Cortical and subcortical morphometric changes and their relation to cognitive impairment in isolated REM sleep behavior disorder

. 2024 Feb ; 45 (2) : 613-627. [epub] 20230905

Jazyk angličtina Země Itálie Médium print-electronic

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid37670125

Grantová podpora
NU20-04-00327 Ministerstvo Zdravotnictví Ceské Republiky
NU21-04-00535 Ministerstvo Zdravotnictví Ceské Republiky
LX22NPO5107 National Institute for Neurological Research
MH CZ-DRO-VFN64165 Univerzita Karlova v Praze
MH CZ-DRO-NNH00023884 Univerzita Karlova v Praze

Odkazy

PubMed 37670125
PubMed Central PMC10791856
DOI 10.1007/s10072-023-07040-z
PII: 10.1007/s10072-023-07040-z
Knihovny.cz E-zdroje

OBJECTIVE: To date, very few studies have focused on structural changes and their association with cognitive performance in isolated REM sleep behaviour disorder (iRBD). Moreover, the results of these studies are inconclusive. This study aims to evaluate differences in the associations between brain morphology and cognitive tests in iRBD and healthy controls. METHODS: Sixty-three patients with iRBD and thirty-six controls underwent MRI with a 3 T scanner. The cognitive performance was assessed by a comprehensive neuropsychological battery. Based on performance, the iRBD group was divided into two subgroups with (iRBD-MCI) and without mild cognitive impairment (iRBD-NC). The high-resolution T1-weighted images were analysed using an automated atlas segmentation tool, voxel-based (VBM) and deformation-based (DBM) morphometry to identify between-group differences and correlations with cognitive performance. RESULTS: VBM, DBM and the comparison of ROI volumes yielded no significant differences between iRBD and controls. In the iRBD group, significant correlations in VBM were found between several cortical and subcortical structures primarily located in the temporal, parietal, occipital lobe, cerebellum, and basal ganglia and three cognitive tests assessing psychomotor speed and one memory test. Between-group analysis of cognition revealed a significant difference between iRBD-MCI and iRBD-NC in tests including a processing speed component. CONCLUSIONS: iRBD shows deficits in several cognitive tests that correlate with morphological changes, the most prominent of which is in psychomotor speed and visual attention as measured by the TMT-A and associated with the volume of striatum, insula, cerebellum, temporal lobe, pallidum and amygdala.

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Assogna F, Liguori C, Cravello L, Macchiusi L, Belli C, Placidi F, Pierantozzi M, Stefani A, Mercuri B, Izzi F, Caltagirone C, Mercuri NB, Pontieri FE, Spalletta G, Pellicano C (2021) Cognitive and neuropsychiatric profiles in idiopathic rapid eye movement sleep behavior disorder and parkinson’s disease. J Pers Med 11(1). 10.3390/jpm11010051 PubMed PMC

Leitner C, D'Este G, Verga L, Rahayel S, Mombelli S, Sforza M, Casoni F, Zucconi M, Ferini-Strambi L, Galbiati A. Neuropsychological changes in isolated rem sleep behavior disorder: a systematic review and meta-analysis of cross-sectional and longitudinal studies. Neuropsychol Rev. 2023 doi: 10.1007/s11065-022-09572-1. PubMed DOI

Gagnon JF, Vendette M, Postuma RB, Desjardins C, Massicotte-Marquez J, Panisset M, Montplaisir J. Mild cognitive impairment in rapid eye movement sleep behavior disorder and Parkinson's disease. Ann Neurol. 2009;66(1):39–47. doi: 10.1002/ana.21680. PubMed DOI

Pereira JB, Weintraub D, Chahine L, Aarsland D, Hansson O, Westman E. Cortical thinning in patients with REM sleep behavior disorder is associated with clinical progression. NPJ Parkinsons Dis. 2019;5:7. doi: 10.1038/s41531-019-0079-3. PubMed DOI PMC

