804
Views
0
CrossRef citations to date
0
Altmetric
Research Article

Investigating the relationship between allocentric spatial working memory and biomarker status in preclinical and prodromal Alzheimer’s disease

ORCID Icon, , , , , , , , & show all

References

  • Albert, M. S., DeKosky, S. T., Dickson, D., Dubois, B., Feldman, H. H., Fox, N. C., Gamst, A., Holtzman, D. M., Jagust, W. J., Petersen, R. C., Snyder, P. J., Carrillo, M. C., Thies, B., & Phelps, C. H. (2011). The diagnosis of mild cognitive impairment due to Alzheimer’s disease: Recommendations from the national institute on aging-Alzheimer’s association workgroups on diagnostic guidelines for Alzheimer’s disease. Alzheimer’s & Dementia : The Journal of the Alzheimer’s Association, 7(3), 270–279. https://doi.org/10.1016/j.jalz.2011.03.008
  • Allison, S. L., Fagan, A. M., Morris, J. C., & Head, D. (2016). Spatial navigation in preclinical Alzheimer’s disease. Journal of Alzheimer’s Disease , 52(1), 77–90. https://doi.org/10.3233/JAD-150855
  • Alzheimer’s Association. (2022). 2022 Alzheimer's disease facts and figures. Alzheimer's & Dementia.18 (3): 700–789. https://doi.org/10.1002/alz.12638
  • Alzheimer’s Disease International. (2015). World Alzheimer Report 2015- The Global Impact of Dementia. https://www.alzint.org/u/WorldAlzheimerReport2015.pdf
  • Arendt, T., Brückner, M. K., Morawski, M., Jäger, C., & Gertz, H.-J. (2015). Early neurone loss in Alzheimer’s disease: cortical or subcortical? Acta Neuropathologica Communications, 3(1), 10. https://doi.org/10.1186/s40478-015-0187-1
  • Bastin, C., Bahri, M. A., Meyer, F., Manard, M., Delhaye, E., Plenevaux, A., Becker, G., Seret, A., Mella, C., Giacomelli, F., Degueldre, C., Balteau, E., Luxen, A., & Salmon, E. (2020). In vivo imaging of synaptic loss in Alzheimer’s disease with [18F]UCB-H positron emission tomography. European Journal of Nuclear Medicine and Molecular Imaging, 47(2), 390–402. https://doi.org/10.1007/s00259-019-04461-x
  • Bennett, D. A., Schneider, J. A., Arvanitakis, Z., Kelly, J. F., Aggarwal, N. T., Shah, R. C., & Wilson, R. S. (2006). Neuropathology of older persons without cognitive impairment from two community-based studies. Neurology, 66(12), 1837–1844. https://doi.org/10.1212/01.wnl.0000219668.47116.e6
  • Berron, D., Vogel, J. W., Insel, P. S., Pereira, J. B., Xie, L., Wisse, L. E. M., Yushkevich, P. A., Palmqvist, S., Mattsson-Carlgren, N., Stomrud, E., Smith, R., Strandberg, O., & Hansson, O. (2021). Early stages of tau pathology and its associations with functional connectivity, atrophy and memory. Brain : A Journal of Neurology, 144(9), 2771–2783. https://doi.org/10.1093/brain/awab114
  • Besson, F. L., La Joie, R., Doeuvre, L., Gaubert, M., Mézenge, F., Egret, S., Landeau, B., Barré, L., Abbas, A., Ibazizene, M., de La Sayette, V., Desgranges, B., Eustache, F., & Chételat, G. (2015). Cognitive and brain profiles associated with current neuroimaging biomarkers of preclinical Alzheimer’s disease. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience, 35(29), 10402–10411. https://doi.org/10.1523/jneurosci.0150-15.2015
  • Bondi, M. W., Edmonds, E. C., Jak, A. J., Clark, L. R., Delano-Wood, L., McDonald, C. R., Nation, D. A., Libon, D. J., Au, R., Galasko, D., & Salmon, D. P. (2014). Neuropsychological criteria for mild cognitive impairment improves diagnostic precision, biomarker associations, and progression rates. Journal of Alzheimer’s Disease, 42(1), 275–289. https://doi.org/10.3233/jad-140276
  • Braak, H., & Del Tredici, K. (2015). The preclinical phase of the pathological process underlying sporadic Alzheimer’s disease. Brain: A Journal of Neurology, 138(Pt 10), 2814–2833. https://doi.org/10.1093/brain/awv236
