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Regional homogeneity changes in patients with primary insomnia

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Abstract

Purpose

The study aimed to explore the regional spontaneous activity changes in primary insomnia (PI) patients.

Materials and methods

Based on the resting-state fMRI datasets acquired from 59 PI patients and 47 healthy controls, a two-sample t-test was performed on individual normalized regional homogeneity (ReHo) maps. Relationships between abnormal ReHo values and the Pittsburgh Sleep Quality Index (PSQI), the self-rating anxiety scale (SAS) and the self-rating depression scale (SDS) were investigated with Pearson correlation analysis.

Results

In PI patients, we found increased ReHo in the left insula, right anterior cingulate gyrus, bilateral precentral gyrus and left cuneus, as well as decreased ReHo in the right middle cingulate cortex and left fusiform (p < 0.05, AlphaSim-corrected). We also found a significant positive correlation between increased ReHo in the left insula and SAS scores, decreased ReHo in the right middle cingulated cortex and SDS, SAS scores as well as a negative correlation between increased ReHo in the right precentral gyrus and SDS scores (p < 0.05).

Conclusions

Our study found abnormal spontaneous activities in multiple brain regions, especially in emotion-related areas in PI patients. Alterative activities in these regions might contribute to an understanding the intrinsic functional architecture of insomnia and its clinical features.

Key Points

Regional spontaneous activity changes were detected in PI patients.

Decreased or increased ReHo of some regions was identified in PI patients.

Significant correlations between mean ReHo and SDS scores were found.

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References

  1. Altena E, Van Der Werf YD, Sanz-Arigita EJ, Voorn TA, Rombouts SA, Kuijer JP, Van Someren EJ (2008) Prefrontal hypoactivation and recovery in insomnia. Sleep 31:1271–1276

    PubMed  PubMed Central  Google Scholar 

  2. Association AP (1994) Diagnostic and statistical manual of mental disorders, 4th edn. American Psychiatric Association, Washington, DC

    Google Scholar 

  3. Baglioni C, Spiegelhalder K, Lombardo C, Riemann D (2010) Sleep and emotions: a focus on insomnia. Sleep Med Rev 14:227–238

    Article  PubMed  Google Scholar 

  4. Biswal B, Yetkin FZ, Haughton VM, Hyde JS (1995) Functional connectivity in the motor cortex of resting human brain using echo-planar MRI. Magn Reson Med 34:537–541

    Article  CAS  PubMed  Google Scholar 

  5. Cano G, Mochizuki T, Saper CB (2008) Neural circuitry of stress-induced insomnia in rats. J Neurosci 28:10167–10184

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Chen MC, Chang C, Glover GH, Gotlib IH (2014) Increased insula coactivation with salience networks in insomnia. Biol Psychol 97:1–8

    Article  PubMed  PubMed Central  Google Scholar 

  7. Cheung JM, Bartlett DJ, Armour CL, Saini B (2013) The insomnia patient perspective, a narrative review. Behav Sleep Med 11:369–389

    Article  PubMed  Google Scholar 

  8. Dai XJ, Peng DC, Gong HH, Wan AL, Nie X, Li HJ, Wang YX (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 10:2163–2175

    Article  PubMed  PubMed Central  Google Scholar 

  9. Davidson RJ, Irwin W, Anderle MJ, Kalin NH (2003) The neural substrates of affective processing in depressed patients treated with venlafaxine. Am J Psychiatry 160:64–75

    Article  PubMed  Google Scholar 

  10. Fair DA, Nigg JT, Iyer S, Bathula D, Mills KL, Dosenbach NU, Schlaggar BL, Mennes M, Gutman D, Bangaru S, Buitelaar JK, Dickstein DP, Di Martino A, Kennedy DN, Kelly C, Luna B, Schweitzer JB, Velanova K, Wang YF, Mostofsky S, Castellanos FX, Milham MP (2012) Distinct neural signatures detected for ADHD subtypes after controlling for micro-movements in resting state functional connectivity MRI data. Front Syst Neurosci 6:80

    PubMed  PubMed Central  Google Scholar 

  11. Groenewold NA, Opmeer EM, de Jonge P, Aleman A, Costafreda SG (2013) Emotional valence modulates brain functional abnormalities in depression: evidence from a meta-analysis of fMRI studies. Neurosci Biobehav Rev 37:152–163

    Article  PubMed  Google Scholar 

  12. Haldane M, Cunningham G, Androutsos C, Frangou S (2008) Structural brain correlates of response inhibition in Bipolar Disorder I. J Psychopharmacol 22:138–143

