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Two Immersive Virtual Reality Tasks for the Assessment of Spatial Orientation in Older Adults with and Without Cognitive Impairment: Concurrent Validity, Group Comparison, and Accuracy Results

Published online by Cambridge University Press:  03 June 2021

Raquel Quimas Molina da Costa Open the ORCID record for Raquel Quimas Molina da Costa [Opens in a new window] ,
José Eduardo Pompeu ,
Emerson Moretto ,
Juliana Magalhães Silva ,
Michelle Didone dos Santos ,
Ricardo Nitrini  and
Sonia Maria Dozzi Brucki
Raquel Quimas Molina da Costa*
Affiliation:
Departamento de Neurologia, Faculdade de Medicina da Universidade de São Paulo, Cerqueira César, SP, Brazil
José Eduardo Pompeu
Affiliation:
Departamento de Fisioterapia, Fonoaudiologia e Terapia ocupacional da Faculdade de Medicina da Universidade de São Paulo, Butantã, SP, Brazil
Emerson Moretto
Affiliation:
Departamento de Engenharia de Sistemas Eletrônicos, Escola Politécnica, Universidade de São Paulo, Butantã, SP, Brazil
Juliana Magalhães Silva
Affiliation:
Departamento de Fisioterapia, Fonoaudiologia e Terapia ocupacional da Faculdade de Medicina da Universidade de São Paulo, Butantã, SP, Brazil
Michelle Didone dos Santos
Affiliation:
Departamento de Fisioterapia, Fonoaudiologia e Terapia ocupacional da Faculdade de Medicina da Universidade de São Paulo, Butantã, SP, Brazil
Ricardo Nitrini
Affiliation:
Departamento de Neurologia, Faculdade de Medicina da Universidade de São Paulo, Cerqueira César, SP, Brazil
Sonia Maria Dozzi Brucki
Affiliation:
Departamento de Neurologia, Faculdade de Medicina da Universidade de São Paulo, Cerqueira César, SP, Brazil
*
*Correspondence and reprint requests to: Raquel Quimas Molina da Costa, R. Diniz Cordeiro 30, 3rd floor, Botafogo, Rio de Janeiro – RJ, 22281-100, Brazil. Email: [email protected]. Phone: +55 21 3883-6000
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Abstract

Objective:

Spatial disorientation is common in Alzheimer’s disease (AD), Mild Cognitive Impairment (MCI), and preclinical individuals with AD biomarkers. However, traditional neuropsychological tests lack ecological validity for the assessment of spatial orientation and to date, there is still no gold standard. The current study aimed to determine the validity and accuracy of two virtual reality tasks for the assessment of spatial orientation.

Methods:

We adapted two spatial orientation tasks to immersive virtual environments: a “survey to route” task in which participants had to transfer information from a map to their body position within a maze [Spatial Orientation in Immersive Virtual Environment Test (SOIVET) Maze], and an allocentric-type, route learning task, with well-established topographic landmarks (SOIVET Route). A total of 19 MCI patients and 29 cognitively healthy older adults aged 61–92 participated in this study. Regular neuropsychological assessments were used for correlation analysis and participant performances were compared between groups. Receiver Operating Characteristic (ROC) curve analysis was performed for accuracy.

Results:

The SOIVET Maze correlated with measures of visuoperception, mental rotation, and planning, and was not related to age, educational level, or technology use profile. The SOIVET Route immediate correlated with measures of mental rotation, memory, and visuoconstruction, and was influenced only by education. Both tasks significantly differentiated MCI and control groups, and demonstrated moderate accuracy for the MCI diagnosis.

Conclusion:

Traditional neuropsychological assessment presents limitations and immersive environments allow for the reproduction of complex cognitive processes. The two immersive virtual reality tasks are valid tools for the assessment of spatial orientation and should be considered for cognitive assessments of older adults.

