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Original Article
Abnormal brain network topology during non-rapid eye movement sleep and its correlation with cognitive behavioral abnormalities in narcolepsy type 1
ZHU Xiaoyu  NI Kunlin  TAN Huiwen  LIU Yishu  ZENG Yin  GUO Qiyong  XIAO Li  YU Bing 

Cite this article as: Zhu XY, Ni KL, Tan HW, et al. Abnormal brain network topology during non-rapid eye movement sleep and its correlation with cognitive behavioral abnormalities in narcolepsy type 1[J]. Chin J Magn Reson Imaging, 2021, 12(6): 57-61, 96. DOI:10.12015/issn.1674-8034.2021.06.011.


[Abstract] Objective Simultaneous electroencephalography (EEG) and functional magnetic resonance imaging (fMRI) were applied to investigate the abnormalities in the topological characteristics of functional brain networks during non-rapid eye movement (NREM) sleep. And we investigated its relationship with cognitive abnormalities in patients with narcolepsy type 1 (NT1) disorder in the current study. Materials andMethods The Beijing version of the Montreal Cognitive Assessment (MoCA-BJ) and EEG-fMRI were applied in 25 patients with NT1 and 25 age-matched healthy controls. All subjects participated in a nocturnal video polysomnography (PSG) study, and total sleep time (TST), percentage of TST (TST%) for each sleep stage and arousal index were calculated. The Epworth Sleepiness Score (ESS) was used to measure the degree of daytime sleepiness. The EEG-fMRI study was performed simultaneously using a 3.0 T MRI system and a 32-channel MRI-compatible EEG system during sleep. Visual scoring of EEG data was used for sleep staging. Cognitive function was assessed for all subjects using the MoCA-BJ. The fMRI data were applied to establish a whole-brain functional connectivity network for all subjects, and the topological characteristics of the whole-brain functional network were analyzed using a graph-theoretic approach. The topological parameters were compared between groups. Lastly, the correlation between topological parameters and the assessment scale using Montreal Cognition was analyzed.Results The MoCA-BJ scores were lower in patients with NT1 than in normal controls. Whole-brain global efficiency during stage N2 sleep in patients with NT1 displayed significantly lower small-world properties than in normal controls. Whole-brain functional network global efficiency in patients with NT1 was significantly correlated with MoCA-BJ scores (r=-0.589, P=0.002).Conclusions The global efficiency of the functional brain network during stage N2 sleep in patients with NT1 and the correspondingly reduced small-world attributes were associated with cognitive impairment.
[Keywords] magnetic resonance imaging;cognitive dysfunction;graph theory analysis;narcolepsy type 1;functional connectivity;sleep;montreal cognitive assessment Beijing edition

ZHU Xiaoyu1   NI Kunlin1   TAN Huiwen2   LIU Yishu2   ZENG Yin2   GUO Qiyong1   XIAO Li2, 3   YU Bing1*  

1 Department of Radiology, Shengjing Hospital of China Medical University, Shenyang 110004, China

2 Department of Pulmonary and Critical Care Medicine, Shengjing Hospital of China Medical University, Shenyang 110004, China

3 Sleep Medicine Center, Shengjing Hospital of China Medical University, Shenyang 110004, China

Yu B, E-mail: dr.yubing@vip.163.com

Conflicts of interest   None.

This work was part of Key Research and Development Program Project Fund of Liaoning Province (No. 2019JH8/10300006).
Received  2020-12-18
Accepted  2021-03-05
DOI: 10.12015/issn.1674-8034.2021.06.011
Cite this article as: Zhu XY, Ni KL, Tan HW, et al. Abnormal brain network topology during non-rapid eye movement sleep and its correlation with cognitive behavioral abnormalities in narcolepsy type 1[J]. Chin J Magn Reson Imaging, 2021, 12(6): 57-61, 96. DOI:10.12015/issn.1674-8034.2021.06.011.

