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European Archives of Psychiatry and Clinical Neuroscience

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12-09-2022 | Insomnia | Original Paper

Distinct functional brain abnormalities in insomnia disorder and obstructive sleep apnea

Authors: Weiwei Duan, Xia Liu, Liangliang Ping, Shushu Jin, Hao Yu, Man Dong, Fangfang Xu, Na Li, Ying Li, Yinghong Xu, Zhe Ji, Yuqi Cheng, Xiufeng Xu, Cong Zhou

Published in: European Archives of Psychiatry and Clinical Neuroscience | Issue 2/2023

Abstract

Insomnia disorder (ID) and obstructive sleep apnea (OSA) are the two most prevalent sleep disorders worldwide, but the pathological mechanism has not been fully understood. Functional neuroimaging findings indicated regional abnormal neural activities existed in both diseases, but the results were inconsistent. This meta-analysis aimed to explore concordant regional functional brain changes in ID and OSA, respectively. We conducted a coordinate-based meta-analysis (CBMA) of resting-state functional magnetic resonance imaging (rs-fMRI) studies using the anisotropic effect-size seed‐based d mapping (AES-SDM) approach. Studies that applied regional homogeneity (ReHo), amplitude of low-frequency fluctuations (ALFF) or fractional ALFF (fALFF) to analyze regional spontaneous brain activities in ID or OSA were included. Meta-regressions were then applied to investigate potential associations between demographic variables and regional neural activity alterations. Significantly increased brain activities in the left superior temporal gyrus (STG.L) and right superior longitudinal fasciculus (SLF.R), as well as decreased brain activities in several right cerebral hemisphere areas were identified in ID patients. As for OSA patients, more distinct and complicated functional activation alterations were identified. Several neuroimaging alterations were functionally correlated with mean age, duration or illness severity in two patients groups revealed by meta-regressions. These functionally altered areas could be served as potential targets for non-invasive brain stimulation methods. This present meta-analysis distinguished distinct brain function changes in ID and OSA, improving our knowledge of the neuropathological mechanism of these two most common sleep disturbances, and also provided potential orientations for future clinical applications.

Registration number: CRD42022301938.

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Khazaie H, Veronese M, Noori K, Emamian F, Zarei M, Ashkan K et al (2017) Functional reorganization in obstructive sleep apnoea and insomnia: a systematic review of the resting-state fMRI. Neurosci Biobehav Rev 77:219–231PubMedPubMedCentralCrossRef

Fasiello E, Gorgoni M, Scarpelli S, Alfonsi V, Ferini Strambi L, De Gennaro L (2022) Functional connectivity changes in insomnia disorder: a systematic review. Sleep Med Rev 61:101569PubMedCrossRef

Morin CM, Drake CL, Harvey AG, Krystal AD, Manber R, Riemann D, et al. Insomnia disorder. Nature Reviews Disease Primers. 2015;1(1).

Tahmasian M, Rosenzweig I, Eickhoff SB, Sepehry AA, Laird AR, Fox PT et al (2016) Structural and functional neural adaptations in obstructive sleep apnea: an activation likelihood estimation meta-analysis. Neurosci Biobehav Rev 65:142–156PubMedPubMedCentralCrossRef

Franklin KA, Lindberg E (2015) Obstructive sleep apnea is a common disorder in the population-a review on the epidemiology of sleep apnea. J Thorac Dis 7(8):1311–1322PubMedPubMedCentral

Ohayon MM, Reynolds CF 3rd (2009) Epidemiological and clinical relevance of insomnia diagnosis algorithms according to the DSM-IV and the International Classification of Sleep Disorders (ICSD). Sleep Med 10(9):952–960PubMedPubMedCentralCrossRef

de Souza RJ, Cao X-L, Wang S-B, Zhong B-L, Zhang L, Ungvari GS et al (2017) The prevalence of insomnia in the general population in China: a meta-analysis. PLoS ONE 12(2):e0170772CrossRef

Wu Y, Zhuang Y, Qi J (2020) Explore structural and functional brain changes in insomnia disorder: a PRISMA-compliant whole brain ALE meta-analysis for multimodal MRI. Medicine 99(14):e19151PubMedPubMedCentralCrossRef

Levy P, Kohler M, McNicholas WT, Barbe F, McEvoy RD, Somers VK et al (2015) Obstructive sleep apnoea syndrome. Nat Rev Dis Primers 1:15015PubMedCrossRef

10.

Chellappa SL, Aeschbach D (2022) Sleep and anxiety: from mechanisms to interventions. Sleep Med Rev 61:101583PubMedCrossRef

11.