  • Brucato, M., Frick, A., Pichelmann, S., Nazareth, A., & Newcombe, N. S. (2023). Measuring spatial perspective taking: Analysis of four measures using item response theory. Topics in Cognitive Science, 15(1), 46–74. https://doi.org/10.1111/tops.12597
  • Brun, V. H., Otnass, M. K., Molden, S., Steffenach, H.-A., Witter, M. P., Moser, M.-B., & Moser, E. I. (2002). Place cells and place recognition maintained by direct entorhinal-hippocampal circuitry. Science, 296(5576), 2243–2246. https://doi.org/10.1126/science.1071089
  • Burt, D. B., Zembar, M. J., & Niederehe, G. (1995). Depression and memory impairment: A meta-analysis of the association, its pattern, and specificity. Psychological Bulletin, 117(2), 285–305. https://doi.org/10.1037/0033-2909.117.2.285
  • Chan, D., Gallaher, L. M., Moodley, K., Minati, L., Burgess, N., & Hartley, T. (2016). The 4 mountains test: A short test of spatial memory with high sensitivity for the diagnosis of pre-dementia Alzheimer’s disease. Journal of Visualized Experiments, (116), 54454. https://doi.org/10.3791/54454
  • Collins, D. W., & Kimura, D. (1997). A large sex difference on a two-dimensional mental rotation task. Behavioral Neuroscience, 111(4), 845–849. https://doi.org/10.1037//0735-7044.111.4.845
  • Colombo, D., Serino, S., Tuena, C., Pedroli, E., Dakanalis, A., Cipresso, P., & Riva, G. (2017). Egocentric and allocentric spatial reference frames in aging: A systematic review. Neuroscience and Biobehavioral Reviews, 80, 605–621. https://doi.org/10.1016/j.neubiorev.2017.07.012
  • Coluccia, E., & Louse, G. (2004). Gender differences in spatial orientation: A review. Journal of Environmental Psychology, 24(3), 329–340. https://doi.org/10.1016/j.jenvp.2004.08.006
  • Coughlan, G., Laczó, J., Hort, J., Minihane, A.-M., & Hornberger, M. (2018). Spatial navigation deficits—overlooked cognitive marker for preclinical Alzheimer disease? Nature Reviews. Neurology, 14(8), 496–506. https://doi.org/10.1038/s41582-018-0031-x
  • Derbie, A. Y., Chau, B. K. H., Wong, C. H. Y., Chen, L.-D., Ting, K.-H., Lam, B. Y. H., Lee, T. M. C., Chan, C. C. H., & Smith, Y. (2021). Common and distinct neural trends of allocentric and egocentric spatial coding: An ALE meta-analysis []. The European Journal of Neuroscience, 53(11), 3672–3687. https://doi.org/10.1111/ejn.15240
  • Driscoll, I., Hamilton, D. A., Yeo, R. A., Brooks, W. M., & Sutherland, R. J. (2005). Virtual navigation in humans: The impact of age, sex, and hormones on place learning. Hormones and Behavior, 47(3), 326–335. https://doi.org/10.1016/j.yhbeh.2004.11.013
  • Dubois, B., Feldman, H. H., Jacova, C., Cummings, J. L., Dekosky, S. T., Barberger-Gateau, P., Delacourte, A., Frisoni, G., Fox, N. C., Galasko, D., Gauthier, S., Hampel, H., Jicha, G. A., Meguro, K., O’Brien, J., Pasquier, F., Robert, P., Rossor, M., Salloway, S., … Scheltens, P. (2010). Revising the definition of Alzheimer’s disease: A new lexicon. The Lancet. Neurology, 9(11), 1118–1127. https://doi.org/10.1016/S1474-4422(10)70223-4
  • Dubois, B., Feldman, H. H., Jacova, C., Dekosky, S. T., Barberger-Gateau, P., Cummings, J., Delacourte, A., Galasko, D., Gauthier, S., Jicha, G., Meguro, K., O’brien, J., Pasquier, F., Robert, P., Rossor, M., Salloway, S., Stern, Y., Visser, P. J., & Scheltens, P. (2007). Research criteria for the diagnosis of Alzheimer’s disease: revising the NINCDS–ADRDA criteria. The Lancet. Neurology, 6(8), 734–746. https://doi.org/10.1016/S1474-4422(07)70178-3
