关的大脑网络，它代表了呼吸-rsfMRI关系中的一个新组成部分，与呼吸相关的rsfMRI伪影不同。它为研究健康和患病条件下呼吸、神经活动和静息态大脑网络之间的相互作用开辟了一条新途径。当我们呼吸时，大脑在做什么？人类和其他有肺的动物依靠呼吸为细胞提供氧气来产生能量。大脑中的神经元通过复杂的血管系统提供氧气。当神经元活跃时，会消耗大量能量，需要稳定的富氧血液供应。事实上，血管与大脑神经元活动之间的关系是如此紧密，为了研究神经元活动，研究人员和临床医生经常使用一种称为功能磁共振成像 (fMRI) 的方法来分析大脑中含氧血液的流动。这种成像技术使科学家能够绘制出大脑不同部分在任何给定时间的活跃程度，而无需进行侵入性医疗程序。不幸的是，功能磁共振成像结果受到呼吸时发生的吸气和呼气周期的影响，即使是在人休息时也是如此。这是因为呼吸的速率和深度可能会发生变化，导致身体不可预测地移动以及大脑中二氧化碳水平的波动，这可能会导致与神经元活动不相关的功能磁共振成像信号的变化。这种误导性的测量被称为“伪影”。假设这些功能磁共振成像结果并不代表真实的大脑活动，这意味着人们对呼吸对大脑不同部位神经元活动的影响知之甚少。为了解决这个问题，Tu和Zhang对大鼠进行了功能磁共振成像，并将结果与呼吸深度和速率的测量结果以及电生理学相结合，这种方法使他们能够直接记录神经元的电特性。这使他们能够绘制出响应呼吸而变得活跃的神经元网络。结果表明，呼吸会产生特定的功能磁共振成像信号，该信号可以与二氧化碳水平波动和身体运动产生的伪影区分开来。该信号与使用电生理学测量的神经元活动和呼吸模式相关，当大脑中神经元的电活动受到抑制时，即使老鼠仍在呼吸，该信号也会消失。这表明呼吸对大脑活动的影响与之前描述的伪影无关。未来的研究可能会集中在大脑如何对呼吸做出反应或呼吸本身如何由大脑控制，所开发的方法使研究人员能够探索在呼吸时增加活动的大脑区域。这为研究专注于呼吸的治疗和练习的神经机制扫清了道路。
Respiration can induce motion and CO2 fluctuation during resting-state fMRI (rsfMRI) scans, which will lead to non-neural artifacts in the rsfMRI signal. In the meantime, as a crucial physiologic process, respiration can directly drive neural activity change in the brain, and may thereby modulate the rsfMRI signal. Nonetheless, this potential neural component in the respiration–fMRI relationship is largely unexplored. To elucidate this issue, here we simultaneously recorded the electrophysiology, rsfMRI, and respiration signals in rats. Our data show that respiration is indeed associated with neural activity changes, evidenced by a phase-locking relationship between slow respiration variations and the gamma-band power of the electrophysiological signal recorded in the anterior cingulate cortex. Intriguingly, slow respiration variations are also linked to a characteristic rsfMRI network, which is mediated by gamma-band neural activity. In addition, this respiration-related brain network disappears when brain-wide neural activity is silenced at an isoelectrical state, while the respiration is maintained, further confirming the necessary role of neural activity in this network. Taken together, this study identifies a respiration-related brain network underpinned by neural activity, which represents a novel component in the respiration–rsfMRI relationship that is distinct from respiration-related rsfMRI artifacts. It opens a new avenue for investigating the interactions between respiration, neural activity, and resting-state brain networks in both healthy and diseased conditions. What does the brain do when we breathe? Humans and other animals with lungs depend on breathing to supply their cells with oxygen for energy production. Neurons in the brain are supplied oxygen through an intricate system of blood vessels. When active, neurons consume a lot of energy and require a steady supply of oxygen-rich blood. In fact, this relationship between blood vessels and activity of neurons in the brain is so tightly linked that to study neuron activity researchers and clinicians often use an approach called functional magnetic resonance imaging (fMRI) to analyze the flow of oxygenated blood in the brain. This imaging technique allows scientists to map how active different parts of the brain are at any given time without the need for an invasive medical procedure. Unfortunately, fMRI results are affected by the cycles of inhalation and exhalation that take place while breathing, even when an individual is at rest. This is because the rate and depth of respiration can vary, resulting in the body moving unpredictably and in CO2 levels fluctuating in the brain, which can lead to changes in fMRI signals that do not correlate with neuron activity. Such misleading measurements are called ‘artifacts’. The assumption that these fMRI results do not represent real brain activity has meant that the effects of breathing on neuron activity in different parts of the brain is poorly understood. To solve this issue, Tu and Zhang performed fMRI on rats and combined the results with measurements of the depth and rate of respiration, and with electrophysiology, an approach that allowed them to directly record the electrical properties of neurons. This allowed them to map out the network of neurons that become active in response to breathing. The results show that breathing leads to a specific fMRI signal that can be distinguished from the artifacts introduced by fluctuating CO2 levels and body movements. The signal correlates with the activity of neurons measured using electrophysiology and with breathing patterns, and it disappears when the electrical activity of neurons in the brain is suppressed, even if the rats are still breathing. This suggests that breathing affects brain activity that is independent of the previously described artifacts. Future studies may focus on how the brain responds to breathing or how respiration itself is controlled by the brain, with the methods developed allowing researchers to explore regions of the brain that increase their activity while breathing. This clears the path towards investigating the neural mechanisms underlying therapies and exercises that focus on breathing.