Induction of haemodynamic travelling waves by glial-related vasomotion in a rat model of neuroinflammation: implications for functional neuroimaging.

IF 9.7 1区医学 Q1 MEDICINE, RESEARCH & EXPERIMENTAL

EBioMedicine Pub Date : 2025-05-27 DOI:10.1016/j.ebiom.2025.105777

Mickaël Pereira, Marine Droguerre, Marco Valdebenito, Louis Vidal, Guillaume Marcy, Sarah Benkeder, Paul Marchal, Jean-Christophe Comte, Olivier Pascual, Luc Zimmer, Benjamin Vidal

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引用次数: 0

Abstract

Background: Cerebral haemodynamics are crucial for brain homoeostasis and serve as a key proxy for brain activity. Although this process involves coordinated interaction between vessels, neurons, and glial cells, its dysregulation in neuroinflammation is not well understood.

Methods: We used in vivo mesoscopic functional ultrasound imaging to monitor cerebral blood volume changes during neuroinflammation in male rats injected with lipopolysaccharide (LPS) in the visual cortex, under resting-state or visual stimulation, combined to advanced ex vivo techniques for glial cell reactivity analysis.

Findings: Cortical neuroinflammation induced large oscillatory haemodynamic travelling waves in the frequency band of vasomotion (∼0.1 Hz) in both anaesthetized and awake rats. Vasomotor waves travelled through large distances between adjacent penetrating vessels, spanning the entire cortex thickness, and even extending to subcortical areas. Moreover, vasomotion amplitude correlated with microglial morphology changes and was significantly reduced by astrocytic toxins, suggesting that both microglia and astrocytes are involved in the enhancement of vasomotion during neuroinflammation. Notably, functional connectivity was increased under this oscillatory state and functional hyperaemia was exacerbated.

Interpretation: These findings further reveal the spatiotemporal properties of cerebral vasomotion and suggest this is a major component of brain haemodynamics in pathological states. Moreover, reactive microglia and astrocytes are participating to increase vasomotion during neuroinflammation. For the field of functional neuroimaging, our results advocate for considering 0.1 Hz haemodynamic oscillations as an important complement to traditional measurements, particularly in neuroinflammatory conditions. Indeed, brain haemodynamics may provide insights not only into neuronal activity but also glial reactivity.

Funding: Supported by ANR ("LabCom-NI2D", "Labex Cortex") and Auvergne-Rhône-Alpes Region ("BI2D").

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神经炎症大鼠模型中神经胶质相关血管运动诱导血流动力学行波：对功能性神经影像学的影响。

背景：脑血流动力学对脑内平衡至关重要，是脑活动的重要指标。尽管这一过程涉及血管、神经元和神经胶质细胞之间的协调相互作用，但其在神经炎症中的失调尚不清楚。方法：采用体内介观功能超声成像技术监测雄性大鼠在静息状态或视觉刺激下，在视觉皮质注射脂多糖（LPS）后，神经炎症期间脑血容量的变化，并结合先进的离体神经胶质细胞反应性分析技术。结果：在麻醉和清醒的大鼠中，皮质神经炎症诱导血管舒缩频带（~ 0.1 Hz）的大振荡血流动力学行波。血管舒缩波在相邻穿透血管之间传播很远的距离，跨越整个皮层厚度，甚至延伸到皮层下区域。此外，血管舒缩幅度与小胶质细胞形态变化相关，星形胶质细胞毒素显著降低了血管舒缩幅度，表明小胶质细胞和星形胶质细胞都参与了神经炎症期间血管舒缩的增强。值得注意的是，在这种振荡状态下，功能连通性增加，功能性充血加剧。解释：这些发现进一步揭示了脑血管舒缩的时空特性，并表明这是病理状态下脑血流动力学的主要组成部分。此外，反应性小胶质细胞和星形胶质细胞参与增加神经炎症时的血管舒缩。对于功能性神经成像领域，我们的研究结果提倡考虑0.1 Hz血流动力学振荡作为传统测量的重要补充，特别是在神经炎症条件下。事实上，脑血流动力学不仅可以提供对神经元活动的见解，还可以提供对神经胶质反应的见解。资金：由ANR（“LabCom-NI2D”，“Labex Cortex”）和Auvergne-Rhône-Alpes区域（“BI2D”）支持。

本文章由计算机程序翻译，如有差异，请以英文原文为准。

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来源期刊

EBioMedicine Biochemistry, Genetics and Molecular Biology-General Biochemistry,Genetics and Molecular Biology

CiteScore

17.70

自引率

0.90%

发文量

579

审稿时长

5 weeks

期刊介绍： eBioMedicine is a comprehensive biomedical research journal that covers a wide range of studies that are relevant to human health. Our focus is on original research that explores the fundamental factors influencing human health and disease, including the discovery of new therapeutic targets and treatments, the identification of biomarkers and diagnostic tools, and the investigation and modification of disease pathways and mechanisms. We welcome studies from any biomedical discipline that contribute to our understanding of disease and aim to improve human health.