Abnormal alterations of regional spontaneous neuronal activity and functional connectivity in insomnia patients with difficulty falling asleep: a resting-state fMRI study
Abstract Background Insomnia disorder (ID) seriously affects people’s daily life. Difficulty falling asleep is the most commonly reported complaint in patients with ID. However, the mechanism of prolonged sleep latency (SL) is still obscure. The aim of our present study was to investigate the relati...
| Main Authors: | , , , , , , |
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| Format: | Article |
| Language: | English |
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BMC
2023-12-01
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| Series: | BMC Neurology |
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| Online Access: | https://doi.org/10.1186/s12883-023-03481-3 |
| _version_ | 1797397858154971136 |
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| author | Tongfei Jiang Xuejiao Yin Liying Zhu Weilin Jia Zhongjian Tan Bin Li Jing Guo |
| author_facet | Tongfei Jiang Xuejiao Yin Liying Zhu Weilin Jia Zhongjian Tan Bin Li Jing Guo |
| author_sort | Tongfei Jiang |
| collection | DOAJ |
| description | Abstract Background Insomnia disorder (ID) seriously affects people’s daily life. Difficulty falling asleep is the most commonly reported complaint in patients with ID. However, the mechanism of prolonged sleep latency (SL) is still obscure. The aim of our present study was to investigate the relationship between prolonged SL and alterations in spontaneous neural activity and brain functional connectivity (FC) in ID patients using functional magnetic resonance imaging (fMRI). Methods A total of 52 insomniacs with difficulty falling asleep and 30 matched healthy controls (HCs) underwent resting-state fMRI. The amplitude of low-frequency fluctuation (ALFF) was measured and group differences were compared. The peak areas with significantly different ALFF values were identified as the seed regions to calculate FC to the whole brain. SL was assessed by a wrist actigraphy device in ID patients. The Pittsburgh Sleep Quality Index (PSQI), Hamilton Anxiety Rating Scale (HAMA), and Hyperarousal Scale (HAS) were evaluated in both ID patients and HCs. Finally, correlation analyses were performed between the clinical features and FC/ALFF values. Results ID patients showed higher PSQI, HAMA, HAS scores than HCs. The functional MRI results indicated increased ALFF value in the left insula and right amygdala and decreased ALFF value in the right superior parietal lobe (SPL) in ID patients. The seed-based FC analysis demonstrated increased FC between the left insula and the bilateral precentral gyrus and FC between the right amygdala and the left posterior cingulate cortex (PCC) in patients with ID. Correlation analysis indicated that the increased FC value of the right amygdala-left PCC was positively correlated with SL measured by actigraphy. Conclusion This study revealed abnormal regional spontaneous fluctuations in the right amygdala, left insula, and right SPL, as well as increased FC in the left insula-precentral and right amygdala-left PCC. Moreover, the prolonged SL was positively correlated with the abnormal FC in the right amygdala-left PCC in ID patients. The current study showed the correlation between prolonged SL and the abnormal function of emotion-related brain regions in ID patients, which may contribute to a better understanding of the neural mechanisms underlying difficulty falling asleep in patients with ID. Clinical Trial Registration http://www.chictr.org.cn ., ChiCTR1800015282. Registered on 20th March 2018. |
| first_indexed | 2024-03-09T01:17:15Z |
| format | Article |
| id | doaj.art-14d0c1df0ed848a2bf2a58630c1a55f7 |
| institution | Directory Open Access Journal |
| issn | 1471-2377 |
| language | English |
| last_indexed | 2024-03-09T01:17:15Z |
| publishDate | 2023-12-01 |
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| series | BMC Neurology |
| spelling | doaj.art-14d0c1df0ed848a2bf2a58630c1a55f72023-12-10T12:22:53ZengBMCBMC Neurology1471-23772023-12-0123111210.1186/s12883-023-03481-3Abnormal alterations of regional spontaneous neuronal activity and functional connectivity in insomnia patients with difficulty falling asleep: a resting-state fMRI studyTongfei Jiang0Xuejiao Yin1Liying Zhu2Weilin Jia3Zhongjian Tan4Bin Li5Jing Guo6Department of Acupuncture and Moxibustion, Beijing Hospital of Traditional Chinese Medicine, Capital Medical University, Beijing Key Laboratory of Acupuncture NeuromodulationDepartment of Acupuncture and Moxibustion, Beijing Hospital of Traditional Chinese Medicine, Capital Medical University, Beijing Key Laboratory of Acupuncture NeuromodulationGraduate School, Beijing University of Chinese MedicineDepartment of Acupuncture and Moxibustion, Beijing Hospital of Traditional Chinese Medicine, Capital Medical University, Beijing Key Laboratory of Acupuncture