Keywords

Cognitive dysfunctionAlzheimer’s diseaseSpatial navigationValidation studiesBiomedical technologyNeuropsychological tests
Type
Regular Research
Information
Journal of the International Neuropsychological Society , Volume 28 , Issue 5 , May 2022 , pp. 460 - 472
Copyright
Copyright © INS. Published by Cambridge University Press, 2021

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References

REFERENCES

Allison, S., Babulal, G., Stout, S., Barco, P., Carr, D., Fagan, A., … Head, D. (2018). Alzheimer Disease Biomarkers and Driving in Clinically Normal Older Adults. Alzheimer Disease and Associated Disorders, 32(2), 101–106. https://doi.org/10.1097/WAD.0000000000000257 CrossRefGoogle ScholarPubMed
Allison, S. L., Rodebaugh, T. L., Johnston, C., Fagan, A. M., Morris, J. C., & Head, D. (2019). Developing a Spatial Navigation Screening Tool Sensitive to the Preclinical Alzheimer Disease Continuum. Archives of Clinical Neuropsychology. https://doi.org/10.1093/arclin/acz019 CrossRefGoogle Scholar
Astur, R. S., Taylor, L. B., Mamelak, A. N., Philpott, L., & Sutherland, R. J. (2002). Humans with hippocampus damage display severe spatial memory impairments in a virtual Morris water task. Behavioural Brain Research, 132(1), 77–84. https://doi.org/10.1016/S0166-4328(01)00399-0 CrossRefGoogle Scholar
Benke, T., Karner, E., Petermichl, S., Prantner, V., & Kemmler, G. (2014). Neuropsychological deficits associated with route learning in Alzheimer disease, MCI, and normal aging. Alzheimer Disease and Associated Disorders, 28(2), 162–167. https://doi.org/10.1097/WAD.0000000000000009 CrossRefGoogle ScholarPubMed
Benton, A. L., Varney, N. R., & Hamsher, K. D. (1978). Visuospatial judgment: A clinical test. Archives of Neurology, 35(6), 364–367. https://doi.org/10.1001/archneur.1978.00500300038006 CrossRefGoogle ScholarPubMed
Bessi, V., Mazzeo, S., Padiglioni, S., Piccini, C., Nacmias, B., Sorbi, S., & Bracco, L. (2018). From subjective cognitive decline to Alzheimer’s disease: The predictive role of neuropsychological assessment, personality traits, and cognitive reserve. A 7-year follow-up study. Journal of Alzheimer’s Disease, 63(4), 1523–1535. https://doi.org/10.3233/JAD-171180 CrossRefGoogle ScholarPubMed
Bisson, E., Contant, B., Sveistrup, H., & Lajoie, Y. (2007). Functional balance and dual-task reaction times in older adults are improved by virtual reality and biofeedback training. CyberPsychology & Behavior, 10(1), 16–23. https://doi.org/10.1089/cpb.2006.9997 CrossRefGoogle ScholarPubMed
Boccia, M., Di Vita, A., Diana, S., Margiotta, R., Imbriano, L., Rendace, L., … Guariglia, C. (2019). Is losing one’s way a sign of cognitive decay? Topographical memory deficit as an early marker of pathological aging. Journal of Alzheimer’s Disease, 68(2), 679–693. https://doi.org/10.3233/JAD-180890 CrossRefGoogle Scholar
Braak, H., & Braak, E. (1991). Demonstration of amyloid deposits and neurofibrillary changes in whole brain sections. Brain Pathology (Zurich, Switzerland), 1(3), 213–216. https://doi.org/10.1111/j.1750-3639.1991.tb00661.x CrossRefGoogle ScholarPubMed
Camicioli, R., Howieson, D., Lehman, S., & Kaye, J. (1997). Talking while walking: The effect of a dual task in aging and Alzheimer’s disease. Neurology, 48(4), 955–958. https://doi.org/10.1212/WNL.48.4.955 CrossRefGoogle ScholarPubMed
Cerman, J., Ross, A., Laczo, J., Martin, V., Zuzana, N., Ivana, M., … Jakub, H. (2018). Subjective spatial navigation complaints - A frequent symptom reported by patients with subjective cognitive decline, mild cognitive impairment and Alzheimer’s disease. Current Alzheimer Research, 15(3), 219–228. https://doi.org/10.2174/1567205014666171120145349 CrossRefGoogle ScholarPubMed
