Rodolphe Nenert , Christina Mueller , Corina Catiul , Jennifer Pilkington , Pierre LeVan , Ayushe Sharma , Jerzy P. Szaflarski , Amy W. Amara
{"title":"大脑生理脉动与老年人的睡眠结构和认知表现有关。","authors":"Rodolphe Nenert , Christina Mueller , Corina Catiul , Jennifer Pilkington , Pierre LeVan , Ayushe Sharma , Jerzy P. Szaflarski , Amy W. Amara","doi":"10.1016/j.neuroimage.2025.121187","DOIUrl":null,"url":null,"abstract":"<div><h3>Background</h3><div>The glymphatic system facilitates efficient waste clearance in the brain through the movement of cerebrospinal fluid (CSF) along perivascular spaces. Animal studies have demonstrated that glymphatic efficiency declines with age, but evidence for such decline in humans is limited. We hypothesized that reduced glymphatic efficiency in older adults may be related to age-related worsening of sleep quality, potentially contributing to cognitive impairment.</div></div><div><h3>Methods</h3><div>20 participants aged ≥60 years provided multi-dimensional cognitive measures, overnight polysomnography, and Magnetic Resonance Encephalography (MREG) performed the morning following the PSG. MREG is a single-shot, three-dimensional (3D) sequence employing a spherical stack-of-spirals trajectory that undersamples 3D k-space, enabling whole-brain data acquisition every 100 milliseconds to non-invasively and dynamically assess brain physiological pulsations. Spectral power and optical flow analyses quantified physiological pulsations within cardiovascular (CvB; 0.52–1.6 Hz), respiratory (RFB; 0.11–0.44 Hz), and low-frequency (LFB; 0.008–0.1 Hz) bands. These measures were correlated with cognitive test scores and sleep parameters assessed by overnight polysomnography.</div></div><div><h3>Results</h3><div>Significant associations emerged between physiological pulsations, sleep, and cognitive measures. Cardiovascular pulsation strength correlated with non-rapid eye movement (NREM) stage 3 (N3) sleep percentage (peak voxel in right frontal pole; <em>r</em> = 0.72, <em>p</em> < 0.001) and language domain performance (left calcarine gyrus; <em>r</em> = 0.56, <em>p</em> = 0.01). Respiratory pulsations correlated strongly with sleep onset latency (right inferior temporal gyrus; <em>r</em> = 0.75, <em>p</em> < 0.001). Additionally, low-frequency pulsations were associated with sleep onset latency (right precentral gyrus; <em>r</em> = 0.67, <em>p</em> = 0.002). These findings suggest that glymphatic efficiency, as reflected by brain pulsations, is closely linked to sleep quality and cognitive performance in older adults, particularly involving cortical and subcortical structures relevant to cognitive and sleep regulatory functions.</div></div><div><h3>Conclusion</h3><div>This study uniquely demonstrates that brain physiological pulsations measured non-invasively with MREG are significantly associated with sleep architecture and cognitive performance in older adults. These findings underscore the potential of MREG to assess glymphatic function and provide important insights into the mechanisms linking sleep disturbances, cognitive decline, and aging. The identified correlations between pulsations and specific brain regions highlight potential pathways through which impaired glymphatic function could contribute to cognitive decline in older adults, suggesting promising avenues for future clinical and research applications.</div></div>","PeriodicalId":19299,"journal":{"name":"NeuroImage","volume":"311 ","pages":"Article 121187"},"PeriodicalIF":4.7000,"publicationDate":"2025-04-03","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":"{\"title\":\"Brain physiological pulsations are linked to sleep architecture and cognitive performance in older adults\",\"authors\":\"Rodolphe Nenert , Christina Mueller , Corina Catiul , Jennifer Pilkington , Pierre LeVan , Ayushe Sharma , Jerzy P. Szaflarski , Amy W. Amara\",\"doi\":\"10.1016/j.neuroimage.2025.121187\",\"DOIUrl\":null,\"url\":null,\"abstract\":\"<div><h3>Background</h3><div>The glymphatic system facilitates efficient waste clearance in the brain through the movement of cerebrospinal fluid (CSF) along perivascular spaces. Animal studies have demonstrated that glymphatic efficiency declines with age, but evidence for such decline in humans is limited. We hypothesized that reduced glymphatic efficiency in older adults may be related to age-related worsening of sleep quality, potentially contributing to cognitive impairment.</div></div><div><h3>Methods</h3><div>20 participants aged ≥60 years provided multi-dimensional cognitive measures, overnight polysomnography, and Magnetic Resonance Encephalography (MREG) performed the morning following the PSG. MREG is a single-shot, three-dimensional (3D) sequence employing a spherical stack-of-spirals trajectory that undersamples 3D k-space, enabling whole-brain data acquisition every 100 milliseconds to non-invasively and dynamically assess brain physiological pulsations. Spectral power and optical flow analyses quantified physiological pulsations within cardiovascular (CvB; 0.52–1.6 Hz), respiratory (RFB; 0.11–0.44 Hz), and low-frequency (LFB; 0.008–0.1 Hz) bands. These measures were correlated with cognitive test scores and sleep parameters assessed by overnight polysomnography.