nach oben

Erschienen in:

29.06.2022 | Original Article

Excessive Daytime Sleepiness in Parkinson’s Disease is Related to Functional Abnormalities in the Left Angular Gyrus

verfasst von: Jin Hua Zheng, Jian Jun Ma, Wen Hua Sun, Zhi Dong Wang, Qing Qing Chang, Lin Rui Dong, Xiao Xue Shi, Ming Jian Li

Erschienen in: Clinical Neuroradiology | Ausgabe 1/2023

Einloggen, um Zugang zu erhalten

Abstract

Purpose

Excessive daytime sleepiness (EDS) is a common non-motor symptom in Parkinson’s disease (PD), but its neuropathology remains elusive. Our goal is to explore the potential neural substrates of EDS in a large sample of individuals with PD.

Methods

We recruited 48 PD patients with and 87 PD patients without EDS. We used resting-state functional magnetic resonance imaging to compare amplitudes of low-frequency fluctuations (ALFF) between the two groups. We also explored functional connectivity (FC) between the entire brain and regions where ALFF differed between the two groups as well as FC between selected regions of interest. Age, Part III of the Movement Disorder Society Unified Parkinson’s Disease Rating Scale (MDS-UPDRS-III) score and use of dopamine receptor agonists were treated as covariates in the comparisons.

Results

EDS was associated with significantly lower ALFF in the left angular gyrus, and ALFF in this region correlated negatively with score on the Epworth Sleepiness Scale in patients with PD. EDS was also associated with significantly lower FC between the left angular gyrus and right cerebellum, based on seed-to-voxel and inter-ROI analyses.

Conclusion

Our results suggest that EDS in PD patients is associated with reduced spontaneous neural activity in the left angular gyrus and with reduced FC between the left angular gyrus and cerebellum. These findings may help understand and treat EDS in PD.

Knie B, Mitra MT, Logishetty K, Chaudhuri KR. Excessive daytime sleepiness in patients with Parkinson’s disease. CNS Drugs. 2011;25:203–12.CrossRefPubMed

Frucht S, Rogers JD, Greene PE, Gordon MF, Fahn S. Falling asleep at the wheel: motor vehicle mishaps in persons taking pramipexole and ropinirole. Neurology. 1999;52:1908–10.CrossRefPubMed

Yoo SW, Kim JS, Oh YS, Ryu DW, Lee KS. Excessive daytime sleepiness and its impact on quality of life in de novo Parkinson’s disease. Neurol Sci. 2019;40:1151–6.CrossRefPubMed

Chahine LM, Amara AW, Videnovic A. A systematic review of the literature on disorders of sleep and wakefulness in Parkinson’s disease from 2005 to 2015. Sleep Med Rev. 2017;35:33–50.CrossRefPubMed

Adler CH, Thorpy MJ. Sleep issues in Parkinson’s disease. Neurology. 2005;64:S12–20.CrossRefPubMed

Happe S, Baier PC, Helmschmied K, Meller J, Tatsch K, Paulus W. Association of daytime sleepiness with nigrostriatal dopaminergic degeneration in early Parkinson’s disease. J Neurol. 2007;254:1037–43.CrossRefPubMed

Pagano G, Molloy S, Bain PG, Rabiner EA, Chaudhuri KR, Brooks DJ, Pavese N. Sleep problems and hypothalamic dopamine D3 receptor availability in Parkinson disease. Neurology. 2016;87:2451–6.CrossRefPubMedPubMedCentral

Yoo SW, Oh YS, Ryu DW, Lee KS, Lyoo CH, Kim JS. Low thalamic monoamine transporter availability is related to excessive daytime sleepiness in early Parkinson’s disease. Neurol Sci. 2020;41:1081–7.CrossRefPubMed

Wen MC, Ng SY, Heng HS, Chao YX, Chan LL, Tan EK, Tan LC. Neural substrates of excessive daytime sleepiness in early drug naive Parkinson’s disease: a resting state functional MRI study. Parkinsonism Relat Disord. 2016;24:63–8.CrossRefPubMed

10.

Wang X, Wang M, Yuan Y, Li J, Shen Y, Zhang K. Altered amplitude of low-frequency fluctuations and functional connectivity in excessive daytime sleepiness in Parkinson disease. Front Neurosci. 2020;14:29.CrossRefPubMedPubMedCentral

11.

