{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,6]],"date-time":"2026-09-06T00:54:25Z","timestamp":1788656065187,"version":"build-2803163510"},"reference-count":90,"publisher":"SAGE Publications","issue":"1","content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["JAD"],"published-print":{"date-parts":[[2022,3,8]]},"abstract":"<jats:p>Background: Cholinergic deficit and medial temporal lobe (MTL) atrophy are hallmarks of Alzheimer\u2019s disease (AD) leading to early allocentric spatial navigation (aSN) impairment. APOE \u025b4 allele (E4) is a major genetic risk factor for late-onset AD and contributes to cholinergic dysfunction. Basal forebrain (BF) nuclei, the major source of acetylcholine, project into multiple brain regions and, along with MTL and prefrontal cortex (PFC), are involved in aSN processing. Objective: We aimed to determine different contributions of individual BF nuclei atrophy to aSN in E4 positive and E4 negative older adults without dementia and assess whether they operate on aSN through MTL and PFC or independently from these structures. Methods: 120 participants (60 E4 positive, 60 E4 negative) from the Czech Brain Aging Study underwent structural MRI and aSN testing in real-space arena setting. Hippocampal and BF nuclei volumes and entorhinal cortex and PFC thickness were obtained. Associations between brain regions involved in aSN were assessed using MANOVA and complex model of mutual relationships was built using structural equation modelling (SEM). Results: Path analysis based on SEM modeling revealed that BF Ch1-2, Ch4p, and Ch4ai nuclei volumes were indirectly associated with aSN performance through MTL (pch1\u00a0-\u00a02\u200a=\u200a0.039; pch4p\u200a=\u200a0.042) and PFC (pch4ai\u200a=\u200a0.044). In the E4 negative group, aSN was indirectly associated with Ch1-2 nuclei volumes (p\u200a=\u200a0.015), while in the E4 positive group, there was indirect effect of Ch4p nucleus (p\u200a=\u200a0.035). Conclusion: Our findings suggest that in older adults without dementia, BF nuclei affect aSN processing indirectly, through MTL and PFC, and that APOE E4 moderates these associations.<\/jats:p>","DOI":"10.3233\/jad-215034","type":"journal-article","created":{"date-parts":[[2022,1,11]],"date-time":"2022-01-11T13:04:10Z","timestamp":1641906250000},"page":"155-171","source":"Crossref","is-referenced-by-count":5,"title":["APOE \u025b4 Allele Moderates the Association Between Basal Forebrain Nuclei Volumes and Allocentric Navigation in Older Adults Without Dementia"],"prefix":"10.1177","volume":"86","author":[{"given":"Ond\u0159ej","family":"Lerch","sequence":"first","affiliation":[{"name":"Memory Clinic, Department of Neurology, Charles University, Second Faculty of Medicine and Motol University Hospital, Prague, Czechia"},{"name":"International Clinical Research Center, St. Anne\u2019s University Hospital Brno, Brno, Czechia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Martina","family":"Lacz\u00f3","sequence":"additional","affiliation":[{"name":"Memory Clinic, Department of Neurology, Charles University, Second Faculty of Medicine and Motol University Hospital, Prague, Czechia"},{"name":"International Clinical Research Center, St. Anne\u2019s University Hospital Brno, Brno, Czechia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Martin","family":"Vyhn\u00e1lek","sequence":"additional","affiliation":[{"name":"Memory Clinic, Department of Neurology, Charles University, Second Faculty of Medicine and Motol University Hospital, Prague, Czechia"},{"name":"International Clinical Research Center, St. Anne\u2019s University Hospital Brno, Brno, Czechia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zuzana","family":"Nedelsk\u00e1","sequence":"additional","affiliation":[{"name":"Memory Clinic, Department of Neurology, Charles University, Second Faculty of Medicine and Motol University Hospital, Prague, Czechia"},{"name":"International Clinical Research Center, St. Anne\u2019s University Hospital Brno, Brno, Czechia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jakub","family":"Hort","sequence":"additional","affiliation":[{"name":"Memory Clinic, Department of Neurology, Charles