Spatial navigation in early multiple sclerosis: a neglected cognitive marker of the disease?
Jazyk angličtina Země Německo Médium print-electronic
Typ dokumentu časopisecké články
Grantová podpora
546317
Grantová Agentura České Republiky
00064203
Ministerstvo Zdravotnictví Ceské Republiky
699012
Institutional Support of Excellence 2. LF UK
PubMed
32700011
DOI
10.1007/s00415-020-10079-z
PII: 10.1007/s00415-020-10079-z
Knihovny.cz E-zdroje
- Klíčová slova
- Allocentric, Cognition, Egocentric, Lesion load, MRI, Neuropsychology, Volumetry, Voxel-based morphometry,
- MeSH
- kognice MeSH
- kognitivní dysfunkce * MeSH
- lidé MeSH
- neuropsychologické testy MeSH
- prostorová navigace * MeSH
- roztroušená skleróza * diagnostické zobrazování MeSH
- vnímání prostoru MeSH
- Check Tag
- lidé MeSH
- Publikační typ
- časopisecké články MeSH
BACKGROUND: Cognitive deficits are common in early multiple sclerosis (MS), however, spatial navigation changes and their associations with brain pathology remain poorly understood. OBJECTIVE: To characterize the profile of spatial navigation changes in two main navigational strategies, egocentric (self-centred) and allocentric (world-centred), and their associations with demyelinating and neurodegenerative changes in early MS. METHODS: Participants with early MS after the first clinical event (n = 51) and age-, gender- and education-matched controls (n = 42) underwent spatial navigation testing in a real-space human analogue of the Morris water maze task, comprehensive neuropsychological assessment, and MRI brain scan with voxel-based morphometry and volumetric analyses. RESULTS: The early MS group had lower performance in the egocentric (p = 0.010), allocentric (p = 0.004) and allocentric-delayed (p = 0.038) navigation tasks controlling for age, gender and education. Based on the applied criteria, lower spatial navigation performance was present in 26-29 and 33-41% of the participants with early MS in the egocentric and the allocentric task, respectively. Larger lesion load volume in cortical, subcortical and cerebellar regions (ß ≥ 0.29; p ≤ 0.032) unlike brain atrophy was associated with less accurate allocentric navigation performance. CONCLUSION: Lower spatial navigation performance is present in up to 41% of the participants with early MS. Demyelinating lesions in early MS may disrupt neural network forming the basis of allocentric navigation.
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Brochet B, Ruet A (2019) Cognitive impairment in multiple sclerosis with regards to disease duration and clinical phenotypes. Front Neurol 10:261 PubMed PMC
Potagas C, Giogkaraki E, Koutsis G, Mandellos D, Tsirempolou E, Sfagos C, Vassilopoulos D (2008) Cognitive impairment in different MS subtypes and clinically isolated syndromes. J Neurol Sci 267:100–106 PubMed
Daams M, Steenwijk MD, Schoonheim MM, Wattjes MP, Balk LJ, Tewarie PK, Killestein J, Uitdehaag BM, Geurts JJ, Barkhof F (2016) Multi-parametric structural magnetic resonance imaging in relation to cognitive dysfunction in long-standing multiple sclerosis. Mult Scler 22:608–619 PubMed
Schultheis MT, Weisser V, Ang J, Elovic E, Nead R, Sestito N, Fleksher C, Millis SR (2010) Examining the relationship between cognition and driving performance in multiple sclerosis. Arch Phys Med Rehabil 91:465–473 PubMed
Honarmand K, Akbar N, Kou N, Feinstein A (2011) Predicting employment status in multiple sclerosis patients: the utility of the MS functional composite. J Neurol 258:244–249 PubMed
Reuter F, ZaaraouiW Crespy L, Faivre A, Rico A, Malikova I, Confort-Gouny S, Cozzone PJ, Ranjeva JP, Pelletier J, Audoin B (2011) Cognitive impairment at the onset of multiple sclerosis: relationship to lesion location. Mult Scler 17:755–758 PubMed