  • Dubois, B., Feldman, H. H., Jacova, C., Hampel, H., Molinuevo, J. L., Blennow, K., DeKosky, S. T., Gauthier, S., Selkoe, D., Bateman, R., Cappa, S., Crutch, S., Engelborghs, S., Frisoni, G. B., Fox, N. C., Galasko, D., Habert, M.-O., Jicha, G. A., Nordberg, A., … Cummings, J. L. (2014). Advancing research diagnostic criteria for Alzheimer’s disease: the IWG-2 criteria. The Lancet. Neurology, 13(6), 614–629. https://doi.org/10.1016/S1474-4422(14)70090-0
  • Eliassen, I. V., Fladby, T., Kirsebom, B.-E., Waterloo, K., Eckerström, M., Wallin, A., Bråthen, G., Aarsland, D., & Hessen, E. (2020). Predictive and diagnostic utility of brief neuropsychological assessment in detecting Alzheimer’s pathology and progression to dementia. Neuropsychology, 34(8), 851–861. https://doi.org/10.1037/neu0000698
  • Espenes, J., Hessen, E., Eliassen, I. V., Waterloo, K., Eckerström, M., Sando, S. B., Timón, S., Wallin, A., Fladby, T., & Kirsebom, B.-E. (2020). Demographically adjusted trail making test norms in a Scandinavian sample from 41 to 84 years. The Clinical Neuropsychologist, 34(sup1), 110–126. https://doi.org/10.1080/13854046.2020.1829068
  • Faul, F., Erdfelder, E., Lang, A.-G., & Buchner, A. (2007). G*Power 3: A flexible statistical power analysis program for the social, behavioral, and biomedical sciences. Behavior Research Methods, 39(2), 175–191. https://doi.org/10.3758/BF03193146
  • Fillenbaum, G. G., van Belle, G., Morris, J. C., Mohs, R. C., Mirra, S. S., Davis, P. C., Tariot, P. N., Silverman, J. M., Clark, C. M., Welsh-Bohmer, K. A., & Heyman, A. (2008). Consortium to establish a registry for Alzheimer’s disease (CERAD): the first twenty years. Alzheimer’s & Dementia : The Journal of the Alzheimer’s Association, 4(2), 96–109. https://doi.org/10.1016/j.jalz.2007.08.005
  • Fladby, T., Pålhaugen, L., Selnes, P., Waterloo, K., Bråthen, G., Hessen, E., Almdahl, I. S., Arntzen, K.-A., Auning, E., Eliassen, C. F., Espenes, R., Grambaite, R., Grøntvedt, G. R., Johansen, K. K., Johnsen, S. H., Kalheim, L. F., Kirsebom, B.-E., Müller, K. I., Nakling, A. E., … Aarsland, D. (2017). Detecting at-risk Alzheimer’s disease cases. Journal of Alzheimer’s Disease, 60(1), 97–105. https://doi.org/10.3233/JAD-170231
  • Fu, H., Rodriguez, G. A., Herman, M., Emrani, S., Nahmani, E., Barrett, G., Figueroa, H. Y., Goldberg, E., Hussaini, S. A., & Duff, K. E. (2017). Tau pathology induces excitatory neuron loss, grid cell dysfunction, and spatial memory deficits reminiscent of early Alzheimer’s disease. Neuron, 93(3), 533–541.e535. https://doi.org/10.1016/j.neuron.2016.12.023
  • Fyhn, M., Molden, S., Witter, M. P., Moser, E. I., & Moser, M.-B. (2004). Spatial representation in the entorhinal cortex. Science, 305(5688), 1258–1264. https://doi.org/10.1126/science.1099901
  • Gazova, I., Laczó, J., Rubinova, E., Mokrisova, I., Hyncicova, E., Andel, R., Vyhnalek, M., Sheardova, K., Coulson, E. J., & Hort, J. (2013). Spatial navigation in young versus older adults [Original Research]. Frontiers in Aging Neuroscience, 5, 94. https://doi.org/10.3389/fnagi.2013.00094
  • Hadjichrysanthou, C., Evans, S., Bajaj, S., Siakallis, L. C., McRae-McKee, K., de Wolf, F., … Anderson, R. M, (2020). The dynamics of biomarkers across the clinical spectrum of Alzheimer’s disease. Alzheimer’s Research & Therapy, 12(1), 74. https://doi.org/10.1186/s13195-020-00636-z
  • Hafting, T., Fyhn, M., Molden, S., Moser, M. B., & Moser, E. I. (2005). Microstructure of a spatial map in the entorhinal cortex. Nature, 436(7052), 801–806. https://doi.org/10.1038/nature03721
  • Hansson, O., Lehmann, S., Otto, M., Zetterberg, H., & Lewczuk, P. (2019). Advantages and disadvantages of the use of the CSF Amyloid β (Aβ) 42/40 ratio in the diagnosis of Alzheimer’s Disease. Alzheimer’s Research & Therapy, 11(1), 34. https://doi.org/10.1186/s13195-019-0485-0