</div></div><div><h3>Results</h3><div>Significant associations emerged between physiological pulsations, sleep, and cognitive measures. Cardiovascular pulsation strength correlated with non-rapid eye movement (NREM) stage 3 (N3) sleep percentage (peak voxel in right frontal pole; <em>r</em> = 0.72, <em>p</em> < 0.001) and language domain performance (left calcarine gyrus; <em>r</em> = 0.56, <em>p</em> = 0.01). Respiratory pulsations correlated strongly with sleep onset latency (right inferior temporal gyrus; <em>r</em> = 0.75, <em>p</em> < 0.001). Additionally, low-frequency pulsations were associated with sleep onset latency (right precentral gyrus; <em>r</em> = 0.67, <em>p</em> = 0.002). These findings suggest that glymphatic efficiency, as reflected by brain pulsations, is closely linked to sleep quality and cognitive performance in older adults, particularly involving cortical and subcortical structures relevant to cognitive and sleep regulatory functions.</div></div><div><h3>Conclusion</h3><div>This study uniquely demonstrates that brain physiological pulsations measured non-invasively with MREG are significantly associated with sleep architecture and cognitive performance in older adults. These findings underscore the potential of MREG to assess glymphatic function and provide important insights into the mechanisms linking sleep disturbances, cognitive decline, and aging. The identified correlations between pulsations and specific brain regions highlight potential pathways through which impaired glymphatic function could contribute to cognitive decline in older adults, suggesting promising avenues for future clinical and research applications.</div></div>\",\"PeriodicalId\":19299,\"journal\":{\"name\":\"NeuroImage\",\"volume\":\"311 \",\"pages\":\"Article 121187\"},\"PeriodicalIF\":4.7000,\"publicationDate\":\"2025-04-03\",\"publicationTypes\":\"Journal Article\",\"fieldsOfStudy\":null,\"isOpenAccess\":false,\"openAccessPdf\":\"\",\"citationCount\":\"0\",\"resultStr\":null,\"platform\":\"Semanticscholar\",\"paperid\":null,\"PeriodicalName\":\"NeuroImage\",\"FirstCategoryId\":\"3\",\"ListUrlMain\":\"https://www.sciencedirect.com/science/article/pii/S1053811925001892\",\"RegionNum\":2,\"RegionCategory\":\"医学\",\"ArticlePicture\":[],\"TitleCN\":null,\"AbstractTextCN\":null,\"PMCID\":null,\"EPubDate\":\"\",\"PubModel\":\"\",\"JCR\":\"Q1\",\"JCRName\":\"NEUROIMAGING\",\"Score\":null,\"Total\":0}","platform":"Semanticscholar","paperid":null,"PeriodicalName":"NeuroImage","FirstCategoryId":"3","ListUrlMain":"https://www.sciencedirect.com/science/article/pii/S1053811925001892","RegionNum":2,"RegionCategory":"医学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"NEUROIMAGING","Score":null,"Total":0}
Brain physiological pulsations are linked to sleep architecture and cognitive performance in older adults
Background
The glymphatic system facilitates efficient waste clearance in the brain through the movement of cerebrospinal fluid (CSF) along perivascular spaces. Animal studies have demonstrated that glymphatic efficiency declines with age, but evidence for such decline in humans is limited. We hypothesized that reduced glymphatic efficiency in older adults may be related to age-related worsening of sleep quality, potentially contributing to cognitive impairment.
Methods
20 participants aged ≥60 years provided multi-dimensional cognitive measures, overnight polysomnography, and Magnetic Resonance Encephalography (MREG) performed the morning following the PSG. MREG is a single-shot, three-dimensional (3D) sequence employing a spherical stack-of-spirals trajectory that undersamples 3D k-space, enabling whole-brain data acquisition every 100 milliseconds to non-invasively and dynamically assess brain physiological pulsations. Spectral power and optical flow analyses quantified physiological pulsations within cardiovascular (CvB; 0.52–1.6 Hz), respiratory (RFB; 0.11–0.44 Hz), and low-frequency (LFB; 0.008–0.1 Hz) bands. These measures were correlated with cognitive test scores and sleep parameters assessed by overnight polysomnography.
Results
Significant associations emerged between physiological pulsations, sleep, and cognitive measures. Cardiovascular pulsation strength correlated with non-rapid eye movement (NREM) stage 3 (N3) sleep percentage (peak voxel in right frontal pole; r = 0.72, p < 0.001) and language domain performance (left calcarine gyrus; r = 0.56, p = 0.01). Respiratory pulsations correlated strongly with sleep onset latency (right inferior temporal gyrus; r = 0.75, p < 0.001). Additionally, low-frequency pulsations were associated with sleep onset latency (right precentral gyrus; r = 0.67, p = 0.002). These findings suggest that glymphatic efficiency, as reflected by brain pulsations, is closely linked to sleep quality and cognitive performance in older adults, particularly involving cortical and subcortical structures relevant to cognitive and sleep regulatory functions.
Conclusion
This study uniquely demonstrates that brain physiological pulsations measured non-invasively with MREG are significantly associated with sleep architecture and cognitive performance in older adults. These findings underscore the potential of MREG to assess glymphatic function and provide important insights into the mechanisms linking sleep disturbances, cognitive decline, and aging. The identified correlations between pulsations and specific brain regions highlight potential pathways through which impaired glymphatic function could contribute to cognitive decline in older adults, suggesting promising avenues for future clinical and research applications.
期刊介绍:
NeuroImage, a Journal of Brain Function provides a vehicle for communicating important advances in acquiring, analyzing, and modelling neuroimaging data and in applying these techniques to the study of structure-function and brain-behavior relationships. Though the emphasis is on the macroscopic level of human brain organization, meso-and microscopic neuroimaging across all species will be considered if informative for understanding the aforementioned relationships.