Sleep quality and the integrity of ascending reticular activating system - A multimodal MRI study

. 2024 Nov 30 ; 10 (22) : e40192. [epub] 20241107

Status PubMed-not-MEDLINE Jazyk angličtina Země Anglie, Velká Británie Médium electronic-ecollection

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid39748972
Odkazy

PubMed 39748972
PubMed Central PMC11693918
DOI 10.1016/j.heliyon.2024.e40192
PII: S2405-8440(24)16223-8
Knihovny.cz E-zdroje

Sleep is crucial for maintaining brain homeostasis and individuals with insufficient sleep are prone to more pronounced brain atrophy as compared to sufficiently sleeping peers. Moreover, sleep quality deteriorates with ageing and ageing is also associated with cerebral structural and functional changes, pointing to their mutual bidirectional interrelationship. This study aimed at determining whether sleep quality and age, separately, affect brain integrity and subsequently, whether sleep significantly modulates the effect of age on brain structural and functional integrity. 113 healthy volunteers underwent a multi-modal MRI imaging to extract information about the microstructure and function of major nodes of the ascending reticular activating system. Sleep quality was assessed by self-administered Pittsburgh's sleep quality index (PSQI) questionnaire. Subject were divided into good (global PSQI score <5) and poor (global PSQI score ≥5) sleep quality group. Whereas only borderline correlations were found between sleep quality and MRI metrics, age exhibited widespread correlations with both functional and microstructural MRI metrics. The latter effect was significantly modulated by sleep quality in ascending reticular activating system, hypothalamus, thalamus and also hippocampus in MRI metrics associated with iron load, cellularity and connectivity, mainly in the subgroup with poor sleep quality. Ergo, our results indicate sleep quality as a substantial contributor to both microstructural and functional brain changes in ageing and call for further research in this emerging topic.

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Herculano-Houzel S. Sleep it out. Science. 2013;342:316–317. doi: 10.1126/science.1245798. PubMed DOI

Xie L., Kang H., Xu Q., Chen M.J., Liao Y., Thiyagarajan M., O'Donnell J., Christensen D.J., Nicholson C., Iliff J.J., Takano T., Deane R., Nedergaard M. Sleep drives metabolite clearance from the adult brain. Science. 2013;342:373–377. doi: 10.1126/science.1241224. PubMed DOI PMC

Bellesi M., Pfister-Genskow M., Maret S., Keles S., Tononi G., Cirelli C. Effects of sleep and wake on oligodendrocytes and their precursors. J. Neurosci. 2013;33:14288–14300. doi: 10.1523/JNEUROSCI.5102-12.2013. PubMed DOI PMC

Lungato L., Marques M.S., Pereira V.G., Hix S., Gazarini M.L., Tufik S., D'Almeida V. Sleep deprivation alters gene expression and antioxidant enzyme activity in mice splenocytes. Scand. J. Immunol. 2013;77:195–199. doi: 10.1111/sji.12029. PubMed DOI

Cirelli C., Faraguna U., Tononi G. Changes in brain gene expression after long-term sleep deprivation. J. Neurochem. 2006;98:1632–1645. doi: 10.1111/j.1471-4159.2006.04058.x. PubMed DOI

Frank M.G. Sleep and synaptic plasticity in the developing and adult brain. Curr Top Behav Neurosci. 2015;25:123–149. doi: 10.1007/7854_2014_305. PubMed DOI PMC

Koutsoumparis A., Welp L.M., Wulf A., Urlaub H., Meierhofer D., Börno S., Timmermann B., Busack I., Bringmann H. Sleep neuron depolarization promotes protective gene expression changes and FOXO activation. Curr. Biol. 2022;32:2248–2262.e9. doi: 10.1016/j.cub.2022.04.012. PubMed DOI

Baldo B.A., Hanlon E.C., Obermeyer W., Bremer Q., Paletz E., Benca R.M. Upregulation of gene expression in reward-modulatory striatal opioid systems by sleep loss. Neuropsychopharmacology. 2013;38:2578–2587. doi: 10.1038/npp.2013.174. PubMed DOI PMC