César, K. G., Yassuda, M. S., Porto, F. H. G., Brucki, S. M. D., & Nitrini, R. (2017). Addenbrooke’s cognitive examination-revised: normative and accuracy data for seniors with heterogeneous educational level in Brazil. International Psychogeriatrics, 29(8), 1345–1353. https://doi.org/10.1017/S1041610217000734 CrossRefGoogle ScholarPubMed
Charlson, M. E., Pompei, P., Ales, K. L., & MacKenzie, C. R. (1987). A new method of classifying prognostic comorbidity in longitudinal studies: development and validation. Journal of Chronic Diseases, 40(5), 373–383.CrossRefGoogle ScholarPubMed
Cogné, M., Taillade, M., N’Kaoua, B., Tarruella, A., Klinger, E., Larrue, F., … Sorita, E. (2017). The contribution of virtual reality to the diagnosis of spatial navigation disorders and to the study of the role of navigational aids: A systematic literature review. Annals of Physical and Rehabilitation Medicine, 60(3), 164–176. https://doi.org/10.1016/j.rehab.2015.12.004 CrossRefGoogle Scholar
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 & Biobehavioral Reviews, 80, 605–621. doi: 10.1016/j.neubiorev.2017.07.012.CrossRefGoogle ScholarPubMed
Coughlan, G., Coutrot, A., Khondoker, M., Minihane, A.-M., Spiers, H., & Hornberger, M. (2019). Toward personalized cognitive diagnostics of at-genetic-risk Alzheimer’s disease. Proceedings of the National Academy of Sciences of the United States of America, 116(19), 9285–9292. https://doi.org/10.1073/pnas.1901600116 CrossRefGoogle ScholarPubMed
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. https://doi.org/10.1038/s41582-018-0031-x CrossRefGoogle Scholar
Coutrot, A., Schmidt, S., Coutrot, L., Pittman, J., Hong, L., Wiener, J. M., … Spiers, H. J. (2019). Virtual navigation tested on a mobile app is predictive of real-world wayfinding navigation performance. PLoS One, 14(3). https://doi.org/10.1371/journal.pone.0213272 CrossRefGoogle Scholar
da Costa, R.Q.M, Pompeu, J.E., de Mello, D.D., Moretto, E., Rodrigues, F.Z., Dos Santos, M.D., … Brucki, S.M.D. (2018). Two new virtual reality tasks for the assessment of spatial orientation: Preliminary results of tolerability, sense of presence and usability. Dementia e Neuropsychologia, 12(2), 196–204. https://doi.org/10.1590/1980-57642018dn12-020013 CrossRefGoogle ScholarPubMed
da Costa, R.Q.M, Pompeu, J.E., Mello, D.D., Moretto, E., Rodrigues, F.Z., Dos Santos, M.D., … Brucki, S.M.D. (2018). A comparison between an immersive virtual reality spatial task and its correspondent paper-and-pencil version with one’s perception of spatial abilities. Alzheimer’s & Dementia, 14(7), P427. https://doi.org/10.1016/j.jalz.2018.06.355 CrossRefGoogle Scholar
da Costa, R.Q.M.D., Pompeu, J.E., Viveiro, L.A.P., & Brucki, S.M.D. (2020). Spatial orientation tasks show moderate to high accuracy for the diagnosis of mild cognitive impairment: a systematic literature review. Arq Neuropsiquiatr, 78(11), 713–723. doi: 10.1590/0004-282X20200043.CrossRefGoogle Scholar
DeIpolyi, A.R., Rankin, K.P., Mucke, L., Miller, B.L., & Gorno-Tempini, M.L. (2007). Spatial cognition and the human navigationnetwork in AD and MCI. Neurology, 69, 986–997.CrossRefGoogle ScholarPubMed
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. doi: 10.1016/j.yhbeh.2004.11.013.CrossRefGoogle ScholarPubMed
Etienne, A.S. & Jeffery, K.J. (2004). Path integration in mammals. Hippocampus, 14(2), 180–192.CrossRefGoogle ScholarPubMed