  • Hartley, T., Bird, C. M., Chan, D., Cipolotti, L., Husain, M., Vargha-Khadem, F., & Burgess, N. (2007). The hippocampus is required for short-term topographical memory in humans. Hippocampus, 17(1), 34–48. https://doi.org/10.1002/hipo.20240
  • Hort, J., Laczó, J., Vyhnálek, M., Bojar, M., Bureš, J., & Vlček, K. (2007). Spatial navigation deficit in amnestic mild cognitive impairment. Proceedings of the National Academy of Sciences of the United States of America, 104(10), 4042–4047. https://doi.org/10.1073/pnas.0611314104
  • Howett, D., Castegnaro, A., Krzywicka, K., Hagman, J., Marchment, D., Henson, R., Rio, M., King, J. A., Burgess, N., & Chan, D. (2019). Differentiation of mild cognitive impairment using an entorhinal cortex-based test of virtual reality navigation. Brain : A Journal of Neurology, 142(6), 1751–1766. https://doi.org/10.1093/brain/awz116
  • Jack, C. R., Bennett, D. A., Blennow, K., Carrillo, M. C., Dunn, B., Haeberlein, S. B., Holtzman, D. M., Jagust, W., Jessen, F., Karlawish, J., Liu, E., Molinuevo, J. L., Montine, T., Phelps, C., Rankin, K. P., Rowe, C. C., Scheltens, P., Siemers, E., Snyder, H. M., & Sperling, R, (2018). NIA-AA research framework: Toward a biological definition of Alzheimer’s disease. Alzheimer’s & Dementia: The Journal of the Alzheimer’s Association, 14(4), 535–562. https://doi.org/10.1016/j.jalz.2018.02.018
  • Kirsebom, B.-E., Espenes, R., Hessen, E., Waterloo, K., Johnsen, S. H., Gundersen, E., Botne Sando, S., Rolfseng Grøntvedt, G., Timón, S., & Fladby, T. (2019). Demographically adjusted CERAD wordlist test norms in a Norwegian sample from 40 to 80 years. The Clinical Neuropsychologist, 33(sup1), 27–39. https://doi.org/10.1080/13854046.2019.1574902
  • Knudtzon, S., Nordengen, K., Grøntvedt, G. R., Jarholm, J., Eliassen, I. V., Selnes, P., … Kirsebom, B.-E. (2023). Age-adjusted CSF t-tau and NfL have lower diagnostic accuracy for Alzheimer’s disease. [Manuscript submitted for publication].
  • Kozhevnikov, M., Motes, M. A., Rasch, B., & Blajenkova, O. (2006). Perspective-taking vs. mental rotation transformations and how they predict spatial navigation performance []. Applied Cognitive Psychology, 20(3), 397–417. https://doi.org/10.1002/acp.1192
  • Kunz, L., Schröder, T. N., Lee, H., Montag, C., Lachmann, B., Sariyska, R., Reuter, M., Stirnberg, R., Stöcker, T., Messing-Floeter, P. C., Fell, J., Doeller, C. F., & Axmacher, N. (2015). Reduced grid-cell like representations in adults at genetic risk for Alzheimer’s disease. Science , 350(6259), 430–433. https://doi.org/10.1126/science.aac8128
  • 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. Behavioural Brain Research, 202(2), 252–259. https://doi.org/10.1016/j.bbr.2009.03.041
  • Lorentzen, I. M., Espenes, J., Hessen, E., Waterloo, K., Bråthen, G., Timón, S., … Kirsebom, B.-E. (2021). Regression-based norms for the FAS phonemic fluency test for ages 40–84 based on a Norwegian sample. Applied Neuropsychology: Adult, 30 (2), 159–168. https://doi.org/10.1080/23279095.2021.1918128
  • Maass, A., Lockhart, S. N., Harrison, T. M., Bell, R. K., Mellinger, T., Swinnerton, K., Baker, S. L., Rabinovici, G. D., & Jagust, W. J. (2018). Entorhinal tau pathology, episodic memory decline, and neurodegeneration in Aging. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience, 38(3), 530–543. https://doi.org/10.1523/JNEUROSCI.2028-17.2017
  • McNaughton, B. L., Battaglia, F. P., Jensen, O., Moser, E. I., & Moser, M.-B. (2006). Path integration and the neural basis of the ‘cognitive map. Nature Reviews. Neuroscience, 7(8), 663–678. https://doi.org/10.1038/nrn1932
