Dataset Information

Cerebral functional networks during sleep in young and older individuals.

ABSTRACT: Even though sleep modification is a hallmark of the aging process, age-related changes in functional connectivity using functional Magnetic Resonance Imaging (fMRI) during sleep, remain unknown. Here, we combined electroencephalography and fMRI to examine functional connectivity differences between wakefulness and light sleep stages (N1 and N2 stages) in 16 young (23.1?±?3.3y; 7 women), and 14 older individuals (59.6?±?5.7y; 8 women). Results revealed extended, distributed (inter-between) and local (intra-within) decreases in network connectivity during sleep both in young and older individuals. However, compared to the young participants, older individuals showed lower decreases in connectivity or even increases in connectivity between thalamus/basal ganglia and several cerebral regions as well as between frontal regions of various networks. These findings reflect a reduced ability of the older brain to disconnect during sleep that may impede optimal disengagement for loss of responsiveness, enhanced lighter and fragmented sleep, and contribute to age effects on sleep-dependent brain plasticity.

SUBMITTER: Daneault V

PROVIDER: S-EPMC7921592 | biostudies-literature | 2021 Mar

REPOSITORIES: biostudies-literature

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Cerebral functional networks during sleep in young and older individuals.

Daneault Véronique V Orban Pierre P Martin Nicolas N Dansereau Christian C Godbout Jonathan J Pouliot Philippe P Dickinson Philip P Gosselin Nadia N Vandewalle Gilles G Maquet Pierre P Lina Jean-Marc JM Doyon Julien J Bellec Pierre P Carrier Julie J

Scientific reports 20210301 1

Even though sleep modification is a hallmark of the aging process, age-related changes in functional connectivity using functional Magnetic Resonance Imaging (fMRI) during sleep, remain unknown. Here, we combined electroencephalography and fMRI to examine functional connectivity differences between wakefulness and light sleep stages (N1 and N2 stages) in 16 young (23.1 ± 3.3y; 7 women), and 14 older individuals (59.6 ± 5.7y; 8 women). Results revealed extended, distributed (inter-between) and lo ...[more]

PMID: 33649377

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Project description:BackgroundGeneral anesthesia (GA) provides an invaluable experimental tool to understand the essential neural mechanisms underlying consciousness. Previous neuroimaging studies have shown the functional integration and segregation of brain functional networks during anesthetic-induced alteration of consciousness. However, the organization pattern of hubs in functional brain networks remains unclear. Moreover, comparisons with the well-characterized physiological unconsciousness can help us understand the neural mechanisms of anesthetic-induced unconsciousness.MethodsResting-state functional magnetic resonance imaging was performed during wakefulness, mild propofol-induced sedation (m-PIS), and deep PIS (d-PIS) with clinical unconsciousness on 8 healthy volunteers and wakefulness and natural sleep on 9 age- and sex-matched healthy volunteers. Large-scale functional brain networks of each volunteer were constructed based on 160 regions of interest. Then, rich-club organizations in brain functional networks and nodal properties (nodal strength and efficiency) were assessed and analyzed among the different states and groups.ResultsRich-clubs in the functional brain networks were reorganized during alteration of consciousness induced by propofol. Firstly, rich-club nodes were switched from the posterior cingulate cortex (PCC), angular gyrus, and anterior and middle insula to the inferior parietal lobule (IPL), inferior parietal sulcus (IPS), and cerebellum. When sedation was deepened to unconsciousness, the rich-club nodes were switched to the occipital and angular gyrus. These results suggest that the rich-club nodes were switched among the high-order cognitive function networks (default mode network [DMN] and fronto-parietal network [FPN]), sensory networks (occipital network [ON]), and cerebellum network (CN) from consciousness (wakefulness) to propofol-induced unconsciousness. At the same time, compared with wakefulness, local connections were switched to rich-club connections during propofol-induced unconsciousness, suggesting a strengthening of the overall information commutation of networks. Nodal efficiency of the anterior and middle insula and ventral frontal cortex was significantly decreased. Additionally, from wakefulness to natural sleep, a similar pattern of rich-club reorganization with propofol-induced unconsciousness was observed: rich-club nodes were switched from the DMN (including precuneus and PCC) to the sensorimotor network (SMN, including part of the frontal and temporal gyrus). Compared with natural sleep, nodal efficiency of the insula, frontal gyrus, PCC, and cerebellum significantly decreased during propofol-induced unconsciousness.ConclusionsOur study demonstrated that the rich-club reorganization in functional brain networks is characterized by switching of rich-club nodes between the high-order cognitive and sensory and motor networks during propofol-induced alteration of consciousness and natural sleep. These findings will help understand the common neurological mechanism of pharmacological and physiological unconsciousness.

Project description:Memory formation is a dynamic process that comprises different phases, such as encoding, consolidation and retrieval. It could be altered by several factors such as sleep quality, anxiety, and depression levels. In the last years, due to COVID-19 pandemic, there was a reduction in sleep quality, an increase in anxiety and depressive symptoms as well as an impairment in emotional episodic memory encoding, especially in young adults. Taking into account the profound impact of sleep quality in daily life a series of rules has been developed that are conducive to consistently achieving good sleep, known as sleep hygiene education. These interventions have been shown to be effective in improving sleep quality and duration and reducing depressive and anxiety symptoms. Here we propose the implementation of a brief sleep hygiene education to improve sleep quality and memory performance as well as to diminish anxiety and depressive scores. For that, participants were divided into two groups: Sleep hygiene education and control group. After that, they were evaluated for anxiety, depression, and sleep quality levels and trained on an episodic memory task. They were tested immediately after (short-term test) and also 1 week later (long-term test). This procedure was also performed before the sleep hygiene education and was taken as baseline level. We found that episodic memory performance for young adults improved for the SHE group after intervention but not for older adults, and no improvements in emotional variables were observed. Despite not observing a significant effect of the intervention for young and older adults regarding the sleep quality scores, we consider that there may be an improvement in sleep physiology that is not subjectively perceived, but would also have a positive impact on memory processes. These results show that even a sleep hygiene education of 1 week could improve cognition in young adults when acute memory and sleep impairment occurs, in this case, due to the isolation by COVID-19 pandemic. However, we suggest that longer interventions should be implemented for older adults who already experience a natural decline in cognitive processes such as episodic memory formation.

Dataset Information

Cerebral functional networks during sleep in young and older individuals.

Publications

Cerebral functional networks during sleep in young and older individuals.

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