A novel virtual-reality-based route-learning test suite: Assessing the effects of cognitive aging on navigation

Jan M Wiener, Denise Carroll, Stacey Moeller, Iram Bibi, Dima Ivanova, Peter Allen, Thomas Wolbers, Jan M Wiener, Denise Carroll, Stacey Moeller, Iram Bibi, Dima Ivanova, Peter Allen, Thomas Wolbers

Abstract

Most research groups studying human navigational behavior with virtual environment (VE) technology develop their own tasks and protocols. This makes it difficult to compare results between groups and to create normative data sets for any specific navigational task. Such norms, however, are prerequisites for the use of navigation assessments as diagnostic tools-for example, to support the early and differential diagnosis of atypical aging. Here we start addressing these problems by presenting and evaluating a new navigation test suite that we make freely available to other researchers (https://osf.io/mx52y/). Specifically, we designed three navigational tasks, which are adaptations of earlier published tasks used to study the effects of typical and atypical aging on navigation: a route-repetition task that can be solved using egocentric navigation strategies, and route-retracing and directional-approach tasks that both require allocentric spatial processing. Despite introducing a number of changes to the original tasks to make them look more realistic and ecologically valid, and therefore easy to explain to people unfamiliar with a VE or who have cognitive impairments, we replicated the findings from the original studies. Specifically, we found general age-related declines in navigation performance and additional specific difficulties in tasks that required allocentric processes. These findings demonstrate that our new tasks have task demands similar to those of the original tasks, and are thus suited to be used more widely.

Keywords: Cognitive aging; Navigation; Navigation test; Route learning.

Figures

Fig. 1
Fig. 1
(Top row) Screenshots taken during the learning phase of the route-repetition task. (a) Participants “stand” at the starting position and start the passive transportation along a route by pressing the SPACE bar. (b) Screenshot taken along the route while approaching an intersection. (c) Screenshot taken at the end of the route. Participants initiated the test phase by pressing the SPACE bar. (Bottom row) Screenshots taken during the test phase. (d) Participants were transported from the start point toward the first intersection. (e) Screenshot taken before the distinctive landmarks at the upcoming intersection were visible. (f) Screenshot taken at the end of the navigation phase of a test trial, before the participant has responded
Fig. 2
Fig. 2
Schematic illustrating the directional-approach task, with an overview of one of the environments used in that task. (a) During the encoding phase, participants always approached the intersection with two distinct landmarks positioned at diagonally opposite corners from the street to the south, starting at the black car (c). During the test phase, they approached the same intersection from the street to the east, the west, or the north. Note that the car could not be seen when participants were asked to give their response. Critically, the approaches to the intersection from the east and west were misaligned with the encoding situation by 90°, whereas an approach from the north was misaligned with the encoding situation by 180° (b)
Fig. 3
Fig. 3
Screenshots taken during the directional-approach task. (Upper row) Encoding phase: (a) Participants initiate translation at the beginning of the encoding phase. (b) Screenshot taken during passive transportation toward the intersection. (c) Final position during the encoding phase. Participants then initiate the test phase. (Lower row) Screenshots taken at the end of the translation in the test phase, when approaching the intersection from the west (d), north (e), and east (f)
Fig. 4
Fig. 4
Performance (a, b) and response times (c, d) for the older and younger participants in the route-repetition and the route-retracing tasks as a function of experimental sessions. The horizontal lines in panels a and b represent chance-level performance. The bars represent mean values, the error bars represent standard errors of the means, and we have overlaid the probability density of the participants’ performance or response times at different values. The plots were generated using the ggplot 2 package in R (Wickham, 2016)
Fig. 5
Fig. 5
Performance (left) and response times (right) for the older and younger participant groups in the directional-approach task. The horizontal line in the left plot represents chance level. Note that approaching the intersection from the east or west was misaligned with the encoding view by 90°, whereas approaching the intersection from the north was misaligned with the encoding view by 180°. Bars represent mean values, error bars represent standard errors of the means, and we have overlaid the probability density of participants’ performance or response times at different values. The plots were generated using the ggplot 2 package in R (Wickham, 2016)