  • Mecca, A. P., Chen, M.-K., O’Dell, R. S., Naganawa, M., Toyonaga, T., Godek, T. A., Harris, J. E., Bartlett, H. H., Zhao, W., Banks, E. R., Ni, G. S., Rogers, K., Gallezot, J. D., Ropchan, J., Emery, P. R., Nabulsi, N. B., Vander Wyk, B. C., Arnsten, A. F. T., Huang, Y., Carson, R. E., & van Dyck, C. H. (2022). Association of entorhinal cortical tau deposition and hippocampal synaptic density in older individuals with normal cognition and early Alzheimer’s disease. Neurobiology of Aging, 111, 44–53. https://doi.org/10.1016/j.neurobiolaging.2021.11.004
  • Moffat, S. D., Elkins, W., & Resnick, S. M. (2006). Age differences in the neural systems supporting human allocentric spatial navigation. Neurobiology of Aging, 27(7), 965–972. https://doi.org/10.1016/j.neurobiolaging.2005.05.011
  • Moodley, K., Minati, L., Contarino, V., Prioni, S., Wood, R., Cooper, R., D’Incerti, L., Tagliavini, F., & Chan, D. (2015). Diagnostic differentiation of mild cognitive impairment due to Alzheimer’s disease using a hippocampus-dependent test of spatial memory. Hippocampus, 25(8), 939–951. https://doi.org/10.1002/hipo.22417
  • Price, J. L., & Morris, J. C. (1999). Tangles and plaques in nondemented aging and “preclinical” Alzheimer’s disease. Annals of Neurology, 45(3), 358–368. https://doi.org/10.1002/1531-8249(199903)45:3 < 358::AID-ANA12 > 3.0.CO;2-X
  • Reitan, R. M., & Wolfson, D. (1985). The Halstead-Reitan Neuropsychological Test Battery. Neuropsychology Press.
  • Ribeiro, F., Guerreiro, M., & De Mendonça, A. (2007). Verbal learning and memory deficits in mild cognitive impairment. Journal of Clinical and Experimental Neuropsychology, 29(2), 187–197. https://doi.org/10.1080/13803390600629775
  • Ritchie, K., Carrière, I., Howett, D., Su, L., Hornberger, M., O’Brien, J. T., Ritchie, C. W., & Chan, D. (2018). Allocentric and egocentric spatial processing in middle-aged adults at high risk of late-onset Alzheimer’s disease: The PREVENT dementia study. Journal of Alzheimer’s Disease, 65(3), 885–896. https://doi.org/10.3233/JAD-180432
  • Rodgers, M. K., Sindone, J. A., & Moffat, S. D. (2012). Effects of age on navigation strategy. Neurobiology of Aging, 33(1), 202.e215–202.e222. https://doi.org/10.1016/j.neurobiolaging.2010.07.021
  • Rye, I., Vik, A., Kocinski, M., Lundervold, A. S., & Lundervold, A. J. (2022). Predicting conversion to Alzheimer’s disease in individuals with Mild Cognitive Impairment using clinically transferable features. Scientific Reports, 12(1), 15566. https://doi.org/10.1038/s41598-022-18805-5
  • Salthouse, T. A. (2000). Aging and measures of processing speed. Biological Psychology, 54(1–3), 35–54. https://doi.org/10.1016/s0301-0511(00)00052-1
  • Siafarikas, N., Kirsebom, B.-E., Srivastava, D. P., Eriksson, C. M., Auning, E., Hessen, E., Selbaek, G., Blennow, K., Aarsland, D., & Fladby, T. (2021). Cerebrospinal fluid markers for synaptic function and Alzheimer type changes in late life depression. Scientific Reports, 11(1), 20375. https://doi.org/10.1038/s41598-021-99794-9
  • Sperling, R. A., Aisen, P. S., Beckett, L. A., Bennett, D. A., Craft, S., Fagan, A. M., Iwatsubo, T., Jack, C. R., Kaye, J., Montine, T. J., Park, D. C., Reiman, E. M., Rowe, C. C., Siemers, E., Stern, Y., Yaffe, K., Carrillo, M. C., Thies, B., Morrison-Bogorad, M., Wagster, M. V., & Phelps, C. H. (2011). Toward defining the preclinical stages of Alzheimer’s disease: Recommendations from the national institute on aging-Alzheimer’s association workgroups on diagnostic guidelines for Alzheimer’s disease. Alzheimer’s & Dementia : The Journal of the Alzheimer’s Association, 7(3), 280–292. https://doi.org/10.1016/j.jalz.2011.03.003
  • Spreen, O., & Benton, A. L. (1969). Neurosensory Center Comprehensive Examination for Aphasia: Manual of instructions (NECCEA). University of Victoria.