Wyss-Coray T., Rogers J. Inflammation in Alzheimer disease-a brief review of the basic science and clinical literature. Cold Spring Harb Perspect Med. 2012;2:a006346. doi: 10.1101/cshperspect.a006346. PubMed DOI PMC

Moreno-García A., Kun A., Calero O., Medina M., Calero M. An overview of the role of lipofuscin in age-related neurodegeneration. Front. Neurosci. 2018;12:464. doi: 10.3389/fnins.2018.00464. PubMed DOI PMC

Perry V.H., Teeling J. Microglia and macrophages of the central nervous system: the contribution of microglia priming and systemic inflammation to chronic neurodegeneration. Semin. Immunopathol. 2013;35:601–612. doi: 10.1007/s00281-013-0382-8. PubMed DOI PMC

Sexton C.E., Storsve A.B., Walhovd K.B., Johansen-Berg H., Fjell A.M. Poor sleep quality is associated with increased cortical atrophy in community-dwelling adults. Neurology. 2014;83:967–973. doi: 10.1212/WNL.0000000000000774. PubMed DOI PMC

Sexton C.E., Zsoldos E., Filippini N., Griffanti L., Winkler A., Mahmood A., Allan C.L., Topiwala A., Kyle S.D., Spiegelhalder K., Singh-Manoux A., Kivimaki M., Mackay C.E., Johansen-Berg H., Ebmeier K.P. Associations between self-reported sleep quality and white matter in community-dwelling older adults: a prospective cohort study: sleep Quality and White Matter. Hum. Brain Mapp. 2017;38:5465–5473. doi: 10.1002/hbm.23739. PubMed DOI PMC

Spira A.P., Gamaldo A.A., An Y., Wu M.N., Simonsick E.M., Bilgel M., Zhou Y., Wong D.F., Ferrucci L., Resnick S.M. Self-reported sleep and β-amyloid deposition in community-dwelling older adults. JAMA Neurol. 2013;70:1537–1543. doi: 10.1001/jamaneurol.2013.4258. PubMed DOI PMC

Yaffe K., Nasrallah I., Hoang T.D., Lauderdale D.S., Knutson K.L., Carnethon M.R., Launer L.J., Lewis C.E., Sidney S. Sleep duration and white matter quality in middle-aged adults. Sleep. 2016;39:1743–1747. doi: 10.5665/sleep.6104. PubMed DOI PMC

Dube J., Lafortune M., Bedetti C., Bouchard M., Gagnon J.F., Doyon J., Evans A.C., Lina J.-M., Carrier J. Cortical thinning explains changes in sleep slow waves during adulthood. J. Neurosci. 2015;35:7795–7807. doi: 10.1523/JNEUROSCI.3956-14.2015. PubMed DOI PMC

Liu Y.-R., Fan D.-Q., Gui W.-J., Long Z.-L., Lei X., Yu J. Sleep-related brain atrophy and disrupted functional connectivity in older adults. Behav. Brain Res. 2018;347:292–299. doi: 10.1016/j.bbr.2018.03.032. PubMed DOI

Mander B.A., Rao V., Lu B., Saletin J.M., Lindquist J.R., Ancoli-Israel S., Jagust W., Walker M.P. Prefrontal atrophy, disrupted NREM slow waves and impaired hippocampal-dependent memory in aging. Nat. Neurosci. 2013;16:357–364. doi: 10.1038/nn.3324. PubMed DOI PMC

Saper C.B., Fuller P.M., Pedersen N.P., Lu J., Scammell T.E. Sleep state switching. Neuron. 2010;68:1023–1042. doi: 10.1016/j.neuron.2010.11.032. PubMed DOI PMC

Kokošová V., Filip P., Kec D., Baláž M. Bidirectional association between sleep and brain atrophy in aging. Front. Aging Neurosci. 2021;13 doi: 10.3389/fnagi.2021.726662. PubMed DOI PMC

Michaeli S., öz G., Sorce D.J., Garwood M., Ugurbil K., Majestic S., Tuite P. Assessment of brain iron and neuronal integrity in patients with Parkinson's disease using novel MRI contrasts. Mov. Disord. 2007;22:334–340. doi: 10.1002/mds.21227. PubMed DOI