Zuo XN, Di Martino A, Kelly C, Shehzad ZE, Gee DG, Klein DF, Castellanos FX, Biswal BB, Milham MP. The oscillating brain: complex and reliable. Neuroimage. 2010;49:1432–45.CrossRefPubMed

12.

Gorges M, Müller HP, Lulé D, Ludolph AC, Pinkhardt EH, Kassubek J. Functional connectivity within the default mode network is associated with saccadic accuracy in Parkinson’s disease: a resting-state FMRI and videooculographic study. Brain Connect. 2013;3:265-72.CrossRefPubMed

13.

Postuma RB, Berg D, Stern M, Poewe W, Olanow CW, Oertel W, Obeso J, Marek K, Litvan I, Lang AE, Halliday G, Goetz CG, Gasser T, Dubois B, Chan P, Bloem BR, Adler CH, Deuschl G. MDS clinical diagnostic criteria for Parkinson’s disease. Mov Disord. 2015;30:1591–601.CrossRefPubMed

14.

Crum RM, Anthony JC, Bassett SS, Folstein MF. Population-based norms for the Mini-Mental State Examination by age and educational level. JAMA. 1993;269:2386–91.CrossRefPubMed

15.

Johns MW. A new method for measuring daytime sleepiness: the Epworth sleepiness scale. Sleep. 1991;14:540–5.CrossRefPubMed

16.

Goetz CG, Tilley BC, Shaftman SR, Stebbins GT, Fahn S, Martinez-Martin P, Poewe W, Sampaio C, Stern MB, Dodel R, Dubois B, Holloway R, Jankovic J, Kulisevsky J, Lang AE, Lees A, Leurgans S, LeWitt PA, Nyenhuis D, Olanow CW, Rascol O, Schrag A, Teresi JA, van Hilten JJ, LaPelle N; Movement Disorder Society UPDRS Revision Task Force. Movement Disorder Society-sponsored revision of the Unified Parkinson’s Disease Rating Scale (MDS-UPDRS): scale presentation and clinimetric testing results. Mov Disord. 2008;23:2129–70.CrossRefPubMed

17.

Jankovic J, McDermott M, Carter J, Gauthier S, Goetz C, Golbe L, Huber S, Koller W, Olanow C, Shoulson I, et al. Variable expression of Parkinson’s disease: a base-line analysis of the DATATOP cohort. The Parkinson Study Group. Neurology. 1990;40:1529–34.CrossRefPubMed

18.

Tomlinson CL, Stowe R, Patel S, Rick C, Gray R, Clarke CE. Systematic review of levodopa dose equivalency reporting in Parkinson’s disease. Mov Disord. 2010;25:2649–53.CrossRefPubMed

19.

Whitfield-Gabrieli S, Nieto-Castanon A. Conn: a functional connectivity toolbox for correlated and anticorrelated brain networks. Brain Connect. 2012;2:125–41.CrossRefPubMed

20.

Yan CG, Wang XD, Zuo XN, Zang YF. DPABI: Data Processing & Analysis for (Resting-State) Brain Imaging. Neuroinformatics. 2016;14:339–51.CrossRef

21.

Raichle ME, MacLeod AM, Snyder AZ, Powers WJ, Gusnard DA, Shulman GL. A default mode of brain function. Proc Natl Acad Sci USA. 2001;98:676–82.CrossRefPubMedPubMedCentral

22.

Qin P, Wu X, Huang Z, Duncan NW, Tang W, Wolff A, Hu J, Gao L, Jin Y, Wu X, Zhang J, Lu L, Wu C, Qu X, Mao Y, Weng X, Zhang J, Northoff G. How are different neural networks related to consciousness? Ann Neurol. 2015;78:594–605.CrossRefPubMed

23.

Seghier ML. The angular gyrus: multiple functions and multiple subdivisions. Neuroscientist. 2013;19:43–61.CrossRefPubMedPubMedCentral

24.

Binder JR, Desai RH. The neurobiology of semantic memory. Trends Cogn Sci. 2011;15:527–36.CrossRefPubMedPubMedCentral

25.

Bonner MF, Peelle JE, Cook PA, Grossman M. Heteromodal conceptual processing in the angular gyrus. Neuroimage. 2013;71:175–86.CrossRefPubMed

26.