University, Second Faculty of Medicine and Motol University Hospital, Prague, Czechia"},{"name":"International Clinical Research Center, St. Anne\u2019s University Hospital Brno, Brno, Czechia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jan","family":"Lacz\u00f3","sequence":"additional","affiliation":[{"name":"Memory Clinic, Department of Neurology, Charles University, Second Faculty of Medicine and Motol University Hospital, Prague, Czechia"},{"name":"International Clinical Research Center, St. Anne\u2019s University Hospital Brno, Brno, 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between Apolipoprotein E genotype and Alzheimer disease","volume":"278","author":"Farrer","year":"1997","journal-title":"JAMA"},{"key":"10.3233\/JAD-215034_ref4","doi-asserted-by":"crossref","first-page":"921","DOI":"10.1126\/science.8346443","article-title":"Gene dose of apolipoprotein E type 4 allele and the risk of Alzheimer\u2019s disease in late onset families","volume":"261","author":"Corder","year":"1993","journal-title":"Science"},{"key":"10.3233\/JAD-215034_ref5","doi-asserted-by":"crossref","first-page":"3903","DOI":"10.1002\/hbm.22447","article-title":"Genetic influence of apolipoprotein E4 genotype on hippocampal morphometry: An=725 surface-based Alzheimer\u2019s disease neuroimaging initiative study","volume":"35","author":"Shi","year":"2014","journal-title":"Hum Brain Mapp"},{"key":"10.3233\/JAD-215034_ref6","doi-asserted-by":"crossref","first-page":"322","DOI":"10.1136\/jnnp.65.3.322","article-title":"Major decrease in the volume of the entorhinal cortex in patients with Alzheimer\u2019s disease carrying the apolipoprotein E \u025b4 allele","volume":"65","author":"Juottonen","year":"1998","journal-title":"J Neurol Neurosurg Psychiatry"},{"key":"10.3233\/JAD-215034_ref7","doi-asserted-by":"crossref","first-page":"12260","DOI":"10.1073\/pnas.92.26.12260","article-title":"Apolipoprotein E4 allele as a predictor of cholinergic deficits and treatment outcome in Alzheimer disease","volume":"92","author":"Poirier","year":"1995","journal-title":"Proc Natl Acad Sci U S A"},{"key":"10.3233\/JAD-215034_ref8","doi-asserted-by":"crossref","first-page":"254","DOI":"10.1037\/0894-4105.16.2.254","article-title":"The apolipoprotein E gene, attention, and brain function","volume":"16","author":"Parasuraman","year":"2002","journal-title":"Neuropsychology"},{"key":"10.3233\/JAD-215034_ref9","doi-asserted-by":"crossref","first-page":"1095","DOI":"10.3233\/JAD-150137","article-title":"The 12 years preceding mild cognitive impairment due to Alzheimer\u2019s disease: The temporal emergence of cognitive decline","volume":"48","author":"Mistridis","year":"2015","journal-title":"J Alzheimers Dis"},{"key":"10.3233\/JAD-215034_ref10","doi-asserted-by":"crossref","first-page":"445","DOI":"10.31887\/DCNS.2013.15.4\/hjahn","article-title":"Memory loss in Alzheimer\u2019s disease","volume":"15","author":"Jahn","year":"2013","journal-title":"Dialogues Clin Neurosci"},{"key":"10.3233\/JAD-215034_ref11","doi-asserted-by":"crossref","first-page":"77","DOI":"10.3233\/JAD-150855","article-title":"Spatial navigation in preclinical Alzheimer\u2019s disease","volume":"52","author":"Allison","year":"2016","journal-title":"J Alzheimers Dis"},{"key":"10.3233\/JAD-215034_ref12","doi-asserted-by":"crossref","first-page":"162","DOI":"10.1097\/WAD.0000000000000009","article-title":"Neuropsychological deficits associated with route learning in Alzheimer disease, MCI, and normal aging","volume":"28","author":"Benke","year":"2014","journal-title":"Alzheimer Dis Assoc Disord"},{"key":"10.3233\/JAD-215034_ref13","doi-asserted-by":"crossref","first-page":"201","DOI":"10.1016\/j.arr.2012.04.007","article-title":"Spatial navigation in normal aging and the prodromal stage of Alzheimer\u2019s disease: Insights from imaging and behavioral studies","volume":"12","author":"Lithfous","year":"2013","journal-title":"Ageing Res Rev"},{"key":"10.3233\/JAD-215034_ref14","first-page":"89","article-title":"Neural correlates of spatial navigation changes in mild cognitive impairment and Alzheimer\u2019s disease","volume":"8","author":"Vl\u010dek","year":"2014","journal-title":"Front