Mitsumori F., Watanabe H., Takaya N. Estimation of brain iron concentration in vivo using a linear relationship between regional iron and apparent transverse relaxation rate of the tissue water at 4.7T: in Vivo Iron Meter for Human Brain. Magn. Reson. Med. 2009;62:1326–1330. doi: 10.1002/mrm.22097. PubMed DOI

Hakkarainen H., Sierra A., Mangia S., Garwood M., Michaeli S., Gröhn O., Liimatainen T. MRI relaxation in the presence of fictitious fields correlate with myelin content in normal rat brain. Magn. Reson. Med. 2016;75:161–168. doi: 10.1002/mrm.25590. PubMed DOI PMC

Liimatainen T., Sorce D.J., O'Connell R., Garwood M., Michaeli S. MRI contrast from relaxation along a fictitious field (RAFF) Magn. Reson. Med. 2010;64:983–994. doi: 10.1002/mrm.22372. PubMed DOI PMC

Kamiya K., Hori M., Aoki S. NODDI in clinical research. J. Neurosci. Methods. 2020;346 doi: 10.1016/j.jneumeth.2020.108908. PubMed DOI

Zhang H., Schneider T., Wheeler-Kingshott C.A., Alexander D.C. NODDI: practical in vivo neurite orientation dispersion and density imaging of the human brain. Neuroimage. 2012;61:1000–1016. doi: 10.1016/j.neuroimage.2012.03.072. PubMed DOI

Zuo X.-N., Ehmke R., Mennes M., Imperati D., Castellanos F.X., Sporns O., Milham M.P. Network centrality in the human functional connectome. Cereb Cortex. 2012;22:1862–1875. doi: 10.1093/cercor/bhr269. PubMed DOI

Zang Y.-F., He Y., Zhu C.-Z., Cao Q.-J., Sui M.-Q., Liang M., Tian L.-X., Jiang T.-Z., Wang Y.-F. Altered baseline brain activity in children with ADHD revealed by resting-state functional MRI. Brain Dev. 2007;29:83–91. doi: 10.1016/j.braindev.2006.07.002. PubMed DOI

Buysse D.J., Reynolds C.F., Monk T.H., Berman S.R., Kupfer D.J. The Pittsburgh Sleep Quality Index: a new instrument for psychiatric practice and research. Psychiatr. Res. 1989;28:193–213. doi: 10.1016/0165-1781(89)90047-4. PubMed DOI

Reisberg D. Oxford University Press; England: 2013. The Oxford Handbook of Cognitive Psychology. DOI

Filip P., Kokošová V., Valenta Z., Baláž M., Mangia S., Michaeli S., Vojtíšek L. Utility of quantitative MRI metrics in brain ageing research. Front. Aging Neurosci. 2023;15 doi: 10.3389/fnagi.2023.1099499. PubMed DOI PMC

Liimatainen T., Hakkarainen H., Mangia S., Huttunen J.M.J., Storino C., Idiyatullin D., Sorce D., Garwood M., Michaeli S. MRI contrasts in high rank rotating frames: MRI Contrasts in High Rank Rotating Frames. Magn. Reson. Med. 2015;73:254–262. doi: 10.1002/mrm.25129. PubMed DOI PMC

Glasser M.F., Sotiropoulos S.N., Wilson J.A., Coalson T.S., Fischl B., Andersson J.L., Xu J., Jbabdi S., Webster M., Polimeni J.R., Van Essen D.C., Jenkinson M., WU-Minn HCP Consortium The minimal preprocessing pipelines for the Human Connectome Project. Neuroimage. 2013;80:105–124. doi: 10.1016/j.neuroimage.2013.04.127. PubMed DOI PMC

