Skip to main content
SpringerLink
Log in

Aberrant functional connectivity in patients with obstructive sleep apnea-hypopnea syndrome: a resting-state functional MRI study

  • Published:
Multimedia Tools and Applications Aims and scope Submit manuscript

Abstract

The objective of this study was to investigate the change in the default mode network (DMN) in subjects with obstructive sleep apnea-hypopnea syndrome (OSAHS) using resting-state functional connectivity (rsFC). Functional magnetic resonance imaging (rs-fMRI) data were collected from twenty-nine subjects with OSAHS and twenty-six normal controls. The data were analyzed with the rsFC method and were compared between OSAHS subjects and controls. The Z-values of abnormal rsFC in different brain regions were correlated with clinical variables, including the apnea-hypopnea index (AHI), oxygen desaturation index (ODI), Epworth sleepiness scale (ESS), Rey-osterrieth complex figure test (CFT-immediately), CFT-delay, Logical memory test-immediately (LMT-immediately), LMT-delay and Minimum mental state examination (MMSE). The rsFC showed significant increases in the left temporal cortex, right midfrontal cortex, and left precuneus cortex as well as decreases in the bilateral inferior parietal lobule (IPL), left medial prefrontal cortex (MPFC), left superior frontal cortex and right cerebellum in patients with OSAHS. The FC strength in the left precuneus showed a remarkable positive correlation with ODI(p = .032, r = .399)and CFT-delay scores (p = .043, r = .378). We found that the FC strength in the right cerebellum was positively correlated with the CFT-delay scores (p = .017, r = .441). FC strength in the right cerebellum and left IPL demonstrated a remarkable positive correlation with LMT-delay scores (p = .037,r = .389;p = .043 and r = .379, respectively). However, there was a strong negative correlation between the left MPFC region and ESS scores (p = .032, r = −.398). The abnormal rsFC in subjects with OSAHS indicated the compensatory change of brain function, which possibly provides an innovative approach and perspective on understanding the neural mechanism alteration of OSAHS-related cognition.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  1. (1992) EEG arousals: scoring rules and examples: a preliminary report from the Sleep Disorders Atlas Task Force of the American Sleep Disorders Association. Sleep. 15(2):173–184

  2. Archbold KH, Borghesani PR, Mahurin RK, Kapur VK, Landis CA (2009) Neural activation patterns during working memory tasks and OSA disease severity: preliminary findings. J Clin Sleep Med 5(1):21–27

    Google Scholar 

  3. Ayalon L, Ancoli-Israel S, Drummond SP (2009) Altered brain activation during response inhibition in obstructive sleep apnea. J Sleep Res 18(2):L204–L208

    Article  Google Scholar 

  4. Ayalon L, Ancoli-lsrael S, Drummond SP (2009) Altered brain activation during response inhibition in obstructive sleep apnea. J Sleep Res 18(2):204–208

    Article  Google Scholar 

  5. Bagai K (2010) Obstructive sleep apnea, stroke, and cardiovascular diseases. Neurologist 16(6):329–339

    Article  Google Scholar 

  6. Buckner RL, Andrewa-Hanna JR, Schacter DL (2008) The brain's default network: anatomy, function, and relevance to disease. AnnNYAcad Sci 1124:1–38

    Article  Google Scholar 

  7. Cavanna AE, Trimble MR (2006) The precuneus: a review of its functional anatomy and behavioural correlates. Brain 129(pt3):564–583

    Article  Google Scholar 

  8. Chao-Gan Y, Yu-Feng Z (2010) DPARSF: a MATLAB toolbox for "pipeline" data analysis of resting-state MRI. Frontiers in systems neuroscience. 4:13

  9. Chen T et al (2016) The resting-state functional connectivity of the default mode networks in patients with obstructive sleep apnea-hypopnea syndrome. CNS Neurol Disord Drug Targets

  10. Cross RL, Kumar R, Macey PM et al (2008) Neural alterations and depressive symptoms in obstructive sleep apnea patients. Sleep 31(8):1103–1109

    Google Scholar 

  11. Dong ZC (2015) Detection of Alzheimer's disease and mild cognitive impairment based on structural volumetric MR images using 3D-DWT and WTA-KSVM trained by PSOTVAC. Biomedical Signal Processing and Control 21:58–73