Fajnerová, I., Rodriguez, M., Levčík, D., Konrádová, L., Mikoláš, P., Brom, C., … Horáček, J. (2014). A virtual reality task based on animal research - spatial learning and memory in patients after the first episode of schizophrenia. Frontiers in Behavioral Neuroscience, 8, 157. doi: 10.3389/fnbeh.2014.00157.CrossRefGoogle ScholarPubMed
Fazekas, F., Chawluk, J.B., Alavi, A., Hurtig, H.I., & Zimmerman, R.A. (1987). MR signal abnormalities at 1.5 T in Alzheimer’s dementia and normal aging. American Journal of Roentgenology, 149(2), 351–356.CrossRefGoogle Scholar
Gallagher, M. & Rapp, P.R. (1997). The use of animal models to study the effects of aging on cognition. Annual Review of Psychology, 48, 339–370. doi: 10.1146/annurev.psych.48.1.339.CrossRefGoogle Scholar
García-Betances, R.I., Jiménez-Mixco, V., Arredondo, M.T., & Cabrera-Umpiérrez, M.F. (2015). Using virtual reality for cognitive training of the elderly. American Journal of Alzheimer’s Disease & Other Dementiasr, 30(1), 49–54. https://doi.org/10.1177/1533317514545866 CrossRefGoogle ScholarPubMed
Gazova, I., Vlcek, K., Laczó, J., Nedelska, Z., Hyncicova, E., Mokrisova, I., … Hort, J. (2012). Spatial navigation-A unique window into physiological and pathological aging. Frontiers in Aging Neuroscience, 4(jun), 16. https://doi.org/10.3389/fnagi.2012.00016 CrossRefGoogle ScholarPubMed
Gramann, K., Onton, J., Riccobon, D., Mueller, H.J., Bardins, S., & Makeig, S. (2010). Human brain dynamics accompanying use of egocentric and allocentric reference frames during navigation. Journal of Cognitive Neuroscience, 22(12), 2836–2849. https://doi.org/10.1162/jocn.2009.21369 CrossRefGoogle ScholarPubMed
Guariglia, C.C. & Nitrini, R. (2009). Topographical disorientation in Alzheimer´s disease. Arquivos de Neuropsiquiaria, 67, 967–972.CrossRefGoogle ScholarPubMed
Hegarty, M., Montello, D.R., Richardson, A.E., Ishikawa, T., & Lovelace, K. (2006). Spatial abilities at different scales: Individual differences in aptitude-test performance and spatial-layout learning. Intelligence, 34(2), 151–176. https://doi.org/10.1016/j.intell.2005.09.005 CrossRefGoogle Scholar
Herting, M.M. & Nagel, B.J. (2012). Aerobic fitness relates to learning on a virtual Morris Water Task and hippocampal volume in adolescents. Behavioural Brain Research, 1, 233(2), 517–525. doi: 10.1016/j.bbr.2012.05.012.CrossRefGoogle ScholarPubMed
Hirsch, P., Nolden, S., & Koch, I. (2017). Higher-order cognitive control in dual tasks: Evidence from task-pair switching. Journal of Experimental Psychology: Human Perception and Performance, 43(3), 569–580. https://doi.org/10.1037/xhp0000309 Google ScholarPubMed
Hort, J., Laczo, J., Vyhnalek, M., Bojar, M., Bures, J., & Vlcek, 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 CrossRefGoogle ScholarPubMed
House, G., Burdea, G., Polistico, K., Roll, D., Kim, J., Grampurohit, N., … Pollack, S. (2016). Integrative rehabilitation of residents chronic post-stroke in skilled nursing facilities: the design and evaluation of the BrightArm Duo. Disability and Rehabilitation: Assistive Technology, 11(8), 683–694. https://doi.org/10.3109/17483107.2015.1068384 Google ScholarPubMed
Howett, D., Castegnaro, A., Krzywicka, K., Hagman, J., Marchment, D., Henson, R., … 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 CrossRefGoogle ScholarPubMed
Iachini, I., Iavarone, A., Senese, V.P., Ruotolo, F., & Ruggiero, G. (2009) Visuospatial memory in healthy elderly, AD and MCI: a review. Current Aging Science, 2(1), 43–59. doi: 10.2174/1874609810902010043.CrossRefGoogle ScholarPubMed
Irish, M., Lawlor, B.A., Coen, R.F., & O’Mara, S.M. (2011). Everyday episodic memory in amnestic mild cognitive impairment: A preliminary investigation. BMC Neuroscience, 12. https://doi.org/10.1186/1471-2202-12-80 CrossRefGoogle Scholar