Guo Z, Jiang Z, Jiang B, McClure MA, Mu Q. High-Frequency Repetitive Transcranial Magnetic Stimulation Could Improve Impaired Working Memory Induced by Sleep Deprivation. Neural Plast. 2019;2019:7030286.CrossRefPubMedPubMedCentral

27.

Ji T, Li X, Chen J, Ren X, Mei L, Qiu Y, Zhang J, Wang S, Xu Z, Li H, Zheng L, Peng Y, Liu Y, Ni X, Tai J, Liu J. Brain function in children with obstructive sleep apnea: a resting-state fMRI study. Sleep. 2021;44:zsab047. CrossRefPubMed

28.

Peng DC, Dai XJ, Gong HH, Li HJ, Nie X, Zhang W. Altered intrinsic regional brain activity in male patients with severe obstructive sleep apnea: a resting-state functional magnetic resonance imaging study. Neuropsychiatr Dis Treat. 2014;10:1819–26.CrossRefPubMedPubMedCentral

29.

Song X, Roy B, Kang DW, Aysola RS, Macey PM, Woo MA, Yan-Go FL, Harper RM, Kumar R. Altered resting-state hippocampal and caudate functional networks in patients with obstructive sleep apnea. Brain Behav. 2018;8:e00994.CrossRefPubMedPubMedCentral

30.

van Geest Q, Westerik B, van der Werf YD, Geurts JJ, Hulst HE. The role of sleep on cognition and functional connectivity in patients with multiple sclerosis. J Neurol. 2017;264:72–80.CrossRefPubMed

31.

Legostaeva L, Poydasheva A, Iazeva E, Sinitsyn D, Sergeev D, Bakulin I, Lagoda D, Kremneva E, Morozova S, Ryabinkina Y, Suponeva N, Piradov M. Stimulation of the Angular Gyrus Improves the Level of Consciousness. Brain Sci. 2019;9:103.CrossRefPubMedPubMedCentral

32.

Huang YS, Hsiao IT, Liu FY, Hwang FM, Lin KL, Huang WC, Guilleminault C. Neurocognition, sleep, and PET findings in type 2 vs type 1 narcolepsy. Neurology. 2018;90:e1478–87.CrossRefPubMed

33.

Huang YS, Liu FY, Lin CY, Hsiao IT, Guilleminault C. Brain imaging and cognition in young narcoleptic patients. Sleep Med. 2016;24:137–44.CrossRefPubMed

34.

DelRosso LM, Hoque R. The cerebellum and sleep. Neurol Clin. 2014;32:893–900.CrossRefPubMed

35.

Pedroso JL, Braga-Neto P, Escorcio-Bezerra ML, Abrahão A, de Albuquerque MV, Filho FM, de Souza PV, de Rezende Pinto WB, Borges FR Jr, Saraiva-Pereira ML, Jardim LB, Barsottini OG. Non-motor and Extracerebellar Features in Spinocerebellar Ataxia Type 2. Cerebellum. 2017;16:34–9.CrossRefPubMed

36.

Dang D, Cunnington D. Excessive daytime somnolence in spinocerebellar ataxia type 1. J Neurol Sci. 2010;290:146–7.CrossRefPubMed

37.

Yuan X, Ou R, Hou Y, Chen X, Cao B, Hu X, Shang H. Extra-Cerebellar Signs and Non-motor Features in Chinese Patients With Spinocerebellar Ataxia Type 3. Front Neurol. 2019;10:110.CrossRefPubMedPubMedCentral

38.

Joo EY, Noh HJ, Kim JS, Koo DL, Kim D, Hwang KJ, Kim JY, Kim ST, Kim MR, Hong SB. Brain Gray Matter Deficits in Patients with Chronic Primary Insomnia. Sleep. 2013;36:999–1007CrossRefPubMedPubMedCentral

39.

Desseilles M, Dang-Vu T, Schabus M, Sterpenich V, Maquet P, Schwartz S. Neuroimaging insights into the pathophysiology of sleep disorders. Sleep. 2008;31:777–94.CrossRefPubMedPubMedCentral

40.