NeuromodulationDepartment of Radiology, Dong Zhimen Hospital Beijing University of Chinese MedicineDepartment of Acupuncture and Moxibustion, Beijing Hospital of Traditional Chinese Medicine, Capital Medical University, Beijing Key Laboratory of Acupuncture NeuromodulationDepartment of Acupuncture and Moxibustion, Beijing Hospital of Traditional Chinese Medicine, Capital Medical University, Beijing Key Laboratory of Acupuncture NeuromodulationAbstract Background Insomnia disorder (ID) seriously affects people’s daily life. Difficulty falling asleep is the most commonly reported complaint in patients with ID. However, the mechanism of prolonged sleep latency (SL) is still obscure. The aim of our present study was to investigate the relationship between prolonged SL and alterations in spontaneous neural activity and brain functional connectivity (FC) in ID patients using functional magnetic resonance imaging (fMRI). Methods A total of 52 insomniacs with difficulty falling asleep and 30 matched healthy controls (HCs) underwent resting-state fMRI. The amplitude of low-frequency fluctuation (ALFF) was measured and group differences were compared. The peak areas with significantly different ALFF values were identified as the seed regions to calculate FC to the whole brain. SL was assessed by a wrist actigraphy device in ID patients. The Pittsburgh Sleep Quality Index (PSQI), Hamilton Anxiety Rating Scale (HAMA), and Hyperarousal Scale (HAS) were evaluated in both ID patients and HCs. Finally, correlation analyses were performed between the clinical features and FC/ALFF values. Results ID patients showed higher PSQI, HAMA, HAS scores than HCs. The functional MRI results indicated increased ALFF value in the left insula and right amygdala and decreased ALFF value in the right superior parietal lobe (SPL) in ID patients. The seed-based FC analysis demonstrated increased FC between the left insula and the bilateral precentral gyrus and FC between the right amygdala and the left posterior cingulate cortex (PCC) in patients with ID. Correlation analysis indicated that the increased FC value of the right amygdala-left PCC was positively correlated with SL measured by actigraphy. Conclusion This study revealed abnormal regional spontaneous fluctuations in the right amygdala, left insula, and right SPL, as well as increased FC in the left insula-precentral and right amygdala-left PCC. Moreover, the prolonged SL was positively correlated with the abnormal FC in the right amygdala-left PCC in ID patients. The current study showed the correlation between prolonged SL and the abnormal function of emotion-related brain regions in ID patients, which may contribute to a better understanding of the neural mechanisms underlying difficulty falling asleep in patients with ID. Clinical Trial Registration http://www.chictr.org.cn ., ChiCTR1800015282. Registered on 20th March 2018.https://doi.org/10.1186/s12883-023-03481-3Insomnia disorderSleep latency (SL)HyperarousalFunctional magnetic resonance imaging (fMRI)Amplitude of low-frequency fluctuation (ALFF)Functional connectivity (FC) |
| spellingShingle | Tongfei Jiang Xuejiao Yin Liying Zhu Weilin Jia Zhongjian Tan Bin Li Jing Guo Abnormal alterations of regional spontaneous neuronal activity and functional connectivity in insomnia patients with difficulty falling asleep: a resting-state fMRI study BMC Neurology Insomnia disorder Sleep latency (SL) Hyperarousal Functional magnetic resonance imaging (fMRI) Amplitude of low-frequency fluctuation (ALFF) Functional connectivity (FC) |
| title | Abnormal alterations of regional spontaneous neuronal activity and functional connectivity in insomnia patients with difficulty falling asleep: a resting-state fMRI study |
| title_full | Abnormal alterations of regional spontaneous neuronal activity and functional connectivity in insomnia patients with difficulty falling asleep: a resting-state fMRI study |
| title_fullStr | Abnormal alterations of regional spontaneous neuronal activity and functional connectivity in insomnia patients with difficulty falling asleep: a resting-state fMRI study |
| title_full_unstemmed | Abnormal alterations of regional spontaneous neuronal activity and functional connectivity in insomnia patients with difficulty falling asleep: a resting-state fMRI study |
| title_short | Abnormal alterations of regional spontaneous neuronal activity and functional connectivity in insomnia patients with difficulty falling asleep: a resting-state fMRI study |
| title_sort | abnormal alterations of regional spontaneous neuronal activity and functional connectivity in insomnia patients with difficulty falling asleep a resting state fmri study |
| topic | Insomnia disorder Sleep latency (SL) Hyperarousal Functional magnetic resonance imaging (fMRI) Amplitude of low-frequency fluctuation (ALFF) Functional connectivity (FC) |
| url | https://doi.org/10.1186/s12883-023-03481-3 |
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