Sarsour K, Morin C, Foley K, Kalsekar A, Walsh J (2010) Association of insomnia severity and comorbid medical and psychiatric disorders in a health plan-based sample: insomnia severity and comorbidities. Sleep Med 11(1):69–74PubMedCrossRef

12.

Budhiraja R, Roth T, Hudgel D, Budhiraja P, Drake C (2011) Prevalence and polysomnographic correlates of insomnia comorbid with medical disorders. Sleep 34(7):859–867PubMedPubMedCentralCrossRef

13.

McCall WV, Benca RM, Rumble ME, Case D, Rosenquist PB, Krystal AD (2019) Prevalence of obstructive sleep apnea in suicidal patients with major depressive disorder. J Psychiatr Res 116:147–150PubMedPubMedCentralCrossRef

14.

Zhang M, Ma Y, Du L, Wang K, Li Z, Zhu W et al (2022) Sleep disorders and non-sleep circadian disorders predict depression: a systematic review and meta-analysis of longitudinal studies. Neurosci Biobehav Rev 134:104532PubMedCrossRef

15.

Fox MD, Raichle ME (2007) Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging. Nat Rev Neurosci 8(9):700–711PubMedCrossRef

16.

Snyder AZ, Raichle ME (2012) A brief history of the resting state: the Washington University perspective. Neuroimage 62(2):902–910PubMedCrossRef

17.

Wang Q, Wang C, Deng Q, Zhan L, Tang Y, Li H et al (2022) Alterations of regional spontaneous brain activities in anxiety disorders: a meta-analysis. J Affect Disord 296:233–240PubMedCrossRef

18.

Zang YF, Zuo XN, Milham M, Hallett M (2015) Toward a meta-analytic synthesis of the resting-state fmri literature for clinical populations. Biomed Res Int 2015:435265PubMedPubMedCentralCrossRef

19.

Salvia E, Tissier C, Charron S, Herent P, Vidal J, Lion S et al (2019) The local properties of bold signal fluctuations at rest monitor inhibitory control training in adolescents. Dev Cogn Neurosci 38:100664PubMedPubMedCentralCrossRef

20.

Aydin S (2011) Computer based synchronization analysis on sleep EEG in insomnia. J Med Syst 35(4):517–520PubMedCrossRef

21.

Aksahin M, Aydin S, Firat H, Erogul O (2012) Artificial apnea classification with quantitative sleep EEG synchronization. J Med Syst 36(1):139–144PubMedCrossRef

22.

Aydin S, Tunga MA, Yetkin S (2015) Mutual information analysis of sleep EEG in detecting psycho-physiological insomnia. J Med Syst 39(5):43PubMedCrossRef

23.

Zhang Y, Zhang Z, Wang Y, Zhu F, Liu X, Chen W et al (2021) Dysfunctional beliefs and attitudes about sleep are associated with regional homogeneity of left inferior occidental gyrus in primary insomnia patients: a preliminary resting state functional magnetic resonance imaging study. Sleep Med 81:188–193PubMedCrossRef

24.

Ji T, Li X, Chen J, Ren X, Mei L, Qiu Y, et al. Brain function in children with obstructive sleep apnea: a resting-state fMRI study. Sleep. 2021;44(8).

25.

Li H, Li L, Kong L, Li P, Zeng Y, Li K et al (2021) Frequency specific regional homogeneity alterations and cognitive function in obstructive sleep apnea before and after short-term continuous positive airway pressure treatment. Nat Sci Sleep 13:2221–2238PubMedPubMedCentralCrossRef

26.

Liu J, Cao L, Li H, Gao Y, Bu X, Liang K, et al. Abnormal resting-state functional connectivity in patients with obsessive-compulsive disorder: A systematic review and meta-analysis. Neuroscience and biobehavioral reviews. 2022:104574.

27.

Muller VI, Cieslik EC, Laird AR, Fox PT, Radua J, Mataix-Cols D et al (2018) Ten simple rules for neuroimaging meta-analysis. Neurosci Biobehav Rev 84:151–161PubMedCrossRef

28.

Tang S, Lu L, Zhang L, Hu X, Bu X, Li H et al (2018) Abnormal amygdala resting-state functional connectivity in adults and adolescents with major depressive disorder: A comparative meta-analysis. EBioMedicine 36:436–445PubMedPubMedCentralCrossRef

29.

Radua J, Mataix-Cols D, Phillips ML, El-Hage W, Kronhaus DM, Cardoner N et al (2012) A new meta-analytic method for neuroimaging studies that combines reported peak coordinates and statistical parametric maps. Eur Psychiatry 27(8):605–611PubMedCrossRef

30.