Behav Neurosci"},{"key":"10.3233\/JAD-215034_ref15","doi-asserted-by":"crossref","first-page":"496","DOI":"10.1038\/s41582-018-0031-x","article-title":"Spatial navigation deficits \u2014 overlooked cognitive marker for preclinical Alzheimer disease?","volume":"14","author":"Coughlan","year":"2018","journal-title":"Nat Rev Neurol"},{"key":"10.3233\/JAD-215034_ref16","doi-asserted-by":"crossref","first-page":"150","DOI":"10.1016\/j.bbr.2016.03.052","article-title":"Real-space path integration is impaired in Alzheimer\u2019s disease and mild cognitive impairment","volume":"307","author":"Mokrisova","year":"2016","journal-title":"Behav Brain Res"},{"key":"10.3233\/JAD-215034_ref17","doi-asserted-by":"crossref","first-page":"921","DOI":"10.1126\/science.280.5365.921","article-title":"Knowing where and getting there: A human navigation network","volume":"280","author":"Maguire","year":"1998","journal-title":"Science"},{"key":"10.3233\/JAD-215034_ref18","doi-asserted-by":"crossref","first-page":"272","DOI":"10.3389\/fnhum.2018.00272","article-title":"Extrahippocampal contributions to age-related changes in spatial navigation ability","volume":"12","author":"Zhong","year":"2018","journal-title":"Front Hum Neurosci"},{"key":"10.3233\/JAD-215034_ref19","doi-asserted-by":"crossref","first-page":"4042","DOI":"10.1073\/pnas.0611314104","article-title":"Spatial navigation deficit in amnestic mild cognitive impairment","volume":"104","author":"Hort","year":"2007","journal-title":"Proc Natl Acad Sci U S A"},{"key":"10.3233\/JAD-215034_ref20","doi-asserted-by":"crossref","first-page":"252","DOI":"10.1016\/j.bbr.2009.03.041","article-title":"Spatial navigation testing discriminates two types of amnestic mild cognitive impairment","volume":"202","author":"Lacz\u00f3","year":"2009","journal-title":"Behav Brain Res"},{"key":"10.3233\/JAD-215034_ref21","doi-asserted-by":"crossref","first-page":"153","DOI":"10.1159\/000333121","article-title":"From Morris water maze to computer tests in the prediction of Alzheimer\u2019s disease","volume":"10","author":"Lacz\u00f3","year":"2012","journal-title":"Neurodegener Dis"},{"key":"10.3233\/JAD-215034_ref22","doi-asserted-by":"crossref","first-page":"169","DOI":"10.1159\/000321581","article-title":"Spatial navigation and APOE in amnestic mild cognitive impairment","volume":"8","author":"Lacz\u00f3","year":"2011","journal-title":"Neurodegener Dis"},{"key":"10.3233\/JAD-215034_ref23","doi-asserted-by":"crossref","first-page":"676","DOI":"10.1037\/neu0000072","article-title":"APOE and spatial navigation in amnestic MCI: Results from a computer-based test","volume":"28","author":"Lacz\u00f3","year":"2014","journal-title":"Neuropsychology"},{"key":"10.3233\/JAD-215034_ref24","doi-asserted-by":"crossref","first-page":"1473","DOI":"10.3233\/JAD-200615","article-title":"The combined effect of APOE and BDNF Val66Met polymorphisms on spatial navigation in older adults","volume":"78","author":"Lacz\u00f3","year":"2020","journal-title":"J Alzheimers 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MCI","volume":"69","author":"deIpolyi","year":"2007","journal-title":"Neurology"},{"key":"10.3233\/JAD-215034_ref31","doi-asserted-by":"crossref","first-page":"263","DOI":"10.5840\/philstudies19802725","article-title":"The hippocampus as a cognitive map","volume":"27","author":"Breathnach","year":"1980","journal-title":"Philos Stud"},{"key":"10.3233\/JAD-215034_ref32","doi-asserted-by":"crossref","first-page":"239","DOI":"10.1016\/0023-9690(81)90020-5","article-title":"Spatial localization does not require the presence of local cues","volume":"12","author":"Morris","year":"1981","journal-title":"Learn Motiv"},{"key":"10.3233\/JAD-215034_ref33","doi-asserted-by":"crossref","first-page":"4398","DOI":"10.1073\/pnas.070039597","article-title":"Navigation-related structural change in the hippocampi of taxi drivers","volume":"97","author":"Maguire","year":"2000","journal-title":"Proc Natl Acad Sci U S A"},{"key":"10.3233\/JAD-215034_ref34","doi-asserted-by":"crossref","first-page":"801","DOI":"10.1038\/nature03721","article-title":"Microstructure of a spatial map in the entorhinal