    Article  PubMed  Google Scholar 

  13. Huang Z, Liang P, Jia X, Zhan S, Li N, Ding Y, Lu J, Wang Y, Li K (2012) Abnormal amygdala connectivity in patients with primary insomnia: evidence from resting state fMRI. Eur J Radiol 81:1288–1295

    Article  PubMed  Google Scholar 

  14. Jiang GH, Qiu YW, Zhang XL, Han LJ, Lv XF, Li LM, Lin CL, Zhuo FZ, Hu SY, Tian JZ (2011) Amplitude low-frequency oscillation abnormalities in the heroin users: a resting state fMRI study. Neuroimage 57:149–154

    Article  PubMed  Google Scholar 

  15. Killgore WD, Schwab ZJ, Kipman M, Deldonno SR, Weber M (2013) Insomnia-related complaints correlate with functional connectivity between sensory-motor regions. Neuroreport 24:233–240

    Article  PubMed  Google Scholar 

  16. Krausz Y, Freedman N, Lester H, Barkai G, Levin T, Bocher M, Chisin R, Lerer B, Bonne O (2007) Brain SPECT study of common ground between hypothyroidism and depression. Int J Neuropsychopharmacol 10:99–106

    Article  PubMed  Google Scholar 

  17. Li Y, Wang E, Zhang H, Dou S, Liu L, Tong L, Lei Y, Wang M, Xu J, Shi D, Zhang Q (2014) Functional connectivity changes between parietal and prefrontal cortices in primary insomnia patients: evidence from resting-state fMRI. Eur J Med Res 19:32

    Article  PubMed  PubMed Central  Google Scholar 

  18. Liu Z, Xu C, Xu Y, Wang Y, Zhao B, Lv Y, Cao X, Zhang K, Du C (2010) Decreased regional homogeneity in insula and cerebellum: a resting-state fMRI study in patients with major depression and subjects at high risk for major depression. Psychiatry Res 182:211–215

    Article  PubMed  Google Scholar 

  19. Maes J, Verbraecken J, Willemen M, De Volder I, van Gastel A, Michiels N, Verbeek I, Vandekerckhove M, Wuyts J, Haex B, Willemen T, Exadaktylos V, Bulckaert A, Cluydts R (2014) Sleep misperception, EEG characteristics and autonomic nervous system activity in primary insomnia: a retrospective study on polysomnographic data. Int J Psychophysiol 91:163–171

    Article  CAS  PubMed  Google Scholar 

  20. Ni L, Qi R, Zhang LJ, Zhong J, Zheng G, Zhang Z, Zhong Y, Xu Q, Liao W, Jiao Q, Wu X, Fan X, Lu GM (2012) Altered regional homogeneity in the development of minimal hepatic encephalopathy: a resting-state functional MRI study. PLoS ONE 7:e42016

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Nofzinger EA, Buysse DJ, Germain A, Price JC, Miewald JM, Kupfer DJ (2004) Functional neuroimaging evidence for hyperarousal in insomnia. Am J Psychiatry 161:2126–2128

    Article  PubMed  Google Scholar 

  22. Ogawa S, Lee TM, Kay AR, Tank DW (1990) Brain magnetic resonance imaging with contrast dependent on blood oxygenation. Proc Natl Acad Sci U S A 87:9868–9872

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Paulus MP, Stein MB (2006) An insular view of anxiety. Biol Psychiatry 60:383–387

    Article  PubMed  Google Scholar 

  24. Perrier J, Clochon P, Bertran F, Couque C, Bulla J, Denise P, Bocca ML (2015) Specific EEG sleep pattern in the prefrontal cortex in primary insomnia. PLoS ONE 10:e116864

    Article  Google Scholar 

  25. Phan KL, Wager T, Taylor SF, Liberzon I (2002) Functional neuroanatomy of emotion: a meta-analysis of emotion activation studies in PET and fMRI. Neuroimage 16:331–348

    Article  PubMed  Google Scholar 

  26. Pourtois G, Vocat R, N'Diaye K, Spinelli L, Seeck M, Vuilleumier P (2010) Errors recruit both cognitive and emotional monitoring systems: simultaneous intracranial recordings in the dorsal anterior cingulate gyrus and amygdala combined with fMRI. Neuropsychologia 48:1144–1159

