Bailes Sydney M, Williams Stephanie D, Ashenagar Baarbod, Licata Joseph, Bosli Massinissa Y, Dormes Brandon J, Yun Hannah J, Zimmerman Dabriel, Moyers Alejandra Hernandez, Salat David H, Lewis Laura D
Department of Electrical Engineering and Computer Science, Massachusetts Institute of Technology, Cambridge, MA, USA.
Department of Biomedical Engineering, Boston University, Boston, MA, USA.
bioRxiv. 2025 Feb 24:2025.02.22.639649. doi: 10.1101/2025.02.22.639649.
Aging reduces the quality and quantity of sleep, and greater sleep loss over the lifespan is predictive of neurodegeneration and cognitive decline. One mechanism by which sleep loss could contribute to impaired brain health is through disruption of cerebrospinal fluid (CSF) circulation. CSF is the primary waste transport system of the brain, and in young adults, CSF waves are largest during NREM sleep. However, whether sleep-dependent brain fluid physiology changes in aging is not known, due to the technical challenges of performing neuroimaging studies during sleep. We collected simultaneous fast fMRI and EEG data to measure large-scale CSF flow in healthy young and older adults and tested whether there were age-related changes to CSF dynamics during nighttime sleep. We found that sleep-dependent CSF flow was reduced in older adults, and this reduction was linked to impaired frontal EEG delta power and global hemodynamic oscillations during sleep. To identify mechanisms underlying reduced CSF flow, we used sensory and vasoactive stimuli to drive CSF flow in daytime task experiments, and found that both neural and cerebrovascular physiological changes contributed to the disruption of CSF flow during sleep. Finally, we found that this reduction in CSF flow was associated with gray matter atrophy in aging. Together, these results demonstrate that the aging human brain has reduced CSF flow during sleep, and identifies underlying neurovascular mechanisms that contribute to this age-related decline, suggesting targets for future interventions.
衰老会降低睡眠的质量和时长,而一生中更多的睡眠缺失预示着神经退行性变和认知能力下降。睡眠缺失导致大脑健康受损的一种机制可能是通过破坏脑脊液(CSF)循环。脑脊液是大脑主要的废物运输系统,在年轻人中,脑脊液波动在非快速眼动睡眠期间最为显著。然而,由于在睡眠期间进行神经影像学研究存在技术挑战,目前尚不清楚与睡眠相关的脑液生理机能在衰老过程中是否会发生变化。我们同时收集了快速功能磁共振成像(fMRI)和脑电图(EEG)数据,以测量健康年轻人和老年人的大规模脑脊液流动情况,并测试夜间睡眠期间脑脊液动力学是否存在与年龄相关的变化。我们发现,老年人中依赖睡眠的脑脊液流动减少,这种减少与睡眠期间额叶脑电图δ波功率受损和整体血液动力学振荡有关。为了确定脑脊液流动减少的潜在机制,我们在白天的任务实验中使用感觉和血管活性刺激来驱动脑脊液流动,发现神经和脑血管生理变化都导致了睡眠期间脑脊液流动的破坏。最后,我们发现脑脊液流动的这种减少与衰老过程中的灰质萎缩有关。总之,这些结果表明,衰老的人类大脑在睡眠期间脑脊液流动减少,并确定了导致这种与年龄相关的下降的潜在神经血管机制,为未来的干预措施提供了靶点。