1
Mahoney CE, Cogswell A, Koralnik IJ, et al. The neurobiological basis of narcolepsy[J]. Nat Rev Neurosci, 2019, 20(2): 83-93. DOI: 10.1038/s41583-018-0097-x.
2
Sieminski M, Chwojnicki K, Sarkanen T, et al. The relationship between orexin levels and blood pressure changes in patients with narcolepsy[J]. PLoS One, 2017, 12(10): e0185975. DOI: 10.1371/journal.pone.0185975.
3
Ponz A, Khatami R, Poryazova R, et al. Reduced amygdala activity during aversive conditioning in human narcolepsy[J]. Ann Neurol, 2010, 67(3): 394-398. DOI: 10.1002/ana.21881.
4
Zamarian L, Högl B, Delazer M, et al. Subjective deficits of attention, cognition and depression in patients with narcolepsy[J]. Sleep Med, 2015, 16(1): 45-51. DOI: 10.1016/j.sleep.2014.07.025.
5
Bayard S, Abril B, Yu H, et al. Decision making in narcolepsy with cataplexy[J]. Sleep, 2011, 34(1): 99-104. DOI: 10.1093/sleep/34.1.99.
6
Gool JK, van der Werf YD, Lammers GJ, et al. The sustained attention to response task shows lower cingulo-opercular and frontoparietal activity in people with narcolepsy type 1: An fMRI study on the neural regulation of attention[J]. Brain Sci, 2020, 10(7): 419. DOI: 10.3390/brainsci10070419.
7
Joo EY, Kim SH, Kim ST, et al. Hippocampal volume and memory in narcoleptics with cataplexy[J]. Sleep Med, 2012, 13(4): 396-401. DOI: 10.1016/j.sleep.2011.09.017.
8
Kim H, Suh S, Joo EY, et al. Morphological alterations in amygdalo-hippocampal substructures in narcolepsy patients with cataplexy[J]. Brain Imaging Behav, 2016, 10(4): 984-994. DOI: 10.1007/s11682-015-9450-0.
9
Křečková M, Kemlink D, Šonka K, et al. Anterior hippocampus volume loss in narcolepsy with cataplexy[J]. J Sleep Res, 2019, 28(4): e12785. DOI: 10.1111/jsr.12785.
10
Schwartz S, Ponz A, Poryazova R, et al. Abnormal activity in hypothalamus and amygdala during humour processing in human narcolepsy with cataplexy[J]. Brain, 2008, 131(Pt 2): 514-522. DOI: 10.1093/brain/awm292.
11
Joo EY, Jeon S, Lee M, et al. Analysis of cortical thickness in narcolepsy patients with cataplexy[J]. Sleep, 2011, 34(10): 1357-1364. DOI: 10.5665/SLEEP.1278.
12
Park YK, Kwon OH, Joo EY, et al. White matter alterations in narcolepsy patients with cataplexy: tract-based spatial statistics[J]. J Sleep Res, 2016, 25(2): 181-189. DOI: 10.1111/jsr.12366.
13
Tezer FI, Erdal A, Gumusyayla S, et al. Differences in diffusion tensor imaging changes between narcolepsy with and without cataplexy[J]. Sleep Med, 2018, 52(2018): 128-133. DOI: 10.1016/j.sleep.2018.08.022.
14
Juvodden HT, Alnæs D, Lund MJ, et al. Widespread white matter changes in post-H1N1 patients with narcolepsy type 1 and first-degree relatives[J]. Sleep, 2018, 41(10): 1-11. DOI: 10.1093/sleep/zsy145.
15
Rieger M, Mayer G, Gauggel S. Attention deficits in patients with narcolepsy[J]. Sleep, 2003, 26(1): 36-43. DOI: 10.1093/sleep/26.1.36.
16
Xiao F, Lu C, Zhao D, et al. Independent component analysis and graph theoretical analysis in patients with narcolepsy[J]. Neurosci Bull, 2019, 35(4): 743-755. DOI: 10.1007/s12264-018-0307-6.
17
van Holst RJ, Janssen LK, van Mierlo P, et al. Enhanced food-related responses in the ventral medial prefrontal cortex in narcolepsy type 1[J]. Sci Rep, 2018, 8(1): 16391. DOI: 10.1038/s41598-018-34647-6.
18
Ponz A, Khatami R, Poryazova R, et al. Abnormal activity in reward brain circuits in human narcolepsy with cataplexy[J]. Ann Neurol, 2010, 67(2): 190-200. DOI: 10.1002/ana.21825.
19
Meletti S, Vaudano AE, Pizza F, et al. The brain correlates of laugh and cataplexy in childhood narcolepsy[J]. J Neurosci, 2015, 35(33): 11583-11594. DOI: 10.1523/JNEUROSCI.0840-15.2015.
20
Juvodden HT, Alnæs D, Lund MJ, et al. Hypocretin-deficient narcolepsy patients have abnormal brain activation during humor processing[J]. Sleep, 2019, 42(7): 82. DOI: 10.1093/sleep/zsz082.
21
