Altered thalamic connectivity in insomnia disorder during wakefulness and sleep

Zou, Guangyuan; Li, Yuezhen; Liu, Jiayi; Zhou, Shuqin; Xu, Jing; Qin, Lang; Shao, Yan; Peng, Yao; Sun, Hongqiang; Zou, Qihong; Gao, Jia‐Hong

doi:10.1002/hbm.25221

Cited by 45 publications

(37 citation statements)

References 70 publications

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“…The study on sleep deprivation revealed increased thalamic activation after total sleep deprivation, which suggested that increased thalamic activation may compensate for the attention in order to complete the task (30). Notably, the more positive connectivity between the thalamus and cortical regions in patients with insomnia was found in comparison with the healthy controls, which also supported the hyperarousal hypothesis (31). In conclusion, these explorative findings may explain the structural connectivity mechanisms underlying the reduced alertness and executive function in patients with SWD.…”

Section: Discussionmentioning

confidence: 63%

Attention Performance Correlated With White Matter Structural Brain Networks in Shift Work Disorder

et al. 2022

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Neuroimaging studies have revealed that shift work disorder (SWD) affected the functional connectivity in specific brain regions and networks. However, topological disruptions in the structural connectivity of the white matter (WM) networks associated with attention function remain poorly understood. In the current study, we recruited 33 patients with SWD and 29 matched healthy subjects. The attention network test (ANT) was employed to investigate the efficiency of alerting, orienting, and executive control networks. The diffusion tensor imaging (DTI) tractography was used to construct the WM structural networks. The graph theory analysis was applied to detect the alterations of topological properties of structural networks. Our results showed lower alerting effect and higher executive effect for patients with SWD. Using the link-based analysis, 15 altered connectivity matrices (lower fiber numbers) were found between the two groups. Meanwhile, the graph theoretical analysis showed that the global efficiency and characteristic path length within SWD patients declined in contrast with the healthy controls. Furthermore, a significantly negative correlation was found between the executive effect and global network efficiency. Our findings provide the new insights into the fundamental architecture of interregional structural connectivity underlying attention deficits in SWD, which may be a potential biomarker for SWD.

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Section: Discussionmentioning

confidence: 63%

Attention Performance Correlated With White Matter Structural Brain Networks in Shift Work Disorder

et al. 2022

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“…Although the mechanism by which subcortical areas, such as the putamen, regulate arousal is still poorly understood, the dysfunction of the frontostriatal circuit seems to have a role in insomnia. In this line, prior functional MRI studies have reported altered patterns of connectivity between subcortical (putamen) and cortical (frontal) regions in insomnia patients [ 52 – 54 ]. We found no relationship, however, with thalamic volumes.…”

Section: Discussionmentioning

confidence: 94%

Specific cortical and subcortical grey matter regions are associated with insomnia severity