Smith S.M., Beckmann C.F., Andersson J., Auerbach E.J., Bijsterbosch J., Douaud G., Duff E., Feinberg D.A., Griffanti L., Harms M.P., Kelly M., Laumann T., Miller K.L., Moeller S., Petersen S., Power J., Salimi-Khorshidi G., Snyder A.Z., Vu A.T., Woolrich M.W., Xu J., Yacoub E., Uğurbil K., Van Essen D.C., Glasser M.F. Wu-minn HCP consortium, resting-state fMRI in the human connectome project. Neuroimage. 2013;80:144–168. doi: 10.1016/j.neuroimage.2013.05.039. PubMed DOI PMC

Cox R.W. AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. Comput. Biomed. Res. 1996;29:162–173. doi: 10.1006/cbmr.1996.0014. PubMed DOI

Tariq M., Schneider T., Alexander D.C., Gandini Wheeler-Kingshott C.A., Zhang H. Bingham-NODDI: mapping anisotropic orientation dispersion of neurites using diffusion MRI. Neuroimage. 2016;133:207–223. doi: 10.1016/j.neuroimage.2016.01.046. PubMed DOI

Spindler M., Özyurt J., Thiel C.M. Automated diffusion-based parcellation of the hypothalamus reveals subunit-specific associations with obesity. Sci. Rep. 2020;10 doi: 10.1038/s41598-020-79289-9. PubMed DOI PMC

Winkler A.M., Ridgway G.R., Webster M.A., Smith S.M., Nichols T.E. Permutation inference for the general linear model. Neuroimage. 2014;92:381–397. doi: 10.1016/j.neuroimage.2014.01.060. PubMed DOI PMC

Nestrasil I., Michaeli S., Liimatainen T., Rydeen C.E., Kotz C.M., Nixon J.P., Hanson T., Tuite P.J. T1ρ and T2ρ MRI in the evaluation of Parkinson's disease. J. Neurol. 2010;257:964–968. doi: 10.1007/s00415-009-5446-2. PubMed DOI PMC

Filip P., Svatkova A., Carpenter A.F., Eberly L.E., Nestrasil I., Nissi M.J., Michaeli S., Mangia S. Rotating frame MRI relaxations as markers of diffuse white matter abnormalities in multiple sclerosis. Neuroimage: Clinical. 2020;26 doi: 10.1016/j.nicl.2020.102234. PubMed DOI PMC

Filip P., Burdová K., Valenta Z., Jech R., Kokošová V., Baláž M., Mangia S., Michaeli S., Bareš M., Vojtíšek L. Tremor associated with similar structural networks in Parkinson's disease and essential tremor. Parkinsonism Relat Disord. 2021;95:28–34. doi: 10.1016/j.parkreldis.2021.12.014. PubMed DOI

Ward R.J., Zucca F.A., Duyn J.H., Crichton R.R., Zecca L. The role of iron in brain ageing and neurodegenerative disorders. Lancet Neurol. 2014;13:1045–1060. doi: 10.1016/S1474-4422(14)70117-6. PubMed DOI PMC

Churchill N.W., Caverzasi E., Graham S.J., Hutchison M.G., Schweizer T.A. White matter microstructure in athletes with a history of concussion: comparing diffusion tensor imaging (DTI) and neurite orientation dispersion and density imaging (NODDI) Hum. Brain Mapp. 2017;38:4201–4211. doi: 10.1002/hbm.23658. PubMed DOI PMC

Colgan N., Siow B., O'Callaghan J.M., Harrison I.F., Wells J.A., Holmes H.E., Ismail O., Richardson S., Alexander D.C., Collins E.C., Fisher E.M., Johnson R., Schwarz A.J., Ahmed Z., O'Neill M.J., Murray T.K., Zhang H., Lythgoe M.F. Application of neurite orientation dispersion and density imaging (NODDI) to a tau pathology model of Alzheimer's disease. Neuroimage. 2016;125:739–744. doi: 10.1016/j.neuroimage.2015.10.043. PubMed DOI PMC

Dowell N.G., Bouyagoub S., Tibble J., Voon V., Cercignani M., Harrison N.A. Interferon-alpha-Induced changes in NODDI predispose to the development of fatigue. Neuroscience. 2019;403:111–117. doi: 10.1016/j.neuroscience.2017.12.040. PubMed DOI PMC