  • Tangen, G. G., Nilsson, M. H., Stomrud, E., Palmqvist, S., & Hansson, O. (2022). Spatial navigation and its association with biomarkers and future dementia in memory clinic patients without dementia. Neurology, 99(19), e2081–e2091. https://doi.org/10.1212/wnl.0000000000201106
  • Therriault, J., Pascoal, T. A., Lussier, F. Z., Tissot, C., Chamoun, M., Bezgin, G., Servaes, S., Benedet, A. L., Ashton, N. J., Karikari, T. K., Lantero-Rodriguez, J., Kunach, P., Wang, Y.-T., Fernandez-Arias, J., Massarweh, G., Vitali, P., Soucy, J.-P., Saha-Chaudhuri, P., Blennow, K., … Rosa-Neto, P. (2022). Biomarker modeling of Alzheimer’s disease using PET-based braak staging. Nature Aging, 2(6), 526–535. https://doi.org/10.1038/s43587-022-00204-0
  • Tromp, D., Dufour, A., Lithfous, S., Pebayle, T., & Després, O. (2015). Episodic memory in normal aging and Alzheimer disease: Insights from imaging and behavioral studies. Ageing Research Reviews, 24(Pt B), 232–262. https://doi.org/10.1016/j.arr.2015.08.006
  • Voyer, D., Voyer, S. D., & Saint-Aubin, J. (2017). Sex differences in visual-spatial working memory: A meta-analysis. Psychonomic Bulletin & Review, 24(2), 307–334. https://doi.org/10.3758/s13423-016-1085-7
  • Warrington, E., & James, M. (1991). A new test of object decision: 2D silhouettes featuring a minimal view. Cortex, 27(3), 377–383. https://doi.org/10.1016/S0010-9452(13)80033-0
  • Weisberg, S., & Fox, J. (2019). An R Companion to Applied Regression. Sage.
  • Wickham, H., Averick, M., Bryan, J., Chang, W., McGowan, L., François, R., Grolemund, G., Hayes, A., Henry, L., Hester, J., Kuhn, M., Pedersen, T., Miller, E., Bache, S., Müller, K., Ooms, J., Robinson, D., Seidel, D., Spinu, V., … Yutani, H. (2019). Welcome to the tidyverse. Journal of Open Source Software, 4(43), 1686. https://doi.org/10.21105/joss.01686
  • Wickham, H., Chang, W., Henry, L., Pedersen, T. L., Takahashi, K., Wilke, C., … Dunnington, D. (2016). ggplot2: Elegant graphics for data analysis. In Springer-Verlag.
  • Wickham, H., François, R., Henry, L., & Müller, K. (2022). dplyr: A grammar of data manipulation. In https://dplyr.tidyverse.org, https://github.com/tidyverse/dplyr
  • Wickham, H., Miller, E., & Smith, D. (2022). Haven: Import and export ‘SPSS’, ‘Stata’ and ‘SAS’ Files. In https://haven.tidyverse.org,https://github.com/tidyverse/haven,https://github.com/WizardMac/ReadStat.
  • Yamanami-Irioka, A., Uchihara, T., Endo, T., Irioka, T., Watanabe, M., Kitagawa, M., & Mizusawa, H. (2011). Amnesia in frontotemporal dementia with amyotrophic lateral sclerosis, masquerading Alzheimer’s disease. Case Reports in Neurology, 3(3), 242–247. https://doi.org/10.1159/000331859
  • Zhang, D. (2022). R-squared and related measures. In (Version 2.5) https://CRAN.R-project.org/package=rsq