    Article  Google Scholar 

  12. Emin Akkoyunlu M, Kart L (2013) Brain diffusion changes in obstructive sleep Apnoea syndrome. Respiration 86(5):414–420

    Article  Google Scholar 

  13. Ferini-Strambi L, Baietto C, Di Gioia MR et al (2003) Cognitive dysfunction in patients with obstructive sleep apnea (OSA): partial reversibility after continuous positive airway pressure (CPAP). Brain Res Bull 61(1):87–92

    Article  Google Scholar 

  14. Fletcher PC, Dolan RJ, Shallice T, Frith CD, Frackowiak RS, Friston KJ (1996) Is multivariate analysis of PET data more revealing than the univariate approach? Evidence from a study of episodic memory retrieval. Neuroimage 3(3Pt1):209–215

    Article  Google Scholar 

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

    Article  Google Scholar 

  16. Fox MD, Snyder AZ, Vincent JL, Corbetta M, van Essen DC, Raichle ME (2005) The human brain is intrinsically organized into dynamic, anticorrelated functional networks. Proc Natl Acad Sci U S A 102(27):9673–9678

    Article  Google Scholar 

  17. Fox MD, Zhang D, Snyder AZ, Raichle ME (2009) The global signal and observed anticorrelated resting state brain networks. J Neurophysiol 101(6):3270–3283

    Article  Google Scholar 

  18. Fransson P (2005) Spontaneous low-frequency BOLD signal fluctuations: an fMRI investigation of the resting-state default mode of brain function hypothesis. Hum Brain Mapp 26(1):15–29

    Article  Google Scholar 

  19. Galea M, Woodward M (2005) Mini-mental state examination (MMSE). Aust J Physiother 51(3):198

    Article  Google Scholar 

  20. Greicius MD, Srivastava G, Reiss AL, Menon V (2004) Default-mode network activity distinguishes Alzheimer’s disease from healthy aging: evidence from functional MRI. Proc Natl Acad Sci U S A 101(13):4637–4642

    Article  Google Scholar 

  21. Gusnard DA, Raichle ME (2001) Searching for a baseline:functional imaging and the resting human brain. Nat Rev Neurosci 2(10):685–694

    Article  Google Scholar 

  22. Ip MS, Lam B, Ng MM, Lam WK, Tsang KW, Lam KS (2002) Obstructive sleep apnea is independently associated with insulin resistance. Am J Respir Crit Care Med 165(5):670–676

    Article  Google Scholar 

  23. Ji G (2016) Preliminary research on abnormal brain detection by wavelet-energy and quantum-behaved PSO. Technol Health Care 24(s2):S641–S649

    Article  Google Scholar 

  24. Johns MW (1991) A new method for measuring daytime sleepiness: the Epworth sleepiness scale. Sleep 14(6):540–545

    Article  Google Scholar 

  25. Joo EY, Jeon S, Kim.ST, Lee.JM, Hong.SB (2013) Localized cortical thinning in patients with obstructive sleep apnea syndrome. Sleep 36(8):1153–1162.

    Article  Google Scholar 

  26. Kim HC, Young T, Matthews CG, Weber SM, Woodward AR, Palta M (1997) Sleep-disordered breathing and neuropsychological deficits: a population-based study. Am J Respir Crit Care Med 156(6):1813–1819

    Article  Google Scholar 

  27. Kumar R, Chavez AS, Macey PM, Woo MA, Yan-Go FL, Harper RM (2012) Altered global and regional brain mean diffusivity in patients with obstructive sleep. J Neurosci Res 90(10):2043–2052

    Article  Google Scholar 

  28. Li HJ, Zhang W, Nie S, Peng DC (2016) Abnormal resting-state functional connectivity within the default mode network subregions in male patients with obstructive sleep apnea. Neuropsychiatr Dis Treat 12:203–212

    Article  Google Scholar 

  29. Liu G (2016) Detection of Alzheimer’s disease by three-dimensional displacement field estimation in structural magnetic resonance imaging. J Alzheimers Dis 50(1):233–248

    MathSciNet  Google Scholar 

  30. Lu S, Yang M (2016) Dual-tree complex wavelet transform and twin support vector machine for pathological brain detection. Applied Science 6(6):169

    Article  Google Scholar 

  31. Lutherer LO, Williams JL (1986) Stimulating fastigial nucleus pressor region elicits patterned respiratory responses. Am J Physiol 250(3Pt2):R418–R426