Radua J, Mataix-Cols D (2009) Voxel-wise meta-analysis of grey matter changes in obsessive-compulsive disorder. Br J Psychiatry 195(5):393–402PubMedCrossRef

31.

Radua J, Rubia K, Canales-Rodriguez EJ, Pomarol-Clotet E, Fusar-Poli P, Mataix-Cols D (2014) Anisotropic kernels for coordinate-based meta-analyses of neuroimaging studies. Front Psych 5:13

32.

Zhou C, Li J, Dong M, Ping L, Lin H, Wang Y et al (2021) Altered white matter microstructures in type 2 diabetes mellitus: a coordinate-based meta-analysis of diffusion tensor imaging studies. Front Endocrinol (Lausanne) 12:658198PubMedCrossRef

33.

Gong J, Wang J, Luo X, Chen G, Huang H, Huang R et al (2020) Abnormalities of intrinsic regional brain activity in first-episode and chronic schizophrenia: a meta-analysis of resting-state functional MRI. J Psychiatry Neurosci 45(1):55–68PubMedCrossRef

34.

Tahmasian M, Noori K, Samea F, Zarei M, Spiegelhalder K, Eickhoff SB et al (2018) A lack of consistent brain alterations in insomnia disorder: an activation likelihood estimation meta-analysis. Sleep Med Rev 42:111–118PubMedPubMedCentralCrossRef

35.

Jiang B, He D, Guo Z, Gao Z (2019) Effect-size seed-based d mapping of resting-state fMRI for persistent insomnia disorder. Sleep Breathing 24(2):653–659PubMedCrossRef

36.

Ma X, Liu J, Liu T, Ma L, Wang W, Shi S et al (2019) Altered resting-state functional activity in medication-naive patients with first-episode major depression disorder vs healthy control: a quantitative meta-analysis. Front Behav Neurosci 13:89PubMedPubMedCentralCrossRef

37.

Wang J, Zhang JR, Zang YF, Wu T. Consistent decreased activity in the putamen in Parkinson's disease: a meta-analysis and an independent validation of resting-state fMRI. GigaScience. 2018;7(6).

38.

Liu J, Li Y, Yang X, Xu H, Ren J, Zhou P (2021) Regional spontaneous neural activity alterations in type 2 diabetes mellitus: a meta-analysis of resting-state functional MRI studies. Front Aging Neurosci 13:678359PubMedPubMedCentralCrossRef

39.

Moher D, Liberati A, Tetzlaff J, Altman DG, Group TP (2009) Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. J Clin Epidemiol 62(10):1006–1012CrossRef

40.

Liberati A, Altman DG, Tetzlaff J, Mulrow C, Gotzsche PC, Ioannidis JP et al (2009) The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate healthcare interventions: explanation and elaboration. BMJ 339:b2700PubMedPubMedCentralCrossRef

41.

Moher, David, Liberati, Alessandro, Tetzlaff, Jennifer, et al. Preferred Reporting Items for Systematic Reviews and Meta-Analyses: The PRISMA Statement. PLoS Medicine. 2009.

42.

Albajes-Eizagirre A, Solanes A, Vieta E, Radua J (2019) Voxel-based meta-analysis via permutation of subject images (PSI): Theory and implementation for SDM. Neuroimage 186:174–184PubMedCrossRef

43.

Gao X, Zhang W, Yao L, Xiao Y, Liu L, Liu J et al (2018) Association between structural and functional brain alterations in drug-free patients with schizophrenia: a multimodal meta-analysis. J Psychiatry Neurosci 43(2):131–142PubMedCrossRef

44.

Qing X, Gu L, Li D (2021) Abnormalities of localized connectivity in obsessive-compulsive disorder: a voxel-wise meta-analysis. Front Hum Neurosci 15:739175PubMedPubMedCentralCrossRef

45.

Yao L, Yang C, Zhang W, Li S, Li Q, Chen L et al (2021) A multimodal meta-analysis of regional structural and functional brain alterations in type 2 diabetes. Front Neuroendocrinol 62:100915PubMedCrossRef

46.

Dai XJ, Peng DC, Gong HH, Wan AL, Nie X, Li HJ et al (2014) Altered intrinsic regional brain spontaneous activity and subjective sleep quality in patients with chronic primary insomnia: a resting-state fMRI study. Neuropsychiatr Dis Treat 10:2163–2175PubMedPubMedCentralCrossRef

47.