et al. 2021

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Background There is an increasing awareness that sleep disturbances are a risk factor for dementia. Prior case-control studies suggested that brain grey matter (GM) changes involving cortical (i.e, prefrontal areas) and subcortical structures (i.e, putamen, thalamus) could be associated with insomnia status. However, it remains unclear whether there is a gradient association between these regions and the severity of insomnia in older adults who could be at risk for dementia. Since depressive symptoms and sleep apnea can both feature insomnia-related factors, can impact brain health and are frequently present in older populations, it is important to include them when studying insomnia. Therefore, our goal was to investigate GM changes associated with insomnia severity in a cohort of healthy older adults, taking into account the potential effect of depression and sleep apnea as well. We hypothesized that insomnia severity is correlated with 1) cortical regions responsible for regulation of sleep and emotion, such as the orbitofrontal cortex and, 2) subcortical regions, such as the putamen. Methods 120 healthy subjects (age 74.8±5.7 years old, 55.7% female) were recruited from the Hillblom Healthy Aging Network at the Memory and Aging Center, UCSF. All participants were determined to be cognitively healthy following a neurological evaluation, neuropsychological assessment and informant interview. Participants had a 3T brain MRI and completed the Insomnia Severity Index (ISI), Geriatric Depression Scale (GDS) and Berlin Sleep Questionnaire (BA) to assess sleep apnea. Cortical thickness (CTh) and subcortical volumes were obtained by the CAT12 toolbox within SPM12. We studied the correlation of CTh and subcortical volumes with ISI using multiple regressions adjusted by age, sex, handedness and MRI scan type. Additional models adjusting by GDS and BA were also performed. Results ISI and GDS were predominantly mild (4.9±4.2 and 2.5±2.9, respectively) and BA was mostly low risk (80%). Higher ISI correlated with lower CTh of the right orbitofrontal, right superior and caudal middle frontal areas, right temporo-parietal junction and left anterior cingulate cortex (p<0.001, uncorrected FWE). When adjusting by GDS, right ventral orbitofrontal and temporo-parietal junction remained significant, and left insula became significant (p<0.001, uncorrected FWE). Conversely, BA showed no effect. The results were no longer significant following FWE multiple comparisons. Regarding subcortical areas, higher putamen volumes were associated with higher ISI (p<0.01). Conclusions Our findings highlight a relationship between insomnia severity and brain health, even with relatively mild insomnia, and independent of depression and likelihood of sleep apnea. The results extend the previous literature showing the association of specific GM areas (i.e, orbitofrontal, insular and temporo-parietal junction) not just with the presence of insomnia, but across the spectrum of severity itself. Moreover, our results suggest subcortical structures (i.e., putamen) are involved as well. Longitudinal studies are needed to clarify how these insomnia-related brain changes in healthy subjects align with an increased risk of dementia.

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“…The program 3dLMEr implemented in AFNI was employed to build the statistical model and perform the linear mixed-effect analysis (Chen, Saad, Britton, Pine, & Cox, 2013) (https://afni.nimh.nih.gov/ pub/dist/doc/htmldoc/programs/3dLMEr_sphx.html#ahelp-3dlmer) because of its advantages in handling unbalanced data and controlling for potential nestedness (Zou et al, 2021). The model included variates of stages, epochs, average FD, age, sex, and years of education.…”

Section: Discussionmentioning

confidence: 99%

Functional connectivity of the human hypothalamus during wakefulness and nonrapid eye movement sleep

Jiang

Zou

Liu

et al. 2021

Human Brain Mapping

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Animal experiments indicate that the hypothalamus plays an essential role in regulating the sleep-wake cycle. A recent neuroimaging study conducted under resting wakefulness conditions suggested the presence of a wake-promoting region and a sleep-promoting region in the human posterior hypothalamus and anterior hypothalamus, respectively, and interpreted their anticorrelated organization in resting-state functional networks as evidence for their opposing roles in sleep-wake regulation.However, whether and how the functional networks of the two hypothalamic regions reorganize according to their wake-or sleep-promoting roles during sleep are unclear. Here, we constructed functional networks of the posterior and anterior hypothalamus during wakefulness and nonrapid eye movement (NREM) sleep using simultaneous electroencephalography and functional magnetic resonance imaging data collected from 62 healthy participants. The functional networks of the posterior and anterior hypothalamus exhibited inversely correlated organizations during both wakefulness and NREM sleep. The connectivity strength of the posterior hypothalamic functional network was stronger during wakefulness than during stable sleep.From wakefulness to sleep, the anterior cingulate gyrus, paracingulate gyrus, insular cortex, and fontal operculum cortex showed decreased positive connectivity, while the precentral gyrus and postcentral gyrus showed decreased negative connectivity with the posterior hypothalamus. Additionally, the insular cortex and frontal operculum cortex showed negative connectivity during wakefulness and positive connectivity during sleep with the anterior hypothalamus, exhibiting an increasing trend. These findings provide insights into the correspondence between the functional network organizations and hypothalamic sleep-wake regulation in humans.

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Altered thalamic connectivity in insomnia disorder during wakefulness and sleep

Cited by 45 publications

References 70 publications

Attention Performance Correlated With White Matter Structural Brain Networks in Shift Work Disorder

Attention Performance Correlated With White Matter Structural Brain Networks in Shift Work Disorder

Specific cortical and subcortical grey matter regions are associated with insomnia severity

Functional connectivity of the human hypothalamus during wakefulness and nonrapid eye movement sleep

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