Jak, A.J., Bondi, M.W., Delano-Wood, L., Wierenga, C., Corey-Bloom, J., Salmon, D.P., & Delis, D.C. (2009). Quantification of five neuropsychological approaches to defining mild cognitive impairment. American Journal of Geriatric Psychiatry, 17, 368–375.CrossRefGoogle ScholarPubMed
Knopman, D.S., Lundt, E.S., Therneau, T.M., Vemuri, P., Lowe, V.J., Kantarci, K., … Jack, C.R. (2019). Entorhinal cortex tau, amyloid-β, cortical thickness and memory performance in non-demented subjects. Brain, 142(4), 1148–1160. https://doi.org/10.1093/brain/awz025 CrossRefGoogle ScholarPubMed
Konishi, K., Joober, R., Poirier, J., MacDonald, K., Chakravarty, M., Patel, R., … Bohbot, V.D. (2018). Healthy versus entorhinal cortical atrophy identification in asymptomatic APOE4 carriers at risk for Alzheimer’s disease. Journal of Alzheimer’s Disease: JAD, 61(4), 1493–1507. https://doi.org/10.3233/JAD-170540 CrossRefGoogle ScholarPubMed
Korotkevich, Y., Trewartha, K.M., Penhune, V.B., & Li, K.Z.H. (2015). Effects of age and cognitive load on response reprogramming. Experimental Brain Research, 233(3), 937–946. https://doi.org/10.1007/s00221-014-4169-5 CrossRefGoogle ScholarPubMed
Kurtz, M.M. (2011). Rivermead behavioral memory test. In Encyclopedia of Clinical Neuropsychology (pp. 2184–2185). New York: Springer. https://doi.org/10.1007/978-0-387-79948-3_1154 CrossRefGoogle Scholar
Laczó, J., Andel, R., Vlček, K., Mat’oška, V., Vyhnálek, M., Tolar, M., … Hort, J. (2011). Spatial navigation and APOE in amnestic mild cognitive impairment. Neurodegenerative Diseases, 8(4), 169–177. https://doi.org/10.1159/000321581 CrossRefGoogle ScholarPubMed
Laczó, J., Andel, R., Vyhnalek, M., Vlcek, K., Magerova, H., Varjassyova, A., … Hort, J. (2010). Human analogue of the morris water maze for testing subjects at risk of Alzheimer’s Disease. Neurodegenerative Diseases, 7(1–3), 148–152. https://doi.org/10.1159/000289226 CrossRefGoogle ScholarPubMed
Laczó, J., Andel, R., Vyhnalek, M., Vlcek, K., Nedelska, Z., Matoska, V., … Hort, J(2014). APOE and spatial navigation in amnestic MCI: Results from a computer-based test. Neuropsychology, 28(5), 676–684. https://doi.org/10.1037/neu0000072 CrossRefGoogle ScholarPubMed
Laczo, J., Vlcek, K., Vyhnalek, M., Vajnerova, O., Ort, M., Holmerova, I., … 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 CrossRefGoogle ScholarPubMed
Laczó, J., Andel, R., Vyhnalek, M., Vlcek, K., Magerova, H., Varjassyova, A., … Hort, J. (2012) From Morris Water Maze to computer tests in the prediction of Alzheimer’s disease. Neurodegenerative Diseases, 10(1–4), 153–157. doi: 10.1159/000333121.CrossRefGoogle ScholarPubMed
LaViola, J. (2000). A discussion of cybersickness in virtual environments. SIGCHI Bulletin, 32(1). https://doi.org/10.1145/333329.333344 CrossRefGoogle Scholar
Lester, A.W., Moffat, S.D., Wiener, J.M., Barnes, C.A., & Wolbers, T. (2017). The Aging navigational system. Neuron, 95(5), 1019–1035. https://doi.org/10.1016/j.neuron.2017.06.037 CrossRefGoogle ScholarPubMed
Li, L., Yu, F., Shi, D., Shi, J., Tian, Z., Yang, J., … Jiang, Q. (2017). Application of virtual reality technology in clinical medicine. American Journal of Translational Research, 9(9), 3867–3880.Google ScholarPubMed
Lithfous, S., Dufour, A., & Després, O. (2013). Spatial navigation in normal aging and the prodromal stage of Alzheimer’s disease: Insights from imaging and behavioral studies. Ageing Research Reviews, 12(1), 201–213. https://doi.org/10.1016/j.arr.2012.04.007 CrossRefGoogle ScholarPubMed