cortex","volume":"436","author":"Hafting","year":"2005","journal-title":"Nature"},{"key":"10.3233\/JAD-215034_ref35","doi-asserted-by":"crossref","first-page":"758","DOI":"10.1126\/science.1125572","article-title":"Conjunctive representation of position, direction, and velocity in entorhinal cortex","volume":"312","author":"Sargolini","year":"2006","journal-title":"Science"},{"key":"10.3233\/JAD-215034_ref36","doi-asserted-by":"crossref","first-page":"1865","DOI":"10.1126\/science.1166466","article-title":"Representation of geometric borders in the entorhinal cortex","volume":"322","author":"Solstad","year":"2008","journal-title":"Science"},{"key":"10.3233\/JAD-215034_ref37","doi-asserted-by":"crossref","first-page":"572","DOI":"10.1002\/hipo.10114","article-title":"Age-related differences in the functional connectivity of the hippocampus during memory encoding","volume":"13","author":"Grady","year":"2003","journal-title":"Hippocampus"},{"key":"10.3233\/JAD-215034_ref38","doi-asserted-by":"crossref","first-page":"84","DOI":"10.1162\/0898929052880048","article-title":"Aging and the neural correlates of successful picture encoding: Frontal activations compensate for decreased medial-temporal activity","volume":"17","author":"Gutchess","year":"2005","journal-title":"J Cogn Neurosci"},{"key":"10.3233\/JAD-215034_ref39","doi-asserted-by":"crossref","first-page":"386","DOI":"10.1002\/hipo.1109","article-title":"Cholinergic system regulation of spatial representation by the hippocampus","volume":"12","author":"Ikonen","year":"2002","journal-title":"Hippocampus"},{"key":"10.3233\/JAD-215034_ref40","doi-asserted-by":"crossref","first-page":"1185","DOI":"10.1016\/0306-4522(83)90108-2","article-title":"Central cholinergic pathways in the rat: An overview based on an alternative nomenclature (Ch1-Ch6)","volume":"10","author":"Mesulam","year":"1983","journal-title":"Neuroscience"},{"key":"10.3233\/JAD-215034_ref41","doi-asserted-by":"crossref","first-page":"170","DOI":"10.1002\/cne.902140206","article-title":"Cholinergic innervation of cortex by the basal forebrain: Cytochemistry and cortical connections of the septal area, diagonal band nuclei, nucleus basalis (Substantia innominata), and hypothalamus in the rhesus monkey","volume":"214","author":"Mesulam","year":"1983","journal-title":"J Comp Neurol"},{"key":"10.3233\/JAD-215034_ref42","doi-asserted-by":"crossref","first-page":"527","DOI":"10.1002\/(SICI)1096-9861(19961125)375:4<527::AID-CNE1>3.0.CO;2-3","article-title":"Cholinergic innervation of the primate hippocampal formation: II. Effects of fimbria\/fornix transection","volume":"375","author":"Alonso","year":"1996","journal-title":"J Comp Neurol"},{"key":"10.3233\/JAD-215034_ref43","doi-asserted-by":"crossref","first-page":"37","DOI":"10.1002\/cne.902400104","article-title":"An analysis of the origins of the cholinergic and noncholinergic septal projections to the hippocampal formation of the rat","volume":"240","author":"Amaral","year":"1985","journal-title":"J Comp Neurol"},{"key":"10.3233\/JAD-215034_ref44","doi-asserted-by":"crossref","first-page":"410","DOI":"10.3389\/fnhum.2018.00410","article-title":"The neural basis of individual differences in directional sense","volume":"12","author":"Burte","year":"2018","journal-title":"Front Hum Neurosci"},{"key":"10.3233\/JAD-215034_ref45","doi-asserted-by":"crossref","first-page":"415","DOI":"10.3389\/fnhum.2018.00415","article-title":"Resting state connectivity between medial temporal lobe regions and intrinsic cortical networks predicts performance in a path integration task","volume":"12","author":"Izen","year":"2018","journal-title":"Front Hum Neurosci"},{"key":"10.3233\/JAD-215034_ref46","doi-asserted-by":"crossref","first-page":"450","DOI":"10.1056\/NEJM200008173430701","article-title":"Patterns of brain activation in people at risk for Alzheimer\u2019s disease","volume":"343","author":"Bookheimer","year":"2000","journal-title":"N Engl J Med"},{"key":"10.3233\/JAD-215034_ref47","doi-asserted-by":"crossref","first-page":"501","DOI":"10.1212\/01.WNL.0000150885.00929.7E","article-title":"fMRI evidence of compensatory mechanisms in older adults at genetic risk for Alzheimer