Altered long‐ and short‐range functional connectivity density associated with poor sleep quality in patients with chronic insomnia disorder: A resting‐state fMRI study

Zhou, Fuqing; Zhu, Yanyan; Zhu, Yujun; Huang, Muhua; Jiang, Jian; He, Laichang; Huang, Su-Hua; Zeng, Xianjun; Gong, Honghan

doi:10.1002/brb3.1844

Cited by 10 publications

(6 citation statements)

References 54 publications

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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][53][54]. We found no relationship, however, with thalamic volumes.…”

Section: Discussionsupporting

confidence: 53%

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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Section: Discussionsupporting

confidence: 53%

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

et al. 2021

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“…Similar results have been reported in previous rs-fMRI researches using FCD analysis regarding other diseases ( 16 , 19 ). These results might be due to the fact that long- and short-range FCDs are not completely independent, but interrelated ( 48 ). Deco et al ( 49 ) has shown that the functional property of local (short-range) connectivity can influence remote (long-range) connectivity through feedback inhibition.…”

Section: Discussionmentioning

confidence: 99%

Altered Long- and Short-Range Functional Connectivity Density in Patients With Thyroid-Associated Ophthalmopathy: A Resting-State fMRI Study

Jiang

Chen

et al. 2022

Front. Neurol.

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Background and PurposeAlthough previous neuroimaging studies have demonstrated emotion- and psychology-associated brain abnormalities in patients with thyroid-associated ophthalmopathy (TAO), the changes of brain functional connectivity in TAO were seldom focused. We aimed to investigate interregional and intraregional functional interactions in patients with TAO by using resting-state functional MRI (rs-fMRI) with long- and short-range functional connectivity density (FCD) analysis.MethodsThirty patients with TAO and 30 well-matched healthy controls (HCs) were recruited in our study. Long- and short-range FCD values were calculated and compared between the two groups. Correlations between long- and short-range FCD values and clinical indicators were analyzed.ResultsCompared with HCs, patients with showed both increased long- and short-range FCDs in the left middle frontal gyrus (MFG), orbital part of superior frontal gyrus (ORBsup), and dorsolateral part of superior frontal gyrus (SFGdor); meanwhile, both decreased long- and short-range FCDs in bilateral postcentral gyrus (PoCG), left superior parietal gyrus (SPG), and inferior parietal (IPL). In addition, patients with TAO showed increased short-range FCD in the right SFGdor, bilateral medial part of superior frontal gyrus (SFGmed), left orbital part of middle frontal gyrus (ORBmid), and orbital part of inferior frontal gyrus (ORBinf), as well as decreased short-range FCD in the right supplementary motor area (SMA) and the left paracentral lobule (PCL) than HCs. Moreover, the short-range value in the left SFGdor showed a negative correlation with Montreal Cognitive Assessment (MoCA) score (r = −0.501, p = 0.005).ConclusionOur findings complemented the functional neural mechanism of TAO, and provided potential neuroimaging markers for assessing the psychiatric, visual, and emotional disturbances in patients with TAO.

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“…In comparison with HCs, patients with CID showed an increased response in the DMN (including right MTG) upon exposure to self-related words ( Marques et al, 2018 ). Zhou et al (2020) discovered increased short DC in the MTG compared with HCs. By using the ICA method, Marques et al (2017) found that patients with CID exhibited increased activation in the right MTG and IPG compared with HCs.…”

Section: Discussionmentioning

confidence: 92%

Real-Time fMRI Neurofeedback Training Changes Brain Degree Centrality and Improves Sleep in Chronic Insomnia Disorder: A Resting-State fMRI Study

Zou

et al. 2022

Front. Mol. Neurosci.

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BackgroundChronic insomnia disorder (CID) is considered a major public health problem worldwide. Therefore, innovative and effective technical methods for studying the pathogenesis and clinical comprehensive treatment of CID are urgently needed.MethodsReal-time fMRI neurofeedback (rtfMRI-NF), a new intervention, was used to train 28 patients with CID to regulate their amygdala activity for three sessions in 6 weeks. Resting-state fMRI data were collected before and after training. Then, voxel-based degree centrality (DC) method was used to explore the effect of rtfMRI-NF training. For regions with altered DC, we determined the specific connections to other regions that most strongly contributed to altered functional networks based on DC. Furthermore, the relationships between the DC value of the altered regions and changes in clinical variables were determined.ResultsPatients with CID showed increased DC in the right postcentral gyrus, Rolandic operculum, insula, and superior parietal gyrus and decreased DC in the right supramarginal gyrus, inferior parietal gyrus, angular gyrus, middle occipital gyrus, and middle temporal gyrus. Seed-based functional connectivity analyses based on the altered DC regions showed more details about the altered functional networks. Clinical scores in Pittsburgh sleep quality index, insomnia severity index (ISI), Beck depression inventory, and Hamilton anxiety scale decreased. Furthermore, a remarkable positive correlation was found between the changed ISI score and DC values of the right insula.ConclusionsThis study confirmed that amygdala-based rtfMRI-NF training altered the intrinsic functional hubs, which reshaped the abnormal functional connections caused by insomnia and improved the sleep of patients with CID. These findings contribute to our understanding of the neurobiological mechanism of rtfMRI-NF in insomnia treatment. However, additional double-blinded controlled clinical trials with larger sample sizes need to be conducted to confirm the effect of rtfMRI-NF from this initial study.

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Altered long‐ and short‐range functional connectivity density associated with poor sleep quality in patients with chronic insomnia disorder: A resting‐state fMRI study

Abstract: This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

Cited by 10 publications

References 54 publications

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

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

Altered Long- and Short-Range Functional Connectivity Density in Patients With Thyroid-Associated Ophthalmopathy: A Resting-State fMRI Study

Real-Time fMRI Neurofeedback Training Changes Brain Degree Centrality and Improves Sleep in Chronic Insomnia Disorder: A Resting-State fMRI Study

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