Ruano L, Portaccio E, Goretti B, Niccolai C, Severo M, Patti F, Cilia S, Gallo P, Grossi P, Ghezzi A, Roscio M, Mattioli F, Stampatori C, Trojano M, Viterbo RG, Amato MP (2017) Age and disability drive cognitive impairment in multiple sclerosis across disease subtypes. Mult Scler 23:1258–1267 PubMed
Lester AW, Moffat SD, Wiener JM, Barnes CA, Wolbers T (2017) The aging navigational system. Neuron 95:1019–1035 PubMed PMC
Maguire EA, Burgess N, Donnett JG, Frackowiak RS, Frith CD, O’Keefe J (1998) Knowing where and getting there: a human navigation network. Science 280:921–924 PubMed
Bastiaansen AEM, van Sonderen A, Titulaer MJ (2017) Autoimmune encephalitis with anti-leucine-rich glioma-inactivated 1 or anti-contactin-associated protein-like 2 antibodies (formerly called voltage-gated potassium channel-complex antibodies). Curr Opin Neurol 30:302–309 PubMed
Schneider CB, Linse K, Schönfeld R, Brown S, Brown S, Koch R, Reichmann H, Leplow B, Storch A (2017) Spatial learning deficits in Parkinson’s disease with and without mild cognitive impairment. Parkinsonism Relat Disord 36:83–88 PubMed
Majerová V, Kalinčík T, Laczó J, Vyhnálek M, Hort J, Bojar M, Růžička E, Roth J (2012) Disturbance of real space navigation in moderately advanced but not in early Huntington’s disease. J Neurol Sci 312:86–91 PubMed
Claessen MHG, Visser-Meily JMA, Meilinger T, Postma A, de Rooij NK, van der Ham IJM (2017) A systematic investigation of navigation impairment in chronic stroke patients: evidence for three distinct types. Neuropsychologia 103:154–161 PubMed
Hort J, Laczó J, Vyhnálek M, Bojar M, Bures J, Vlcek K (2007) Spatial navigation deficit in amnestic mild cognitive impairment. Proc Natl Acad Sci 104:4042–4047 PubMed
Amlerova J, Laczo J, Vlcek K, Javurkova A, Andel R, Marusic P (2013) Risk factors for spatial memory impairment in patients with temporal lobe epilepsy. Epilepsy Behav 26:57–60 PubMed
Hyncicova E, Vyhnalek M, Kalina A, Martinkovič L, Nikolai T, Lisý J, Hort J, Meluzínová E, Laczó J (2017) Cognitive impairment and structural brain changes in patients with clinically isolated syndrome at high risk for multiple sclerosis. J Neurol 264:482–493 PubMed
Henry RG, Shieh M, Okuda DT, Evangelista A, Gorno-Tempini ML, Pelletier D (2008) Regional grey matter atrophy in clinically isolated syndromes at presentation. J Neurol Neurosurg Psychiatry 79:1236–1244 PubMed PMC
Hyncicova E, Kalina A, Vyhnalek M, Nikolai T, Martinkovic L, Lisy J, Hort J, Meluzinova E, Laczó J (2018) Health-related quality of life, neuropsychiatric symptoms and structural brain changes in clinically isolated syndrome. PLoS One 13:e0200254 PubMed PMC
Audoin B, Zaaraoui W, Reuter F, Rico A, Malikova I, Confort-Gouny S, Cozzone P, Pelletier J, Ranjeva J (2010) Atrophy mainly affects the limbic system and the deep grey matter at the first stage of multiple sclerosis. J Neurol Neurosurg Psychiatry 81:690–695 PubMed
Thompson AJ, Banwell BL, Barkhof F, Carroll WM, Coetzee T, Comi G, Correale J, Fazekas F, Filippi M, Freedman MS, Fujihara K, Galetta SL, Hartung HP, Kappos L, Lublin FD, Marrie RA, Miller AE, Miller DH, Montalban X, Mowry EM, Sorensen PS, Tintoré M, Traboulsee AL, Trojano M, Uitdehaag BMJ, Vukusic S, Waubant E, Weinshenker BG, Reingold SC, Cohen JA (2018) Diagnosis of multiple sclerosis: 2017 revisions of the McDonald criteria. Lancet Neurol 17:162–173 PubMed
Laczó J, Andel R, Nedelska Z, Vyhnalek M, Vlcek K, Crutch S, Harrison J, Hort J (2017) Exploring the contribution of spatial navigation to cognitive functioning in older adults. Neurobiol Aging 51:67–70 PubMed
Laczó J, Vlcek K, Vyhnálek M, Vajnerová O, Ort M, Holmerová I, Tolar M, Andel R, Bojar M, Hort J (2009) Spatial navigation testing discriminates two types of amnestic mild cognitive impairment. Behav Brain Res 202:252–259 PubMed
Petersen RC (2004) Mild cognitive impairment as a diagnostic entity. J Intern Med 256:183–194 PubMed