Massetti, T., da Silva, T.D., Crocetta, T.B., Guarnieri, R., de Freitas, B.L., Lopes, P.B., … Monteiro, C.B.M. (2018). The clinical utility of virtual reality in neurorehabilitation: A systematic review. Journal of Central Nervous System Disease, 10, 1179573518813541. https://doi.org/10.1177/1179573518813541 CrossRefGoogle ScholarPubMed
Malloy-Diniz, L.F., Lasmar, V.A.P., Gazinelli, L.S.R., Fuentes, D., & Salgado, J.V. (2007). The rey auditory-verbal learning test: Applicability for the Brazilian elderly population. Brazilian Journal of Psychiatry, 29(4), 324–329.https://doi.org/10.1590/S1516-44462006005000053 CrossRefGoogle ScholarPubMed
McEwen, D., Taillon-Hobson, A., Bilodeau, M., Sveistrup, H., & Finestone, H. (2014). Virtual Reality exercise improves mobility after stroke. Stroke, 45(6), 1853–1855. https://doi.org/10.1161/STROKEAHA.114.005362 CrossRefGoogle ScholarPubMed
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 CrossRefGoogle Scholar
Milner, B. (1971). Interhemispheric differences in the localization of psychological processes in man. British Medical Bulletin, 27(3), 272–277. https://doi.org/10.1093/oxfordjournals.bmb.a070866 CrossRefGoogle ScholarPubMed
Miniaci, M.C. & De Leonibus, E. (2018). Missing the egocentric spatial reference: a blank on the map. F1000Research, 9(7), 168. https://doi.org/10.12688/f1000research.13675.1 CrossRefGoogle Scholar
Mioshi, E., Dawson, K., Mitchell, J., Arnold, R., & Hodges, J.R. (2006). The Addenbrooke’s Cognitive Examination Revised (ACE-R): a brief cognitive test battery for dementia screening. International Journal of Geriatric Psychiatry, 21(11), 1078–1085. https://doi.org/10.1002/gps.1610 CrossRefGoogle ScholarPubMed
Mitolo, M., Gardini, S., Fasano, F., Crisi, G., & Pelosi, A. (2013). Visuospatial Memory and neuroimaging correlates in mild cognitive impairment. Journal of Alzheimer´s Disease, 35, 75–90. https://doi.org/10.3233/JAD-121288 CrossRefGoogle ScholarPubMed
Moffat, S.D. & Resnick, S.M. (2002). Effects of age on virtual environment place navigation and allocentric cognitive mapping. Behavioral Neuroscience, 116(5), 851–859. https://doi.org/10.1037/0735-7044.116.5.851 CrossRefGoogle ScholarPubMed
Moghaddam, M. & Bures, J. (1996) Contribution of egocentric spatial memory to place navigation of rats in the Morris water maze. Behavioural Brain Research, 78(2), 121–129. doi: 10.1016/0166-4328(95)00240-5.CrossRefGoogle ScholarPubMed
Mokrisova, I., Laczo, J., Andel, R., Gazova, I., Vyhnalek, M., Nedelska, Z., … Hort, J. (2016). Real-space path integration is impaired in Alzheimer’s disease and mild cognitive impairment. Behavioural Brain Research, 307, 150–158. https://doi.org/10.1016/j.bbr.2016.03.052 CrossRefGoogle ScholarPubMed
Money, J., Alexander, D., & Walker, H. (1967). A Standardized Road-Map Test of Direction Sense. Baltimore: Johns Hopkins Press.Google Scholar
Montero-Odasso, M., Sarquis-Adamson, Y., Speechley, M., Borrie, M.J., Hachinski, V.C., Wells, J., … Muir-Hunter, S. (2017). Association of dual-task gait with incident dementia in mild cognitive impairment: Results from the gait and brain study. JAMA Neurology, 74(7), 857–865. https://doi.org/10.1001/jamaneurol.2017.0643 LK -CrossRefGoogle ScholarPubMed
Moodley, K., Minati, L., Contarino, V., Prioni, S., Wood, R., Cooper, R., … 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 CrossRefGoogle ScholarPubMed
Morganti, F., Marrakchi, S., Urban, P.P., Iannoccari, G., & Riva, G. (2009). A virtual reality based tool for the assessment of “ survey to route ” spatial organization ability in elderly population : preliminary data. Cognitive Neuroscience, 10(Suppl 2), 257–259. https://doi.org/10.1007/s10339-009-0284-9 Google ScholarPubMed