Wang T, Li S, Jiang G, Lin C, Li M, Ma X et al (2016) Regional homogeneity changes in patients with primary insomnia. Eur Radiol 26(5):1292–1300PubMedCrossRef

48.

Dai XJ, Nie X, Liu X, Pei L, Jiang J, Peng DC et al (2016) Gender differences in regional brain activity in patients with chronic primary insomnia: evidence from a resting-state fMRI study. J Clin Sleep Med 12(3):363–374PubMedPubMedCentralCrossRef

49.

Li C, Ma X, Dong M, Yin Y, Hua K, Li M et al (2016) Abnormal spontaneous regional brain activity in primary insomnia: a resting-state functional magnetic resonance imaging study. Neuropsychiatr Dis Treat 12:1371–1378PubMedPubMedCentral

50.

Ran Q, Chen J, Li C, Wen L, Yue F, Shu T et al (2017) Abnormal amplitude of low-frequency fluctuations associated with rapid-eye movement in chronic primary insomnia patients. Oncotarget 8(49):84877–84888PubMedPubMedCentralCrossRef

51.

Wang YK, Shi XH, Wang YY, Zhang X, Liu HY, Wang XT et al (2020) Evaluation of the age-related and gender-related differences in patients with primary insomnia by fractional amplitude of low-frequency fluctuation: a resting-state functional magnetic resonance imaging study. Medicine 99(3):e18786PubMedPubMedCentralCrossRef

52.

Zhao B, Bi Y, Li L, Zhang J, Hong Y, Zhang L et al (2020) The instant spontaneous neuronal activity modulation of transcutaneous auricular vagus nerve stimulation on patients with primary insomnia. Front Neurosci 14:205PubMedPubMedCentralCrossRef

53.

Feng Y, Fu S, Li C, Ma X, Wu Y, Chen F et al (2022) Interaction of gut microbiota and brain function in patients with chronic insomnia: a regional homogeneity study. Front Neurosci 15:804843PubMedPubMedCentralCrossRef

54.

Santarnecchi E, Sicilia I, Richiardi J, Vatti G, Polizzotto NR, Marino D et al (2013) Altered cortical and subcortical local coherence in obstructive sleep apnea: a functional magnetic resonance imaging study. J Sleep Res 22(3):337–347PubMedCrossRef

55.

Peng DC, Dai XJ, Gong HH, Li HJ, Nie X, Zhang W (2014) Altered intrinsic regional brain activity in male patients with severe obstructive sleep apnea: a resting-state functional magnetic resonance imaging study. Neuropsychiatr Dis Treat 10:1819–1826PubMedPubMedCentral

56.

Li HJ, Dai XJ, Gong HH, Nie X, Zhang W, Peng DC (2015) Aberrant spontaneous low-frequency brain activity in male patients with severe obstructive sleep apnea revealed by resting-state functional MRI. Neuropsychiatr Dis Treat 11:207–214PubMedPubMedCentral

57.

Kang D, Qin Z, Wang W, Zheng Y, Hu H, Bao Y et al (2020) Brain functional changes in tibetan with obstructive sleep apnea hypopnea syndrome: a resting state fMRI study. Medicine 99(7):e18957PubMedPubMedCentralCrossRef

58.

Qin Z, Kang D, Feng X, Kong D, Wang F, Bao H (2020) Resting-state functional magnetic resonance imaging of high altitude patients with obstructive sleep apnoea hypopnoea syndrome. Sci Rep 10(1):15546PubMedPubMedCentralCrossRef

59.

Zhou L, Shan X, Peng Y, Liu G, Guo W, Luo H et al (2020) Reduced regional homogeneity and neurocognitive impairment in patients with moderate-to-severe obstructive sleep apnea. Sleep Med 75:418–427PubMedCrossRef

60.

Bai J, Wen H, Tai J, Peng Y, Li H, Mei L et al (2021) Altered spontaneous brain activity related to neurologic and sleep dysfunction in children with obstructive sleep apnea syndrome. Front Neurosci 15:595412PubMedPubMedCentralCrossRef

61.

Santarnecchi E, Sprugnoli G, Sicilia I, Dukart J, Neri F, Romanella SM, et al. Thalamic altered spontaneous activity and connectivity in obstructive sleep apnea syndrome. J Neuroimaging. 2021.

62.

Riemann D, Spiegelhalder K, Feige B, Voderholzer U, Berger M, Perlis M et al (2010) The hyperarousal model of insomnia: a review of the concept and its evidence. Sleep Med Rev 14(1):19–31PubMedCrossRef

63.