Nikolai T, Stepankova H, Kopecek M, Sulc Z, Vyhnalek M, Bezdicek O (2018) The uniform data set, Czech version: normative data in older adults from an international perspective. J Alzheimers Dis 61:1233–1240 PubMed PMC
Smith SM, Zhang Y, Jenkinson M, Chen J, Matthews PM, Federico A, De Stefano N (2002) Accurate, robust and automated longitudinal and cross-sectional brain change analysis. NeuroImage 17:479–489 PubMed
Smith SM, Jenkinson M, Woolrich MW, Beckmann CF, Behrens TE, Johansen-Berg H, Bannister PR, De Luca M, Drobnjak I, Flitney DE, Niazy RK, Saunders J, Vickers J, Zhang Y, De Stefano N, Brady JM, Matthews PM (2004) Advances in functional and structural MR image analysis and implementation as FSL. NeuroImage 23:208–219
Patenaude B, Smith SM, Kennedy DN, Jenkinson M (2011) A Bayesian model of shape and appearance for subcortical brain segmentation. Neuroimage 56:907–922 PubMed PMC
Jack CR, Petersen RC, O’Brien PC, Tangalos EG (1992) MR-based hippocampal volumetry in the diagnosis of Alzheimer’s disease. Neurology 42:183–188 PubMed
Battaglini M, Jenkinson M, De Stefano N (2012) Evaluating and reducing the impact of white matter lesions on brain volume measurements. Hum Brain Mapp 33:2062–2071 PubMed
Jenkinson M, Bannister P, Brady M, Smith S (2002) Improved optimization for the robust and accurate linear registration and motion correction of brain images. NeuroImage 17:825–841 PubMed
Winkler AM, Ridgway GR, Webster MA, Smith SM, Nichols TE (2014) Permutation inference for the general linear model. NeuroImage 92:381–397 PubMed PMC
Feuillet L, Reuter F, Audoin B, Malikova I, Barrau K, Cherif AA, Pelletier J (2007) Early cognitive impairment in patients with clinically isolated syndrome suggestive of multiple sclerosis. Mult Scler 13:124–127 PubMed
Deloire MS, Ruet A, Hamel D, Bonnet M, Dousset V, Brochet B (2011) MRI predictors of cognitive outcome in early multiple sclerosis. Neurology 76:1161–1167 PubMed PMC
Glanz BI, Holland CM, Gauthier SA, Amunwa EL, Liptak Z, Houtchens MK, Sperling RA, Khoury SJ, Guttmann CR, Weiner HL (2007) Cognitive dysfunction in patients with clinically isolated syndromes or newly diagnosed multiple sclerosis. Mult Scler 13:1004–1010 PubMed
Planche V, Ruet A, Coupé P, Lamargue-Hamel D, Deloire M, Pereira B, Manjon JV, Munsch F, Moscufo N, Meier DS, Guttmann CR, Dousset V, Brochet B, Tourdias T (2017) Hippocampal microstructural damage correlates with memory impairment in clinically isolated syndrome suggestive of multiple sclerosis. Mult Scler 23:1214–1224 PubMed
Lommers E, Simon J, Reuter G, Delrue G, Dive D, Degueldre C, Balteau E, Phillips C, Maquet P (2019) Multiparameter MRI quantification of microstructural tissue alterations in multiple sclerosis. Neuroimage Clin 23:1018–1079
Murias K, Slone E, Tariq S, Iaria G (2019) Development of spatial orientation skills: an fMRI study. Brain Imaging Behav 13:1590–1601 PubMed
Mollison D, Sellar R, Bastin M, Mollison D, Chandran S, Wardlaw J, Connick P (2017) The clinico-radiological paradox of cognitive function and MRI burden of white matter lesions in people with multiple sclerosis: a systematic review and meta-analysis. PLoS One 12:15
Uher T, Krasensky J, Sobisek L, Blahova Dusankova J, Seidl Z, Kubala Havrdova E, Sormani MP, Horakova D, Kalincik T, Vaneckova M (2017) Cognitive clinico-radiological paradox in early stages of multiple sclerosis. Ann Clin Transl Neurol 5:81–91 PubMed PMC
Di Filippo M, Portaccio E, Mancini A, Calabresi P (2018) Multiple sclerosis and cognition: synaptic failure and network dysfunction. Nat Rev Neurosci 19:599–609 PubMed
Penner IK, Stemper B, Calabrese P, Freedman MS, Polman CH, Edan G, Hartung HP, Miller DH, Montalban X, Barkhof F, Pleimes D, Lanius V, Pohl C, Kappos L, Sandbrink R (2012) Effects of interferon beta-1b on cognitive performance in patients with a first event suggestive of multiple sclerosis. Mult Scler 18:1466–1471 PubMed PMC