    Google Scholar 

  32. Lutherer LO, Lutherer BC, Dormer KJ, Janssen HF, Barnes CD (1983) Bilateral lesions of the fastigial nucleus prevent the recovery of blood pressure following hypotension induced by hemorrhage or administration of endotoxin. Brain Res 269(2):251–257

    Article  Google Scholar 

  33. Macey PM, Henderson LA, Macey KE (2002) Brain morphology associated with obstructive sleep apnea. Am J Respir Crit Care Med 166(10):1382–1387

    Article  Google Scholar 

  34. Maddock R, Garrett A, Buonocore M (2001) Remembering familiar people: the posterior cingulate cortex and autobiographicalmemory retrieval. Neuroscience 104(3):667–676

    Article  Google Scholar 

  35. Naghavi HR, Nyberg L (2005) Common fronto-parietal activity in attention, memory, and consciousness: shared demands on integration? Conscious Cogn 14(2):390–425

    Article  Google Scholar 

  36. Park JG, Ramar K, Olson EJ et al (2011) Updates on definition, consequences, and management of obstructive sleep apnea. Mayo Clinic Proc 86(6):549–555

    Article  Google Scholar 

  37. Peng B (2016) Image processing methods to elucidate spatial characteristics of retinal microglia after optic nerve transection. Scientific Reports 6:21816

    Article  Google Scholar 

  38. 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 10:1819–1826

    Google Scholar 

  39. Prilipko O, Huynh N, Schwartz S et al (2011) Task positive and default mode networks during a parametric working memory task in obstructive sleep apnea patients and healthy controls. Sleep 34(3):293–301

    Article  Google Scholar 

  40. Punjabi NM (2008) The epidemiology of adult obstructive sleep apnea. Proc Am Thorac Soc 5(2):136–143

    Article  Google Scholar 

  41. Raichle ME (2010) Two views of brain function. Trends Cogn Sci 14(4):180–190

    Article  Google Scholar 

  42. Raichle ME, MacLeod AM, Snyder AZ et al (2001) A default mode of brain function. PNAS 98(2):676–682

    Article  Google Scholar 

  43. Redline S, Budhiraja R, Kapur V et al (2007) The scoring of respiratory events in sleep: reliability and validity. Journal of clinical sleep medicine: JCSM: official publication of the American Academy of Sleep Medicine 3(2):169–200

    Google Scholar 

  44. Sarchielli P, Presciutti O, Alberti A et al (2008) A 1H magnetic resonance spectroscopy study in patients with obstructive sleep apnea. Eur J Neurol 15(10):1058–1064

    Article  Google Scholar 

  45. Saunamäki T, Jehkonen M (2007) A review of executive functions in obstructive sleep apnea syndrome. Acta Neurol Scand 115(1):1–11

    Article  Google Scholar 

  46. Seneviratne U, Puvanendran K (2004) Excessive daytime sleepiness in obstructive sleep apnea: prevalence, severity, and predictors. Sleep Med 5(4):339–343

    Article  Google Scholar 

  47. Shen Y, Cao X, Tan T, Shan C, Wang Y, Pan J, He H, Yuan TF (2016) 10-Hz repetitive transcranial magnetic stimulation of the left dorsolateral prefrontal cortex reduces heroin cue craving in long-term addicts. Biol Psychiatry 80(3):e13–e14

    Article  Google Scholar 

  48. Shin MS, Park SY, Park SR, Seol SH, Kwon JS (2006) Clinical and empirical applications of the Rey-Osterrieth complex figure test. Nat Protoc 1(2):892–899

    Article  Google Scholar 

  49. Song XW, Dong ZY, Long XY et al (2011) REST: a toolkit for resting-state functional magnetic resonance imaging data processing. PLoS One 6(9):e25031

    Article  Google Scholar 

  50. Squire LR, Stark CE, Clark RE (2004) The medial temporal lobe. Annu Rev Neurosci 27:279–306

    Article  Google Scholar 

  51. Sun Y (2016) A multilayer perceptron based smart pathological brain detection system by fractional Fourier entropy. J Med Syst 40(7):173

    Article  Google Scholar 

  52. Supekar K, Uddin LQ, Prater K et al (2010) Development of functional and structural connectivity within the default mode network in young children. NeuroImage 52(1):290–301