Rahayel S, Postuma RB, Montplaisir J, Misic B, Tremblay C, Vo A, Lewis S, Matar E, Ehgoetz Martens K, Blanc F, Yao C, Carrier J, Monchi O, Gaubert M, Dagher A, Gagnon JF. A prodromal brain-clinical pattern of cognition in synucleinopathies. Ann Neurol. 2021;89(2):341–357. doi: 10.1002/ana.25962. PubMed DOI

Rahayel S, Postuma RB, Montplaisir J, Genier Marchand D, Escudier F, Gaubert M, Bourgouin PA, Carrier J, Monchi O, Joubert S, Blanc F, Gagnon JF. Cortical and subcortical gray matter bases of cognitive deficits in REM sleep behavior disorder. Neurology. 2018;90(20):e1759–e1770. doi: 10.1212/WNL.0000000000005523. PubMed DOI PMC

Campabadal A, Segura B, Junque C, Serradell M, Abos A, Uribe C, Baggio HC, Gaig C, Santamaria J, Compta Y, Bargallo N, Iranzo A. Cortical gray matter and hippocampal atrophy in idiopathic rapid eye movement sleep behavior disorder. Front Neurol. 2019;10:312. doi: 10.3389/fneur.2019.00312. PubMed DOI PMC

Rahayel S, Montplaisir J, Monchi O, Bedetti C, Postuma RB, Brambati S, Carrier J, Joubert S, Latreille V, Jubault T, Gagnon JF. Patterns of cortical thinning in idiopathic rapid eye movement sleep behavior disorder. Mov Disord. 2015;30(5):680–687. doi: 10.1002/mds.25820. PubMed DOI

Figorilli M, Meloni F, Lecca R, Tamburrino L, Mascia MG, Cocco V, Meloni M, Marques AR, Vidal T, Congiu P, Defazio G, Durif F, Lanza G, Ferri R, Schenck CH, Fantini ML, Puligheddu M (2023) Severity of REM sleep without atonia correlates with measures of cognitive impairment and depressive symptoms in REM sleep behaviour disorder. J Sleep Res e13880. 10.1111/jsr.13880 PubMed

American Academy of Sleep Medicine (2014) International Classification of Sleep Disorders. American Academy of Sleep Medicine, Darien, IL

Campabadal A, Inguanzo A, Segura B, Serradell M, Abos A, Uribe C, Gaig C, Santamaria J, Compta Y, Bargallo N, Junque C, Iranzo A. Cortical gray matter progression in idiopathic REM sleep behavior disorder and its relation to cognitive decline. Neuroimage Clin. 2020;28:102421. doi: 10.1016/j.nicl.2020.102421. PubMed DOI PMC

Gaser C, Dahnke R. A Computational Anatomy Toolbox for SPM. 12.7 ed PubMed PMC

UCL queen square institute of neurology. Stat Parametric Mapp. v7771 ed2020

MathWorks. MATLAB. R2018b ed2018

Hammers A, Allom R, Koepp MJ, Free SL, Myers R, Lemieux L, Mitchell TN, Brooks DJ, Duncan JS. Three-dimensional maximum probability atlas of the human brain, with particular reference to the temporal lobe. Hum Brain Mapp. 2003;19(4):224–247. doi: 10.1002/hbm.10123. PubMed DOI PMC

Berry RB, Brooks R, Gamaldo CE, Harding SM, Lloyd RM, Marcus CL, Vaughn BV, for the American Academy of Sleep Medicine (2015) The AASM manual for the scoring of sleep and associated events: rules, terminology and technical specifications, Version 2.2. American Academy of Sleep Medicine, Darien, IL

Frauscher B, Iranzo A, Gaig C, Gschliesser V, Guaita M, Raffelseder V, Ehrmann L, Sola N, Salamero M, Tolosa E, Poewe W, Santamaria J, Hogl B, Group S Normative EMG values during REM sleep for the diagnosis of REM sleep behavior disorder. Sleep. 2012;35(6):835–47. doi: 10.5665/sleep.1886. PubMed DOI PMC

Nepozitek J, Dostalova S, Dusek P, Kemlink D, Prihodova I, Ibarburu Lorenzo YLV, Friedrich L, Bezdicek O, Nikolai T, Perinova P, Dall'Antonia I, Dusek P, Ruml M, Ruzicka E, Sonka K (2019) Simultaneous tonic and phasic REM sleep without atonia best predicts early phenoconversion to neurodegenerative disease in idiopathic REM sleep behavior disorder. Sleep 42(9). 10.1093/sleep/zsz132 PubMed