disease","volume":"64","author":"Bondi","year":"2005","journal-title":"Neurology"},{"key":"10.3233\/JAD-215034_ref48","doi-asserted-by":"crossref","first-page":"127","DOI":"10.1016\/j.neurobiolaging.2017.04.015","article-title":"APOE moderates compensatory recruitment of neuronal resources during working memory processing in healthy older adults","volume":"56","author":"Scheller","year":"2017","journal-title":"Neurobiol Aging"},{"key":"10.3233\/JAD-215034_ref49","doi-asserted-by":"crossref","first-page":"106","DOI":"10.1038\/nrneurol.2012.263","article-title":"Apolipoprotein E and Alzheimer disease: Risk, mechanisms and therapy","volume":"9","author":"Liu","year":"2013","journal-title":"Nat Rev Neurol"},{"key":"10.3233\/JAD-215034_ref50","doi-asserted-by":"crossref","first-page":"e030379","DOI":"10.1136\/bmjopen-2019-030379","article-title":"Czech Brain Aging Study (CBAS): Prospective multicentre cohort study on risk and protective factors for dementia in the Czech Republic","volume":"9","author":"Sheardova","year":"2019","journal-title":"BMJ Open"},{"key":"10.3233\/JAD-215034_ref51","doi-asserted-by":"crossref","first-page":"103208","DOI":"10.1016\/j.jbi.2019.103208","article-title":"The REDCap consortium: Building an international community of software platform partners","volume":"95","author":"Harris","year":"2019","journal-title":"J Biomed Inform"},{"key":"10.3233\/JAD-215034_ref52","doi-asserted-by":"crossref","first-page":"377","DOI":"10.1016\/j.jbi.2008.08.010","article-title":"Research electronic data capture (REDCap)-A metadata-driven methodology and workflow process for providing translational research informatics support","volume":"42","author":"Harris","year":"2009","journal-title":"J Biomed Inform"},{"key":"10.3233\/JAD-215034_ref53","doi-asserted-by":"crossref","first-page":"844","DOI":"10.1016\/j.jalz.2014.01.001","article-title":"A conceptual framework for research on subjective cognitive decline in preclinical Alzheimer\u2019s disease","volume":"10","author":"Jessen","year":"2014","journal-title":"Alzheimers Dement"},{"key":"10.3233\/JAD-215034_ref54","doi-asserted-by":"crossref","first-page":"1160","DOI":"10.1001\/archneur.62.7.1160","article-title":"Mild cognitive impairment as a clinical entity and treatment target","volume":"62","author":"Petersen","year":"2004","journal-title":"Arch Neurol"},{"key":"10.3233\/JAD-215034_ref55","doi-asserted-by":"crossref","first-page":"545","DOI":"10.1016\/S0022-2275(20)43176-1","article-title":"Restriction isotyping of human apolipoprotein E by gene amplification and cleavage with HhaI","volume":"31","author":"Hixson","year":"1990","journal-title":"J Lipid Res"},{"key":"10.3233\/JAD-215034_ref56","doi-asserted-by":"crossref","first-page":"968","DOI":"10.1016\/j.neuroimage.2006.01.021","article-title":"An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest","volume":"31","author":"Desikan","year":"2006","journal-title":"Neuroimage"},{"key":"10.3233\/JAD-215034_ref57","doi-asserted-by":"crossref","first-page":"341","DOI":"10.1016\/S0896-6273(02)00569-X","article-title":"Whole brain segmentation: Automated labeling of neuroanatomical structures in the human brain","volume":"33","author":"Fischl","year":"2002","journal-title":"Neuron"},{"key":"10.3233\/JAD-215034_ref58","doi-asserted-by":"crossref","first-page":"11","DOI":"10.1093\/cercor\/bhg087","article-title":"Automatically parcellating the human cerebral cortex","volume":"14","author":"Fischl","year":"2004","journal-title":"Cereb Cortex"},{"key":"10.3233\/JAD-215034_ref59","doi-asserted-by":"crossref","first-page":"179","DOI":"10.1006\/nimg.1998.0395","article-title":"Cortical surface-based analysis","volume":"9","author":"Dale","year":"1999","journal-title":"Neuroimage"},{"key":"10.3233\/JAD-215034_ref60","doi-asserted-by":"crossref","first-page":"1310","DOI":"10.1109\/TMI.2010.2046908","article-title":"N4ITK: Improved N3 bias correction","volume":"29","author":"Tustison","year":"2010","journal-title":"IEEE Trans Med Imaging"},{"key":"10.3233\/JAD-215034_ref61","doi-asserted-by":"crossref","first-page":"2626","DOI":"10.1093\/brain\/awh589","article-title":"Measurement of basal 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