    Article  PubMed  Google Scholar 

  27. Riemann D, Kloepfer C, Berger M (2009) Functional and structural brain alterations in insomnia: implications for pathophysiology. Eur J Neurosci 29:1754–1760

    Article  CAS  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  29. Shackman AJ, Salomons TV, Slagter HA, Fox AS, Winter JJ, Davidson RJ (2011) The integration of negative affect, pain and cognitive control in the cingulate cortex. Nat Rev Neurosci 12:154–167

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Simmons AN, Stein MB, Strigo IA, Arce E, Hitchcock C, Paulus MP (2011) Anxiety positive subjects show altered processing in the anterior insula during anticipation of negative stimuli. Hum Brain Mapp 32:1836–1846

    Article  PubMed  PubMed Central  Google Scholar 

  31. Spiegelhalder K, Regen W, Feige B, Holz J, Piosczyk H, Baglioni C, Riemann D, Nissen C (2012) Increased EEG sigma and beta power during NREM sleep in primary insomnia. Biol Psychol 91:329–333

    Article  PubMed  Google Scholar 

  32. Stoffers D, Moens S, Benjamins J, van Tol MJ, Penninx BW, Veltman DJ, Van der Wee NJ, Van Someren EJ (2012) Orbitofrontal gray matter relates to early morning awakening: a neural correlate of insomnia complaints? Front Neurol 3:105

    Article  PubMed  PubMed Central  Google Scholar 

  33. Taylor DJ, Lichstein KL, Durrence HH (2003) Insomnia as a health risk factor. Behav Sleep Med 1:227–247

    Article  PubMed  Google Scholar 

  34. Tsuno N, Besset A, Ritchie K (2005) Sleep and depression. J Clin Psychiatry 66:1254–1269

    Article  PubMed  Google Scholar 

  35. Tu PC, Hsieh JC, Li CT, Bai YM, Su TP (2012) Cortico-striatal disconnection within the cingulo-opercular network in schizophrenia revealed by intrinsic functional connectivity analysis: a resting fMRI study. Neuroimage 59:238–247

    Article  PubMed  Google Scholar 

  36. Wu QZ, Li DM, Kuang WH, Zhang TJ, Lui S, Huang XQ, Chan RC, Kemp GJ, Gong QY (2011) Abnormal regional spontaneous neural activity in treatment-refractory depression revealed by resting-state fMRI. Hum Brain Mapp 32:1290–1299

    Article  PubMed  Google Scholar 

  37. Wu T, Long X, Zang Y, Wang L, Hallett M, Li K, Chan P (2009) Regional homogeneity changes in patients with Parkinson's disease. Hum Brain Mapp 30:1502–1510

    Article  PubMed  Google Scholar 

  38. Zang Y, Jiang T, Lu Y, He Y, Tian L (2004) Regional homogeneity approach to fMRI data analysis. Neuroimage 22:394–400

    Article  PubMed  Google Scholar 

  39. Zhang X, Yao S, Zhu X, Wang X, Zhu X, Zhong M (2012) Gray matter volume abnormalities in individuals with cognitive vulnerability to depression: a voxel-based morphometry study. J Affect Disord 136:443–452

    Article  PubMed  Google Scholar 

  40. Zhong Y, Lu G, Zhang Z, Jiao Q, Li K, Liu Y (2011) Altered regional synchronization in epileptic patients with generalized tonic-clonic seizures. Epilepsy Res 97:83–91

    Article  PubMed  Google Scholar 

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Acknowledgments

The authors would like to express their appreciation to Queenie Chan and all the reviewers who improved the article greatly.

The scientific guarantor of this publication is Guihua Jiang. The authors of this manuscript declare no relationships with any companies whose products or services may be related to the subject matter of the article.

This study was funded by the National Natural Science Foundation of China (Grant No.:81471639) and The Science and Technology Planning Project of Guangdong Province, China (Grant No.: 2011B031800044, 2012B031800170, 2012A030400019).

Jinwu Liu kindly provided statistical advice for this manuscript. Institutional review board approval was obtained. Written informed consent was obtained from all subjects (patients) in this study.

Some study subjects or cohorts have been previously reported in the fMRI studies of primary insomnia [17]. Methodology: prospective, case-control study, performed at one institution.

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Correspondence to Guihua Jiang.

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Tianyue Wang and Shumei Li contributed equally to this work.

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Wang, T., Li, S., Jiang, G. et al. Regional homogeneity changes in patients with primary insomnia. Eur Radiol 26, 1292–1300 (2016). https://doi.org/10.1007/s00330-015-3960-4

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