Zhang LB, Zhang J, Sun MJ, Chen H, Yan J, Luo FL, Yao ZX, Wu YM, Hu B. Neuronal Activity in the Cerebellum During the Sleep-Wakefulness Transition in Mice. Neurosci Bull. 2020;36:919–31.CrossRefPubMedPubMedCentral

41.

Canto CB, Onuki Y, Bruinsma B, van der Werf YD, De Zeeuw CI. The Sleeping Cerebellum. Trends Neurosci. 2017;40:309–23.CrossRefPubMed

42.

Zhang Y, Yang Y, Yang Y, Li J, Xin W, Huang Y, Shao Y, Zhang X. Alterations in Cerebellar Functional Connectivity Are Correlated With Decreased Psychomotor Vigilance Following Total Sleep Deprivation. Front Neurosci. 2019;13:134.CrossRefPubMedPubMedCentral

43.

Yang L, Lei Y, Wang L, Chen P, Cheng S, Chen S, Sun J, Li Y, Wang Y, Hu W, Yang Z. Abnormal functional connectivity density in sleep-deprived subjects. Brain Imaging Behav. 2018;12:1650–7.CrossRefPubMed

44.

Desjardins MÈ, Baril AA, Soucy JP, Dang-Vu TT, Desautels A, Petit D, Montplaisir J, Zadra A. Altered brain perfusion patterns in wakefulness and slow-wave sleep in sleepwalkers. Sleep. 2018;41:zsy039.CrossRefPubMedPubMedCentral

45.

Lim JS, Shin SA, Lee JY, Nam H, Lee JY, Kim YK. Neural substrates of rapid eye movement sleep behavior disorder in Parkinson’s disease. Parkinsonism Relat Disord. 2016;23:31–6.CrossRefPubMed

46.

Ayalon L, Ancoli-Israel S, Drummond SP. Altered brain activation during response inhibition in obstructive sleep apnea. J Sleep Res. 2009;18:204–8.CrossRefPubMedPubMedCentral

47.

Zhou F, Huang S, Zhuang Y, Gao L, Gong H. Frequency-dependent changes in local intrinsic oscillations in chronic primary insomnia: A study of the amplitude of low-frequency fluctuations in the resting state. Neuroimage Clin. 2016;15:458–65.CrossRefPubMed

48.

Han XH, Li XM, Tang WJ, Yu H, Wu P, Ge JJ, Wang J, Zuo CT, Shi KY. Assessing gray matter volume in patients with idiopathic rapid eye movement sleep behavior disorder. Neural Regen Res. 2019;14:868–75.CrossRefPubMedPubMedCentral

49.

Tholfsen LK, Larsen JP, Schulz J, Tysnes OB, Gjerstad MD. Development of excessive daytime sleepiness in early Parkinson disease. Neurology. 2015;85:162–8.CrossRefPubMed

50.

Johns MW. Sensitivity and specificity of the multiple sleep latency test (MSLT), the maintenance of wakefulness test and the epworth sleepiness scale: failure of the MSLT as a gold standard. J Sleep Res. 2000;9:5–11.CrossRefPubMed

51.

Tandberg E, Larsen JP, Karlsen K. A community-based study of sleep disorders in patients with Parkinson’s disease. Mov Disord. 1998;13:895–9.CrossRefPubMed

52.

Videnovic A, Golombek D. Circadian and sleep disorders in Parkinson’s disease. Exp Neurol. 2013;243:45–56.CrossRefPubMed

Titel: Excessive Daytime Sleepiness in Parkinson’s Disease is Related to Functional Abnormalities in the Left Angular Gyrus
verfasst von: Jin Hua Zheng
Jian Jun Ma
Wen Hua Sun
Zhi Dong Wang
Qing Qing Chang
Lin Rui Dong
Xiao Xue Shi
Ming Jian Li
Publikationsdatum: 29.06.2022
Verlag: Springer Berlin Heidelberg
Erschienen in: Clinical Neuroradiology / Ausgabe 1/2023
Print ISSN: 1869-1439
Elektronische ISSN: 1869-1447
DOI: https://doi.org/10.1007/s00062-022-01190-x

Update Radiologie

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert.

Newsletter bestellen

Live-Webinar "Urologie und Sexualmedizin in der Praxis"

Springer Medizin

Excessive Daytime Sleepiness in Parkinson’s Disease is Related to Functional Abnormalities in the Left Angular Gyrus