Vaudano AE, Pizza F, Talami F, et al. The neuronal network of laughing in young patients with untreated narcolepsy[J]. Neurology, 2019, 92(5): 1-12. DOI: 10.1212/WNL.0000000000006853.
22
Reiss AL, Hoeft F, Tenforde AS, et al. Anomalous hypothalamic responses to humor in cataplexy[J]. PLoS One, 2008, 3(5): e2225. DOI: 10.1371/journal.pone.0002225.
23
Fulong X, Karen S, Chao L, et al. Resting-state brain network topological properties and the correlation with neuropsychological assessment in adolescent narcolepsy[J]. Sleep, 2020, 43(8): 18. DOI: 10.1093/sleep/zsaa018.
24
Xu J, Pan Y, Zhou S, et al. EEG microstates are correlated with brain functional networks during slow-wave sleep[J]. Neuroimage, 2020, 215: 116786. DOI: 10.1016/j.neuroimage.2020.116786.
25
Wirsich J, Jorge J, Iannotti GR, et al. The relationship between EEG and fMRI connectomes is reproducible across simultaneous EEG-fMRI studies from 1.5 T to 7 T[J]. Neuroimage, 2021, 231: 117864.
26
Billings ME, Rosen CL, Rosen CL, et al. Psychometric performance and responsiveness of the functional outcomes of sleep questionnaire and sleep apnea quality of life instrument in a randomized trial: the HomePAP study[J]. Sleep, 2014, 37(12): 2017-2024. DOI: 10.5665/sleep.4262.
27
Berry RB, Budhiraja R, Gottlieb DJ, et al. Rules for scoring respiratory events in sleep: update of the 2007 AASM Manual for the Scoring of Sleep and Associated Events. Deliberations of the Sleep Apnea Definitions Task Force of the American Academy of Sleep Medicine[J]. J Clin Sleep Med, 2012, 8(5): 597-619. DOI: 10.5664/jcsm.2172.
28
Littner MR, Kushida C, Wise M, et al. Practice parameters for clinical use of the multiple sleep latency test and the maintenance of wakefulness test[J]. Sleep, 2005, 28(1): 113-121. DOI: 10.1093/sleep/28.1.113.
29
Huang L, Chen KL, Lin BY, et al. Chinese version of montreal cognitive assessment basic for discrimination among different severities of Alzheimer's disease[J]. Neuropsychiatr Dis Treat, 2018, 14: 2133-2140. DOI: 10.2147/NDT.S174293.
30
Zhu Y, Ren F, Zhu Y, et al. Gradually increased interhemispheric functional connectivity during one night of sleep deprivation[J]. Nat Sci Sleep, 2020, 12: 1067-1074. DOI: 10.2147/NSS.S270009.
31
Ipiña IP, Kehoe PD, Kringelbach M, et al. Modeling regional changes in dynamic stability during sleep and wakefulness[J]. NeuroImage, 2020, 215: 116833. DOI: 10.1016/j.neuroimage.2020.116833.
32
Yan CG, Wang XD, Zuo XN, et al. DPABI: Data processing & analysis for (Resting-State) brain imaging[J]. Neuroinformatics, 2016, 14(3): 339-351. DOI: 10.1007/s12021-016-9299-4.
33
Xin Z, Chen X, Zhang Q, et al. Alteration in topological properties of brain functional network after 2-year high altitude exposure: A panel study[J]. Brain Behav, 2020, 10(10): e01656.
34
Liu J, Tan G, Lan W, et al. Identification of early mild cognitive impairment using multi-modal data and graph convolutional networks[J]. BMC Bioinformatics, 2020, 21(Suppl 6): 123. DOI: 10.1186/s12859-020-3437-6.
35
Chen LT, Fan XL, Li HJ, et al. Disrupted small-world brain functional network topology in male patients with severe obstructive sleep apnea revealed by resting-state fMRI[J]. Neuropsychiatr Dis Treat, 2017, 13: 1471-1482.
36
Bassett DS, Bullmore ET. Small-world brain networks revisited[J]. Neuroscientist, 2017, 23(5): 499-516. DOI: 10.1177/1073858416667720.
37
Li J, Xu Y, Dong XS, et al. Changes of sleep architecture in patients with narcolepsy[J]. Natl Med J China, 2007, 87(9): 619-621. DOI: 10.3760/j:issn:0376-2491.2007.09.011.
38
Drissi NM, Szakács A, Witt ST, et al. Altered brain microstate dynamics in adolescents with narcolepsy[J]. Front Hum Neurosci, 2016, 10: 369. DOI: 10.3389/fnhum.2016.00369.
39
Seitzman BA, Snyder AZ, Leuthardt EC, et al. The state of resting state networks[J]. Top Magn Reson Imaging, 2019, 28(4): 189-196. DOI: 10.1097/RMR.0000000000000214.

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