Morganti, F. & Riva, G. (2014). Virtual reality as allocentric/egocentric technology for the assessment of cognitive decline in the elderly. Studies in Health Technology and Informatics, 196, 278–284.Google ScholarPubMed
Morganti, F., Stefanini, S., & Riva, G. (2013). From allo- to egocentric spatial ability in early Alzheimer’s disease: a study with virtual reality spatial tasks. Cognitive Neuroscience, 4(3–4), 171–180. https://doi.org/10.1080/17588928.2013.854762 CrossRefGoogle ScholarPubMed
Nedelska, Z., Andel, R., Laczó, J., Vlcek, K., Horinek, D., Lisy, J., … Hort, J. (2012). Spatial navigation impairment is proportional to right hippocampal volume. Proceedings of the National Academy of Sciences of the United States of America, 109(7), 2590–2594. https://doi.org/10.1073/pnas.1121588109 CrossRefGoogle ScholarPubMed
Negut, A., Andrei-Matu, S., Sava, F.A., & David, D. (2016). Task difficulty of virtual reality-based assessment tools compared to classical paper-and-pencil or computerized measures: A meta-analytic approach. Computers in Human Behavio, 54, 414–424.CrossRefGoogle Scholar
Optale, G., Urgesi, C., Busato, V., Marin, S., Piron, L., Priftis, K., … Bordin, A. (2010). Controlling memory impairment in elderly adults using virtual reality memory training: A randomized controlled pilot study. Neurorehabilitation and Neural Repair, 24(4), 348–357. https://doi.org/10.1177/1545968309353328 CrossRefGoogle ScholarPubMed
Pengas, G., Patterson, K., Arnold, R.J., Bird, C.M., Burgess, N., & Nestor, P.J. (2010). Lost and found: Bespoke memory testing for Alzheimer’s disease and semantic dementia. Journal of Alzheimer’s Disease, 21(4), 1347–1365. https://doi.org/10.3233/JAD-2010-100654 CrossRefGoogle ScholarPubMed
Peter, J., Sandkamp, R., Minkova, L., Schumacher, L.V, Kaller, C.P., Abdulkadir, A., & Kloeppel, S. (2018). Real-world navigation in amnestic mild cognitive impairment: The relation to visuospatial memory and volume of hippocampal subregions. Neuropsychologia, 109, 86–94. https://doi.org/10.1016/j.neuropsychologia.2017.12.014 CrossRefGoogle ScholarPubMed
Petersen, R.C. (2004). Mild cognitive impairment as a diagnostic entity. Journal of Internal Medicine, 256(3), 183–194. https://doi.org/10.1111/j.1365-2796.2004.01388.x CrossRefGoogle ScholarPubMed
Pickering, C.E.Z., Ridenour, K., Salaysay, Z., Reyes-Gastelum, D., & Pierce, S.J. (2018). EATI Island – A virtual-reality-based elder abuse and neglect educational intervention. Gerontology & Geriatrics Education, 39(4), 445–463. https://doi.org/10.1080/02701960.2016.1203310 CrossRefGoogle ScholarPubMed
Plancher, G., Tirard, A., Gyselinck, V., Nicolas, S., & Piolino, P. (2012). Using virtual reality to characterize episodic memory profiles in amnestic mild cognitive impairment and Alzheimer’s disease: Influence of active and passive encoding. Neuropsychologia, 50(5), 592–602. https://doi.org/10.1016/j.neuropsychologia.2011.12.013 CrossRefGoogle ScholarPubMed
Ritchie, K, Carrière, I, Howett, D, Su, L, Hornberger, M, O’Brien, JT, Ritchie, CW, 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 Alzheimerʼs Disease, 65(3), 885–896. doi: 10.3233/JAD-180432 CrossRefGoogle ScholarPubMed
Riva, G. (2018). The neuroscience of body memory: From the self through the space to the others. Cortex, 104, 241–260. https://doi.org/10.1016/J.CORTEX.2017.07.013 CrossRefGoogle ScholarPubMed
