Dataset Information

Sleep Deficits Inter-Link Lower Basal Forebrain-Posterior Cingulate Connectivity and Perceived Stress and Anxiety Bidirectionally in Young Men.

ABSTRACT:

Background

The basal nucleus of Meynert (BNM), a primary source of cholinergic projections to the cortex, plays key roles in regulating the sleep-wake cycle and attention. Sleep deficit is associated with impairment in cognitive and emotional functions. However, whether or how cholinergic circuit, sleep, and cognitive/emotional dysfunction are inter-related remains unclear.

Methods

We curated the Human Connectome Project data and explored BNM resting state functional connectivities (rsFC) in relation to sleep deficit, based on the Pittsburgh Sleep Quality Index (PSQI), cognitive performance, and subjective reports of emotional states in 687 young adults (342 women). Imaging data were processed with published routines and evaluated at a corrected threshold. We assessed the correlation between BNM rsFC, PSQI, and clinical measurements with Pearson regressions and their inter-relationships with mediation analyses.

Results

In whole-brain regressions with age and alcohol use severity as covariates, men showed lower BNM rsFC with the posterior cingulate cortex (PCC) in correlation with PSQI score. No clusters were identified in women at the same threshold. Both BNM-PCC rsFC and PSQI score were significantly correlated with anxiety, perceived stress, and neuroticism scores in men. Moreover, mediation analyses showed that PSQI score mediated the relationship between BNM-PCC rsFC and these measures of negative emotions bidirectionally in men.

Conclusions

Sleep deficit is associated with negative emotions and lower BNM rsFC with the PCC. Negative emotional states and BNM-PCC rsFC are bidirectionally related through poor sleep quality. These findings are specific to men, suggesting potential sex differences in the neural circuits regulating sleep and emotional states.

SUBMITTER: Li G

PROVIDER: S-EPMC10726414 | biostudies-literature | 2023 Dec

REPOSITORIES: biostudies-literature

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Publications

Sleep Deficits Inter-Link Lower Basal Forebrain-Posterior Cingulate Connectivity and Perceived Stress and Anxiety Bidirectionally in Young Men.

Li Guangfei G Zhong Dandan D Li Bao B Chen Yu Y Yang Lin L Li Chiang-Shan R CR

The international journal of neuropsychopharmacology 20231201 12

<h4>Background</h4>The basal nucleus of Meynert (BNM), a primary source of cholinergic projections to the cortex, plays key roles in regulating the sleep-wake cycle and attention. Sleep deficit is associated with impairment in cognitive and emotional functions. However, whether or how cholinergic circuit, sleep, and cognitive/emotional dysfunction are inter-related remains unclear.<h4>Methods</h4>We curated the Human Connectome Project data and explored BNM resting state functional connectivitie ...[more]

PMID: 37924270

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Project description:The posterior cingulate cortex (PCC) is a critical brain network hub particularly sensitive to Alzheimer's disease (AD) and can be subdivided into ventral (vPCC) and dorsal (dPCC) regions. The aim of the present study was to highlight functional connectivity (FC) disruption, atrophy, and hypometabolism within the ventral and dorsal PCC networks in patients with amnestic mild cognitive impairment (aMCI) or AD. Forty-three healthy elders (HE) (68.7 ± 6 years), 34 aMCI (73.4 ± 6.8 years) and 24 AD (70.9 ± 9.1 years) patients underwent resting-state functional MRI, anatomical T1-weighted MRI and FDG-PET scans. We compared FC maps obtained from the vPCC and dPCC seeds in HE to identify the ventral and dorsal PCC networks. We then compared patients and HE on FC, gray matter volume and metabolism within each network. In HE, the ventral PCC network involved the hippocampus and posterior occipitotemporal and temporoparietal regions, whereas the dorsal PCC network included mainly frontal, middle temporal and temporoparietal areas. aMCI patients had impaired ventral network FC in the bilateral hippocampus, but dorsal network FC was preserved. In AD, the ventral network FC disruption had spread to the left parahippocampal and angular regions, while the dorsal network FC was also affected in the right middle temporal cortex. The ventral network was atrophied in the bilateral hippocampus in aMCI patients, and in the vPCC and angular regions as well in AD patients. The dorsal network was only atrophied in AD patients, in the dPCC, bilateral supramarginal and temporal regions. By contrast, hypometabolism was already present in both the vPCC and dPCC networks in aMCI patients, and further extended to include the whole networks in AD patients. The vPCC and dPCC connectivity networks were differentially sensitive to AD. Atrophy and FC disruption were only present in the vPCC network in aMCI patients, and extended to the dPCC network in AD patients, suggesting that the pathology spreads from the vPCC to the dPCC networks. By contrast, hypometabolism seemed to follow a different route, as it was present in both networks since the aMCI stage, possibly reflecting not only local disruption but also distant synaptic dysfunction.

Project description:BackgroundCholinergic basal forebrain (BF) pathology is a hallmark of Parkinson's disease (PD) with mild cognitive impairment (PD-MCI). Assessment of functional connectivity (FC) of different cholinergic BF nuclei may deepen the understanding of PD-MCI pathogenesis.MethodsSeed-based FC analysis was performed with bilateral medial septal nucleus, the nucleus of the vertical limb of the diagonal band, nucleus of the horizontal limb of the diagonal band (Ch1-3), and the nucleus basalis of Meynert (NBM/Ch4) to explore the BF functional alterations in different frequency bands. Correlations between FC values of abnormal regions and scores of cognitive domains and depression in the PD group were also assessed.ResultsFor the right Ch4, in the conventional frequency band, the PD-MCI group exhibited lower FC values in the right middle cingulate and paracingulate gyri, middle frontal gyrus, left inferior parietal gyrus, and superior frontal gyrus compared with healthy controls (HC), and in the left calcarine fissure and surrounding cortex compared with PD with normal cognition (PD-NC). For the slow 4 subbands, the PD-MCI group showed significantly lower FC values in the left putamen, middle frontal gyrus, right middle frontal gyrus, and precuneus compared with HC, and in right middle frontal gyrus cingulate and paracingulate gyri compared with the PD-NC group. For the slow 5 subbands, the PD-MCI group showed increased FC values in the right calcarine fissure and surrounding cortex, and left cerebellum. For the left Ch1-3, FC values in the right middle cingulate and paracingulate gyri were lower in patients with PD-MCI than in the PD-NC group in slow 4 subbands. Furthermore, altered FC values in the cortical regions for Ch4 seed were possibly correlated with depression and different cognitive domain scores.ConclusionsThe study identified an imbalanced association between different cholinergic BF nuclei and cortical regions in patients with PD-MCI, and showed that FC changes are frequency-specific, which may provide new insights into functional alterations within the cholinergic system in cognitive impairment associated with PD.

Dataset Information

Sleep Deficits Inter-Link Lower Basal Forebrain-Posterior Cingulate Connectivity and Perceived Stress and Anxiety Bidirectionally in Young Men.

Background

Methods

Results

Conclusions

Publications

Sleep Deficits Inter-Link Lower Basal Forebrain-Posterior Cingulate Connectivity and Perceived Stress and Anxiety Bidirectionally in Young Men.

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