    Article  Google Scholar 

  53. Thomas RJ, Rosen BR, Stern CE, Weiss JW, Kwong KK (2005) Functional imaging of working memory in obstructive sleep-disordered breathing. J Appl Physiol 98(6):2226–2234

    Article  Google Scholar 

  54. Tregear S, Reston J, Schoelles K, Phillips B (2009) Obstructive sleep apnea and risk of motor vehicle crash: systematic review and meta-analysis. J Clin Sleep Med 5(6):573–581

    Google Scholar 

  55. Uddin LQ et al (2009) Functional connectivity of default mode network components: correlation, anticorrelation, and causality. Hum Brain Mapp 30(2):625–637

    Article  Google Scholar 

  56. Wang Y, Shen Y, Cao X, Shan C, Pan J, He H, Ma Y, Yuan TF (2016) Transcranial direct current stimulation of the frontal-parietal-temporal area attenuates cue-induced craving for heroin. J Psychiatr Res 79:1–3

    Article  Google Scholar 

  57. Wilson CR, Gaffan D, Browning PG, Baxter MG (2010) Functional localiza-tion within the prefrontal cortex: missing the forest for the trees? Trends Neurosci 33(12):533–540

    Article  Google Scholar 

  58. Xu F, Frazier DT (1997) Respiratory-related neurons of the fastigial nucleus in response to chemical and mechanical challenges. Journal of applied physiology (Bethesda, Md.: 1985) 82(4):1177–1184

    Article  Google Scholar 

  59. Yeon JE, Suk TW, Joo LM et al (2010) Reduced brain gray matter concentration in patients with obstructive sleep apnea syndrome. Sleep 33(2):235–241

    Article  Google Scholar 

  60. Yuan TF (2015) Detection of subjects and brain regions related to Alzheimer’s disease using 3D MRI scans based on eigenbrain and machine learning. Front Comput Neurosci 9(66):1–15

    Google Scholar 

  61. Zang YF, Jiang TZ, Lu YL et al (2004) Regional homogeneity approach to fMRI data analysis. Neuro Image 22(1):394–400

    Google Scholar 

  62. Zhang Q, Wang D, Qin W et al (2013) Altered resting-state brain activity in obstructive sleep apnea. Sleep 36(5):651–659

    Article  Google Scholar 

  63. Zhao XH, Wang PJ, Li CB et al (2007) Altered default mode network activity in patient with anxiety disorders:all fMRI study. Eur J Radiol 63(3):373–378

    Article  Google Scholar 

  64. Zhou XX, Wu L (2016) Comparison of machine learning methods for stationary wavelet entropy-based multiple sclerosis detection: decision tree, k-nearest neighbors, and support vector machine. SIMULATION 92(9):861–871

    Article  Google Scholar 

Download references

Acknowledgments

This paper was supported by the Clinical Medical Science and Technology Special Project of Jiangsu,China(NO. BL2013029) and was partly supported by the Maternity and Child Care Project, Jiangsu Province,China(F201554), Science and Technology Development Project, Nanjing, China (2015sc511023) and Six Talent Peaks Project in Jiangsu Province (WSN-192),China.

Author information

Authors and Affiliations

  1. Department of Radiology, Zhongda Hospital, SEU (Southeast University), Nanjing, 210009, China

    Ting Chen, Ya-Qing Huang, Hui-Xin Zhang & Bin Liu

  2. Medical School of SEU, Nanjing, 210009, China

    Yu -Ting Liu

  3. Department of Radiology, Children’s Hospital, Nanjing Medical University, Nanjing, 210008, China

    Hui-Jun Li & Ming Yang

  4. Department of Otolaryngology-Head and Neck Surgery, Zhongda Hospital, SEU, Nanjing, 210009, China

    Lian Zhang & Zhi-chun Huang

Authors
  1. Yu -Ting Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Hui-Jun Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ting Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ya-Qing Huang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Lian Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Hui-Xin Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Zhi-chun Huang
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Bin Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Ming Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Bin Liu or Ming Yang.

Additional information

Yu-Ting Liu and Hui-Jun Li contributed equally to this work.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Liu, Y.T., Li, HJ., Chen, T. et al. Aberrant functional connectivity in patients with obstructive sleep apnea-hypopnea syndrome: a resting-state functional MRI study. Multimed Tools Appl 77, 4065–4079 (2018). https://doi.org/10.1007/s11042-017-4670-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11042-017-4670-5

Keywords

Search

Navigation