Large‐scale functional network connectivity mediate the associations of gut microbiota with sleep quality and executive functions

Cai, Huanhuan; Wang, Chunli; Qian, Yinfeng; Zhang, Shujun; Zhang, Cun; Zhao, Wenming; Zhang, Tingting; Zhang, Biao; Chen, Jingyao; Liu, Siyu; Zhu, Jiajia; Yu, Yongqiang

doi:10.1002/hbm.25419

Cited by 40 publications

(41 citation statements)

References 67 publications

(73 reference statements)

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“…Regarding the metabolic pathways, arginine and proline metabolism, phenylalanine metabolism, and biosynthesis of unsaturated fatty acids contribute most to the associations; the executive control and sensorimotor systems are considered as being most contributive at the neural level. The present study, extending our previous work ( Cai et al, 2021 ) in an elegant way, may shed light on the gut Bacteroides -metabolic pathways-functional connectivity-cognition relationships.…”

Section: Discussionsupporting

confidence: 77%

“…We demonstrate that multiple Bacteroides -related metabolic pathways preferentially influence functional connectivity of the executive control and sensorimotor systems. The executive control system mainly consists of the prefrontal and lateral parietal cortices, which are thought to be involved in a variety of goal-oriented cognitive-control processes such as working memory, inhibitory control, and attention ( Song et al, 2013 ; Cai et al, 2021 ). In agreement with the concept, we found that functional connectivity of the executive control system mediated the relation of Bacteroides -related metabolic pathways with working memory and behavioral inhibition.…”

Section: Discussionmentioning

confidence: 99%

“…By leveraging seed-based functional connectivity approaches, researchers have revealed associations of gut Bacteroides with reduced connectivity between core reward regions in patients with obesity after laparoscopic sleeve gastrectomy ( Dong et al, 2020 ) and lower connectivity between the dorsolateral prefrontal cortex and anterior medial frontal cortex in patients with major depressive disorder ( Strandwitz et al, 2019 ). While our previous work indicates significant effects of microbial diversity and enterotypes on functional connectivity between and within large-scale neural networks ( Cai et al, 2021 ), the exact relationship between gut Bacteroides and large-scale functional network connectivity has yet to be determined.…”

Section: Introductionmentioning

confidence: 93%

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Metabolic and Neural Mechanisms Underlying the Associations Between Gut Bacteroides and Cognition: A Large-Scale Functional Network Connectivity Study

Zhang

Qian

et al. 2021

Front. Neurosci.

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There is a proof-of-concept that microbial metabolites provide a molecular connection between the gut and the brain. Extensive research has established a link between gut Bacteroides and human cognition, yet the metabolic and neural mechanisms underlying this association remain largely unknown. Here, we collected fecal samples, resting-state functional MRI, and cognitive data from a large and homogeneous sample of 157 healthy young adults. 16S rRNA gene sequencing was conducted with abundances of Bacteroides and metabolic pathways quantified by species annotation and functional prediction analyses, respectively. Large-scale intra- and internetwork functional connectivity was measured using independent component analysis. Results showed that gut Bacteroides were related to multiple metabolic pathways, which in turn were associated with widespread functional network connectivity. Furthermore, functional network connectivity mediated the associations between some Bacteroides-related metabolic pathways and cognition. Remarkably, arginine and proline metabolism, phenylalanine metabolism, and biosynthesis of unsaturated fatty acids act as the key metabolic pathways that are most contributive, and the executive control and sensorimotor systems contribute most strongly at the neural level. Our findings suggest complex poly-pathway and poly-network processes linking Bacteroides to cognition, more generally yielding a novel conceptualization of targeting gut Bacteroides as an intervention strategy for individuals with cognitive impairment.

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Section: Discussionsupporting

confidence: 77%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 93%

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Metabolic and Neural Mechanisms Underlying the Associations Between Gut Bacteroides and Cognition: A Large-Scale Functional Network Connectivity Study

Zhang

Qian

et al. 2021

Front. Neurosci.