Buell S.J., Coleman P.D. Dendritic growth in the aged human brain and failure of growth in senile dementia. Science. 1979;206:854–856. doi: 10.1126/science.493989. PubMed DOI

Pyapali G.K., Turner D.A. Increased dendritic extent in hippocampal CA1 neurons from aged F344 rats. Neurobiol. Aging. 1996;17:601–611. doi: 10.1016/0197-4580(96)00034-6. PubMed DOI

Granberg T., Fan Q., Treaba C.A., Ouellette R., Herranz E., Mangeat G., Louapre C., Cohen-Adad J., Klawiter E.C., Sloane J.A., Mainero C. In vivo characterization of cortical and white matter neuroaxonal pathology in early multiple sclerosis. Brain. 2017;140:2912–2926. doi: 10.1093/brain/awx247. PubMed DOI PMC

Grussu F., Schneider T., Tur C., Yates R.L., Tachrount M., Ianuş A., Yiannakas M.C., Newcombe J., Zhang H., Alexander D.C., DeLuca G.C., Gandini Wheeler-Kingshott C.A.M. Neurite dispersion: a new marker of multiple sclerosis spinal cord pathology? Ann Clin Transl Neurol. 2017;4:663–679. doi: 10.1002/acn3.445. PubMed DOI PMC

Mitchell T., Archer D.B., Chu W.T., Coombes S.A., Lai S., Wilkes B.J., McFarland N.R., Okun M.S., Black M.L., Herschel E., Simuni T., Comella C., Xie T., Li H., Parrish T.B., Kurani A.S., Corcos D.M., Vaillancourt D.E. Neurite orientation dispersion and density imaging (NODDI) and free-water imaging in Parkinsonism. Hum. Brain Mapp. 2019;40:5094–5107. doi: 10.1002/hbm.24760. PubMed DOI PMC

Sierra A., Michaeli S., Niskanen J.-P., Valonen P.K., Gröhn H.I., Ylä-Herttuala S., Garwood M., Gröhn O.H. Water spin dynamics during apoptotic cell death in glioma gene therapy probed by T1ρ and T2ρ. Magn. Reson. Med. 2008;59:1311–1319. doi: 10.1002/mrm.21600. PubMed DOI PMC

Satzer D., DiBartolomeo C., Ritchie M.M., Storino C., Liimatainen T., Hakkarainen H., Idiyatullin D., Mangia S., Michaeli S., Parr A.M., Low W.C. Assessment of dysmyelination with RAFFn MRI: application to murine MPS I. PLoS One. 2015;10 doi: 10.1371/journal.pone.0116788. PubMed DOI PMC

Miyata S., Taniguchi M., Koyama Y., Shimizu S., Tanaka T., Yasuno F., Yamamoto A., Iida H., Kudo T., Katayama T., Tohyama M. Association between chronic stress-induced structural abnormalities in Ranvier nodes and reduced oligodendrocyte activity in major depression. Sci. Rep. 2016;6 doi: 10.1038/srep23084. PubMed DOI PMC

Lehto L.J., Albors A.A., Sierra A., Tolppanen L., Eberly L.E., Mangia S., Nurmi A., Michaeli S., Gröhn O. Lysophosphatidyl choline induced demyelination in rat probed by relaxation along a fictitious field in high rank rotating frame. Front. Neurosci. 2017;11:433. doi: 10.3389/fnins.2017.00433. PubMed DOI PMC

Li H., Li L., Shao Y., Gong H., Zhang W., Zeng X., Ye C., Nie S., Chen L., Peng D. Abnormal intrinsic functional hubs in severe male obstructive sleep apnea: evidence from a voxel-wise degree centrality analysis. PLoS One. 2016;11 doi: 10.1371/journal.pone.0164031. PubMed DOI PMC

Ponticorvo S., Canna A., Moeller S., Akcakaya M., Metzger G.J., Filip P., Eberly L.E., Michaeli S., Mangia S. Reducing thermal noise in high-resolution quantitative magnetic resonance imaging rotating frame relaxation mapping of the human brain at 3 T. NMR Biomed. 2024;e5228 doi: 10.1002/nbm.5228. PubMed DOI PMC

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