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 URTF 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(15):2129–70. doi: 10.1002/mds.22340. PubMed DOI

Ciharova M, Cigler H, Dostalova V, Sivicova G, Bezdicek O. Beck depression inventory, second edition, Czech version: demographic correlates, factor structure and comparison with foreign data. Int J Psychiatry Clin Pract. 2020;24(4):371–9. doi: 10.1080/13651501.2020.1775854. PubMed DOI

Spielberger CD, Gorsuch RL, Lushene RD, Vagg PR, Jacobs GA. Manual for the state-trait anxiety inventory. Palo Alto, CA: Consulting Psychologists Press; 1983.

Johns MW. A new method for measuring daytime sleepiness: the epworth sleepiness scale. Sleep. 1991;14(6):540–545. doi: 10.1093/sleep/14.6.540. PubMed DOI

Krámská L (2014) Hodnocení premorbidního intelektu v neuropsychologii: Český test čtení slov. Propsyco, Otrokovice

Wenke Š, Mana J, Havlík F, Cohn M, Nikolai T, Buschke H, Nepožitek J, Peřinová P, Dostálová S, Ibarburu Lorenzo Y Losada V, Růžička E, Šonka K, Dušek P, Bezdicek O (2022) Characterization of memory profile in idiopathic REM sleep behavior disorder. J Clin Exp Neuropsychol 1–14. 10.1080/13803395.2022.2107182 PubMed

Harrell FE, Dupont C. Hmisc: Harrell Miscellaneous. 4.6–0 ed2021

Halai AD, Woollams AM, Lambon Ralph MA. Using principal component analysis to capture individual differences within a unified neuropsychological model of chronic post-stroke aphasia: Revealing the unique neural correlates of speech fluency, phonology and semantics. Cortex. 2017;86:275–289. doi: 10.1016/j.cortex.2016.04.016. PubMed DOI PMC

RStudio Team (2020) RStudio: Integrated Development for R. 1.3.1073 ed. Boston: RStudio, PBC

Campabadal A, Segura B, Junque C, Iranzo A. Structural and functional magnetic resonance imaging in isolated REM sleep behavior disorder: A systematic review of studies using neuroimaging software. Sleep Med Rev. 2021;59:101495. doi: 10.1016/j.smrv.2021.101495. PubMed DOI

Remillard-Pelchat D, Rahayel S, Gaubert M, Postuma RB, Montplaisir J, Pelletier A, Monchi O, Brambati SM, Carrier J, Gagnon JF. Comprehensive analysis of brain volume in REM sleep behavior disorder with mild cognitive impairment. J Parkinsons Dis. 2022;12(1):229–241. doi: 10.3233/JPD-212691. PubMed DOI

Mak E, Su L, Williams GB, Firbank MJ, Lawson RA, Yarnall AJ, Duncan GW, Owen AM, Khoo TK, Brooks DJ, Rowe JB, Barker RA, Burn DJ, O'Brien JT. Baseline and longitudinal grey matter changes in newly diagnosed Parkinson's disease: ICICLE-PD study. Brain. 2015;138(Pt 10):2974–2986. doi: 10.1093/brain/awv211. PubMed DOI PMC

Muslimovic D, Post B, Speelman JD, De Haan RJ, Schmand B. Cognitive decline in Parkinson's disease: a prospective longitudinal study. J Int Neuropsychol Soc. 2009;15(3):426–437. doi: 10.1017/S1355617709090614. PubMed DOI

Koerts J, Meijer HA, Colman KS, Tucha L, Lange KW, Tucha O. What is measured with verbal fluency tests in Parkinson's disease patients at different stages of the disease? J Neural Transm (Vienna) 2013;120(3):403–411. doi: 10.1007/s00702-012-0885-9. PubMed DOI