Sha Z, Wager TD, Mechelli A, He Y (2019) Common dysfunction of large-scale neurocognitive networks across psychiatric disorders. Biol Psychiat 85(5):379–388PubMedCrossRef

64.

Regen W, Kyle SD, Nissen C, Feige B, Baglioni C, Hennig J et al (2016) Objective sleep disturbances are associated with greater waking resting-state connectivity between the retrosplenial cortex/ hippocampus and various nodes of the default mode network. J Psychiatry Neurosci 41(5):295–303PubMedPubMedCentralCrossRef

65.

Cai W, Zhao M, Liu J, Liu B, Yu D, Yuan K. Right arcuate fasciculus and superior longitudinal fasciculus abnormalities in primary insomnia. Brain imaging and behavior. 2019.

66.

Pisner DA, Shumake J, Beevers CG, Schnyer DM (2019) The superior longitudinal fasciculus and its functional triple-network mechanisms in brooding. NeuroImage Clin 24:101935PubMedPubMedCentralCrossRef

67.

Sanjari Moghaddam H, Mohammadi E, Dolatshahi M, Mohebi F, Ashrafi A, Khazaie H et al (2021) White matter microstructural abnormalities in primary insomnia: a systematic review of diffusion tensor imaging studies. Prog Neuropsychopharmacol Biol Psychiatry 105:110132PubMedCrossRef

68.

Hu X, Liu Q, Li B, Tang W, Sun H, Li F et al (2016) Multivariate pattern analysis of obsessive-compulsive disorder using structural neuroanatomy. Eur Neuropsychopharmacol 26(2):246–254PubMedCrossRef

69.

Ramnani N (2012) Frontal lobe and posterior parietal contributions to the cortico-cerebellar system. Cerebellum 11(2):366–383PubMedCrossRef

70.

Schmahmann JD, Weilburg JB, Sherman JC (2007) The neuropsychiatry of the cerebellum—insights from the clinic. Cerebellum 6(3):254–267PubMedCrossRef

71.

Hampshire A, Chamberlain SR, Monti MM, Duncan J, Owen AM (2010) The role of the right inferior frontal gyrus: inhibition and attentional control. Neuroimage 50(3):1313–1319PubMedCrossRef

72.

Marklund P, Persson J (2012) Context-dependent switching between proactive and reactive working memory control mechanisms in the right inferior frontal gyrus. Neuroimage 63(3):1552–1560PubMedCrossRef

73.

Wang S, Wang H, Liu X, Yan W, Wang M, Zhao R. A resting-state functional MRI study in patients with vestibular migraine during interictal period. Acta neurologica Belgica. 2021.

74.

Jiang CG, Zhang T, Yue FG, Yi ML, Gao D (2013) Efficacy of repetitive transcranial magnetic stimulation in the treatment of patients with chronic primary insomnia. Cell Biochem Biophys 67(1):169–173PubMedCrossRef

75.

Arens R, Sin S, Nandalike K, Rieder J, Khan UI, Freeman K et al (2011) Upper airway structure and body fat composition in obese children with obstructive sleep apnea syndrome. Am J Respir Crit Care Med 183(6):782–787PubMedCrossRef

76.

Drager LF, Togeiro SM, Polotsky VY, Lorenzi-Filho G (2013) Obstructive sleep apnea: a cardiometabolic risk in obesity and the metabolic syndrome. J Am Coll Cardiol 62(7):569–576PubMedPubMedCentralCrossRef

77.

Inge T, King W, Jenkins T, Courcoulas A, Mitsnefes M, Flum D et al (2013) The effect of obesity in adolescence on adult health status. Pediatrics 132(6):1098–1104PubMedPubMedCentralCrossRef

Title: Distinct functional brain abnormalities in insomnia disorder and obstructive sleep apnea
Authors: Weiwei Duan
Xia Liu
Liangliang Ping
Shushu Jin
Hao Yu
Man Dong
Fangfang Xu
Na Li
Ying Li
Yinghong Xu
Zhe Ji
Yuqi Cheng
Xiufeng Xu
Cong Zhou
Publication date: 12-09-2022
Publisher: Springer Berlin Heidelberg
Keywords: Insomnia
Sleep Apnea
Published in: European Archives of Psychiatry and Clinical Neuroscience / Issue 2/2023
Print ISSN: 0940-1334
Electronic ISSN: 1433-8491
DOI: https://doi.org/10.1007/s00406-022-01485-7

At a glance: The STEP trials

Springer Medicine

Distinct functional brain abnormalities in insomnia disorder and obstructive sleep apnea

Abstract

At a glance: The STEP trials

Springer Medicine

Abstract

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