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“…Prevotella dominated enterotype has been demonstrated to be associated with an elevated functional intra-network connectivity of the ECN. 10 Furthermore, this connectivity mediated reaction times in an executive control task, further supporting the functional profile of the ECN-DMN-Prevotella + -Blautia − and FPN-Bifido-Prevotella to executive control and attention. Our study may add more facets to this picture by the division between attention related to Bifidobacterium and Prevotella covariance patterns and executive control with DMN association and lower abundance of Blautia .…”

Section: Discussionmentioning

confidence: 53%

“… 9 A recent study (n = 157) focused on certain enteroptypes and diversity measures in the gut and their association to specific large-scale brain networks. 10 The authors found an association between gut microbial diversity measures with network connectivity of executive control, default mode and sensorimotor control, as well as within executive control network. Enterotypes were linked to executive control network.…”

Section: Introductionmentioning

confidence: 95%

Multivariate associative patterns between the gut microbiota and large-scale brain network connectivity

et al. 2021

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Research on the gut–brain axis has accelerated substantially over the course of the last years. Many reviews have outlined the important implications of understanding the relation of the gut microbiota with human brain function and behavior. One substantial drawback in integrating gut microbiome and brain data is the lack of integrative multivariate approaches that enable capturing variance in both modalities simultaneously. To address this issue, we applied a linked independent component analysis (LICA) to microbiota and brain connectivity data.We analyzed data from 58 healthy females (mean age =  21.5 years). Magnetic Resonance Imaging data were acquired using resting state functional imaging data. The assessment of gut microbial composition from feces was based on sequencing of the V4 16S rRNA gene region. We used the LICA model to simultaneously factorize the subjects’ large-scale brain networks and microbiome relative abundance data into 10 independent components of spatial and abundance variation.LICA decomposition resulted in four components with non-marginal contribution of the microbiota data. The default mode network featured strongly in three components, whereas the two-lateralized fronto-parietal attention networks contributed to one component. The executive-control (with the default mode) network was associated to another component. We found that the abundance of Prevotella genus was associated with the strength of expression of all networks, whereas Bifidobacterium was associated with the default mode and frontoparietal-attention networks.We provide the first exploratory evidence for multivariate associative patterns between the gut microbiota and brain network connectivity in healthy humans considering the complexity of both systems.

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Impact of sex and serum lipids interaction on working memory: A large‐scale brain networks study

Zhang

Sun

et al. 2023

Brain and Behavior

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Backgrounds: Previous studies have demonstrated that both serum lipid levels and sex are crucial factors associated with individual cognition. However, the impact of sex and serum lipid interaction effects on the brain and cognition remains largely unknown.This study aimed to explore the underlying neural mechanisms among sex, serum lipids, and cognition using large-scale brain networks. Methods:Resting-state functional MRI data were collected from 157 young healthy adults. Independent component analysis was used to examine large-scale inter-and intra-network functional connectivity (FCs). Peripheral venous blood samples were collected to measure serum lipid levels. The three-back task was employed to assess cognition (i.e., working memory). General linear model, correlation, and mediation analyses were conducted to examine the interaction effects of sex and serum lipids on large-scale brain networks and their relationship with working memory. Results:We found that inter-network connectivity with the executive control network at its core was more susceptible to sex and triglyceride interaction effects. The intra-network connectivity in the dorsal attention networks (DANs), lateral visual networks, and anterior default mode networks was influenced by the interaction effects of sex and total cholesterol (TC)/low-density lipoprotein cholesterol. Specifically, correlations between serum lipids and affected brain networks were found to be sex-specific.In addition, higher intra-network FC in the right inferior parietal (R-IPL) of the DAN correlated with a longer three-back reaction time in females. More importantly, the relationship between serum TC levels and three-back reaction time was mediated by intra-network connectivity in the R-IPL of the DAN.Conclusions: Our findings describe the impact of sex and serum lipid interaction effects on large-scale brain networks, as well as on cognitive function. Our data suggest that sex-specific usage of serum lipids or brain networks would be beneficial for monitoring and therapy in dyslipidemia-related cognition decline.

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Large‐scale functional network connectivity mediate the associations of gut microbiota with sleep quality and executive functions

Cited by 40 publications

References 67 publications

Metabolic and Neural Mechanisms Underlying the Associations Between Gut Bacteroides and Cognition: A Large-Scale Functional Network Connectivity Study

Metabolic and Neural Mechanisms Underlying the Associations Between Gut Bacteroides and Cognition: A Large-Scale Functional Network Connectivity Study

Multivariate associative patterns between the gut microbiota and large-scale brain network connectivity

Impact of sex and serum lipids interaction on working memory: A large‐scale brain networks study

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