Hanakawa T, Goldfine AM, Hallett M (2017) A common function of basal ganglia-cortical circuits subserving speed in both motor and cognitive domains. eNeuro 4(6). 10.1523/ENEURO.0200-17.2017 PubMed PMC

Botzung A, Philippi N, Noblet V, Loureiro de Sousa P, Blanc F. Pay attention to the basal ganglia: a volumetric study in early dementia with Lewy bodies. Alzheimers Res Ther. 2019;11(1):108. doi: 10.1186/s13195-019-0568-y. PubMed DOI PMC

Geng C, Wang S, Li Z, Xu P, Bai Y, Zhou Y, Zhang X, Li Y, Zhang J, Zhang H. Resting-state functional network topology alterations of the occipital lobe associated with attention impairment in isolated rapid eye movement behavior disorder. Front Aging Neurosci. 2022;14:844483. doi: 10.3389/fnagi.2022.844483. PubMed DOI PMC

Zhang HJ, Wang SH, Bai YY, Zhang JW, Chen S. Abnormal striatal-cortical networks contribute to the attention/executive function deficits in idiopathic rem sleep behavior disorder: a resting state functional MRI study. Front Aging Neurosci. 2021;13:690854. doi: 10.3389/fnagi.2021.690854. PubMed DOI PMC

Bezdicek O, Motak L, Axelrod BN, Preiss M, Nikolai T, Vyhnalek M, Poreh A, Ruzicka E. Czech version of the trail making test: normative data and clinical utility. Arch Clin Neuropsychol. 2012;27(8):906–914. doi: 10.1093/arclin/acs084. PubMed DOI

Talwar N, Churchill NW, Hird MA, Tam F, Graham SJ, Schweizer TA. Functional magnetic resonance imaging of the trail-making test in older adults. PLoS One. 2020;15(5):e0232469. doi: 10.1371/journal.pone.0232469. PubMed DOI PMC

Zakzanis KK, Mraz R, Graham SJ. An fMRI study of the Trail Making Test. Neuropsychologia. 2005;43(13):1878–1886. doi: 10.1016/j.neuropsychologia.2005.03.013. PubMed DOI

Yao ZF, Yang MH, Hsieh S. Brain structural-behavioral correlates underlying grooved pegboard test performance across lifespan. J Mot Behav. 2021;53(3):373–384. doi: 10.1080/00222895.2020.1787320. PubMed DOI

Campabadal A, Abos A, Segura B, Serradell M, Uribe C, Baggio HC, Gaig C, Santamaria J, Compta Y, Bargallo N, Junque C, Iranzo A. Disruption of posterior brain functional connectivity and its relation to cognitive impairment in idiopathic REM sleep behavior disorder. Neuroimage Clin. 2020;25:102138. doi: 10.1016/j.nicl.2019.102138. PubMed DOI PMC

Bezdicek O, Nikolai T, Nepozitek J, Perinova P, Kemlink D, Dusek P, Prihodova I, Dostalova S, Ibarburu V, Trnka J, Kupka K, Meckova Z, Keller J, Vymazal J, Ruzicka E, Sonka K, Dusek P. Prospective memory impairment in idiopathic REM sleep behavior disorder. Clin Neuropsychol. 2018;32(5):1019–1037. doi: 10.1080/13854046.2017.1394493. PubMed DOI

Nisser J, Derlien S, Bublak P, Schwab M, Witte OW, Kesper K, Schultze T, Rupprecht S. Systematic quantitative assessment of motor function in clinically isolated REM sleep behaviour disorder: A diagnostic window into early alpha-synucleinopathies. J Sleep Res. 2022;31(2):e13459. doi: 10.1111/jsr.13459. PubMed DOI

Litvan I, Goldman JG, Tröster AI, Schmand BA, Weintraub D, Petersen RC, Mollenhauer B, Adler CH, Marder K, Williams-Gray CH, Aarsland D, Kulisevsky J, Rodriguez-Oroz MC, Burn DJ, Barker RA, Emre M. Diagnostic criteria for mild cognitive impairment in Parkinson's disease: movement disorder society task force guidelines. Mov Disord. 2012;27(3):349–356. doi: 10.1002/mds.24893. PubMed DOI PMC

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