Ruggiero, G., Iavarone, A., & Iachini, T. (2018) Allocentric to Egocentric Spatial Switching: Impairment in aMCI and Alzheimer’s Disease Patients? Current Alzheimer Research, 15(3), 229–236. doi: 10.2174/1567205014666171030114821.CrossRefGoogle ScholarPubMed
Ruggiero, G., Ruotolo, F., Iavarone, A., & Iachini, T. (2020) Allocentric coordinate spatial representations are impaired in aMCI and Alzheimer’s disease patients. Behavioural Brain Research, 1(393), 112793. doi: 10.1016/j.bbr.2020.112793.CrossRefGoogle Scholar
Rusconi, M.L., Suardi, A., Zanetti, M., & Rozzini, L.(2015). Spatial navigation in elderly healthy subjects, amnestic and non amnestic MCI patients. Journal of the Neurological Sciences, 359(1–2), 430–437. https://doi.org/10.1016/j.jns.2015.10.010 CrossRefGoogle ScholarPubMed
Serino, S, Morganti, F., Colombo, D., Pedroli, E., Cipresso, P., & Riva, G. (2018). Disentangling the contribution of spatial reference frames to executive functioning in healthy and pathological aging: An experimental study with virtual reality. Sensors (Switzerland), 18(6). https://doi.org/10.3390/s18061783 CrossRefGoogle Scholar
Serino, S., Cipresso, P., Morganti, F., & Riva, G. (2014). The role of egocentric and allocentric abilities in Alzheimer’s disease: A systematic review. Ageing Research Reviews, 16, 32–44. https://doi.org/10.1016/j.arr.2014.04.004 CrossRefGoogle ScholarPubMed
Shallice, T. (1982). Specific Impairments of Planning. Philosophical Transactions of the Royal Society B: Biological Sciences, 298(1089), 199–209. https://doi.org/10.1098/rstb.1982.0082 Google ScholarPubMed
Sneider, J.T., Hamilton, D.A., Cohen-Gilbert, J.E., Crowley, D.J., Rosso, I.M., & Silveri, M.M. (2015). Sex differences in spatial navigation and perception in human adolescents and emerging adults. Behavioural Processes, 111, 42–50. doi: 10.1016/j.beproc.2014.11.015.CrossRefGoogle ScholarPubMed
Tarnanas, I., Laskaris, N., Tsolaki, M., Muri, R., Nef, T., & Mosimann, U.P. (2015) On the comparison of a novel serious game and electroencephalography biomarkers for early dementia screening. Advances in Experimental Medicine and Biology, 821, 63–77. doi: 10.1007/978-3-319-08939-3_11.CrossRefGoogle ScholarPubMed
Vann, S.D., Aggleton, J.P., & Maguire, E.A. (2009). What does the retrosplenial cortex do? Nature Reviews Neuroscience, 10(11), 792–802. https://doi.org/10.1038/nrn2733 CrossRefGoogle Scholar
Virk, S. & McConville, K.M.V. (2006). Virtual Reality Applications in Improving Postural Control and Minimizing Falls. 2006 International Conference of the IEEE Engineering in Medicine and Biology Society, 2694–2697. https://doi.org/10.1109/IEMBS.2006.260751 CrossRefGoogle Scholar
Vlček, K. & Laczó, J. (2014). Neural correlates of spatial navigation changes in mild cognitive impairment and Alzheimer’s disease. Frontiers in Behavioral Neuroscience, 8(March), 89. https://doi.org/10.3389/fnbeh.2014.00089 Google ScholarPubMed
Weakley, A. & Schmitter-Edgecombe, M. (2019). Naturalistic assessment of task interruption in individuals with mild cognitive impairment. Neuropsychology, 33(1), 1–12. https://doi.org/10.1037/neu0000481 CrossRefGoogle ScholarPubMed
Wolbers, T., Wiener, J.M., Mallot, H.A., & Büchel, C. (2007). Differential recruitment of the hippocampus, medial prefrontal cortex, and the human motion complex during path integration in humans. The Journal of Neuroscience : The Official Journal of the Society for Neuroscience, 27(35), 9408–9416. https://doi.org/10.1523/JNEUROSCI.2146-07.2007 CrossRefGoogle ScholarPubMed
Youden, W.J. (1950). Index for rating diagnostic tests. Cancer, 3(1), 32–35. https://doi.org/10.1002/1097-0142(1950)3:1<32:aid-cncr2820030106>3.0.co;2-3 3.0.CO;2-3>CrossRefGoogle ScholarPubMed