References

    1. Allison S, Head D. Route repetition and route reversal: Effects of age and encoding method. Psychology and Aging. 2017;32:220–231. doi: 10.1037/pag0000170.
    1. Bakeman R. Recommended effect size statistics for repeated measures designs. Behavior Research Methods. 2005;37:379–384. doi: 10.3758/BF03192707.
    1. Braak H, Del Tredici K. The preclinical phase of the pathological process underlying sporadic Alzheimer’s disease. Brain. 2015;138:2814–2833. doi: 10.1093/brain/awv236.
    1. de Condappa O, Wiener JM. Human place and response learning: Navigation strategy selection, pupil size and gaze behavior. Psychological Research. 2016;80:82–93. doi: 10.1007/s00426-014-0642-9.
    1. Fjell AM, McEvoy L, Holland D, Dale AM, Walhovd KB. Brain changes in older adults at very low risk for Alzheimer’s disease. Journal of Neuroscience. 2013;33:8237–8242. doi: 10.1523/JNEUROSCI.5506-12.2013.
    1. Gramann K. Embodiment of spatial reference frames and individual differences in reference frame proclivity. Spatial Cognition & Computation. 2013;13:1–25. doi: 10.1080/13875868.2011.589038.
    1. Harris MA, Wolbers T. Ageing effects on path integration and landmark navigation. Hippocampus. 2012;22:1770–1780. doi: 10.1002/hipo.22011.
    1. Hartley T, Maguire EA, Spiers HJ, Burgess N. The well-worn route and the path less traveled: Distinct neural bases of route following and wayfinding in humans. Neuron. 2003;37:877–888. doi: 10.1016/S0896-6273(03)00095-3.
    1. Head D, Isom M. Age effects on wayfinding and route learning skills. Behavioural Brain Research. 2010;209:49–58. doi: 10.1016/j.bbr.2010.01.012.
    1. Hsieh S, Schubert S, Hoon C, Mioshi E, Hodges JR. Validation of the Addenbrooke’s Cognitive Examination III in frontotemporal dementia and Alzheimer’s disease. Dementia and Geriatric Cognitive Disorders. 2013;36:242–250. doi: 10.1159/000351671.
    1. Iaria G, Palermo L, Committeri G, Barton JJS. Age differences in the formation and use of cognitive maps. Behavioural Brain Research. 2009;196:187–191. doi: 10.1016/j.bbr.2008.08.040.
    1. Iglói K, Doeller CF, Berthoz A, Rondi-Reig L, Burgess N. Lateralized human hippocampal activity predicts navigation based on sequence or place memory. Proceedings of the National Academy of Sciences. 2010;107:14466–14471. doi: 10.1073/pnas.1004243107.
    1. Konishi K, Etchamendy N, Roy S, Marighetto A, Rajah N, Bohbot VD. Decreased functional magnetic resonance imaging activity in the hippocampus in favor of the caudate nucleus in older adults tested in a virtual navigation task. Hippocampus. 2013;23:1005–1014. doi: 10.1002/hipo.22181.
    1. Kunz, L., Schröder, T. N., Lee, H., Montag, C., Lachmann, B., Sariyska, R., . . . Axmacher, N. (2015). Reduced grid-cell-like representations in adults at genetic risk for Alzheimer’s disease. Science, 350, 430–433. 10.1126/science.aac8128
    1. Lester AW, Moffat SD, Wiener JM, Barnes CA, Wolbers T. The aging navigational system. Neuron. 2017;95:1019–1035. doi: 10.1016/j.neuron.2017.06.037.
    1. Liu I, Levy RM, Barton JJ, Iaria G. Age and gender differences in various topographical orientation strategies. Brain Research. 2011;1410:112–119. doi: 10.1016/j.brainres.2011.07.005.
    1. Mathuranath PS, Nestor PJ, Berrios GE, Rakowicz W, Hodges JR. A brief cognitive test battery to differentiate Alzheimer’s disease and frontotemporal dementia. Neurology. 2000;55:1613–1620. doi: 10.1212/01.wnl.0000434309.85312.19.
    1. Moffat SD. Aging and spatial navigation: What do we know and where do we go? Neuropsychology Review. 2009;19:478–489. doi: 10.1007/s11065-009-9120-3.
    1. Moffat SD, Kennedy KM, Rodrigue KM, Raz N. Extrahippocampal contributions to age differences in human spatial navigation. Cerebral Cortex. 2007;17:1274–1282. doi: 10.1093/cercor/bhl036.
    1. Moffat SD, Resnick SM. Effects of age on virtual environment place navigation and allocentric cognitive mapping. Behavioral Neuroscience. 2002;116:851–859. doi: 10.1037/0735-7044.116.5.851.
    1. Moffat SD, Zonderman AB, Resnick SM. Age differences in spatial memory in a virtual environment navigation task. Neurobiology of Aging. 2001;22:787–796. doi: 10.1016/S0197-4580(01)00251-2.
    1. Naveh-Benjamin M, Hussain Z, Guez J, Bar-On M. Adult age differences in episodic memory: Further support for an associative-deficit hypothesis. Journal of Experimental Psychology: Learning, Memory, and Cognition. 2003;29:826–837. doi: 10.1037/0278-7393.29.5.826.
    1. Noone P. Addenbrooke’s Cognitive Examination-III. Occupational Medicine. 2015;65:418–420. doi: 10.1093/occmed/kqv041.
    1. O’Malley M, Innes A, Wiener JM. How do we get there? Effects of cognitive aging on route memory. Memory & Cognition. 2018;46:274–284. doi: 10.3758/s13421-017-0763-7.
    1. Pai MC, Jacobs WJ. Topographical disorientation in community-residing patients with Alzheimer’s disease. International Journal of Geriatric Psychiatry. 2004;19:250–252. doi: 10.1002/gps.1081.
    1. Raz, N., Lindenberger, U., Rodrigue, K. M., Kennedy, K. M., Head, D., Williamson, A., . . . Acker, J. D. (2005). Regional brain changes in aging healthy adults: General trends, individual differences and modifiers. Cerebral Cortex, 15, 1676–1689. 10.1093/cercor/bhi044
    1. Ritchie K, Carrière I, Su L, O’Brien JT, Lovestone S, Wells K, Ritchie CW. The midlife cognitive profiles of adults at high risk of late-onset Alzheimer’s disease: The PREVENT study. Alzheimer’s and Dementia. 2017;13:1089–1097. doi: 10.1016/j.jalz.2017.02.008.
    1. Rodgers MK, Sindone JA, III, Moffat SD. Effects of age on navigation strategy. Neurobiology of Aging. 2012;33:202.e15–202.e22. doi: 10.1016/j.neurobiolaging.2010.07.021.
    1. Salthouse TA. The processing-speed theory of adult age differences in cognition. Psychological Review. 1996;103:403–428. doi: 10.1037/0033-295X.103.3.403.
    1. Serino S, Morganti F, Di Stefano F, Riva G. Detecting early egocentric and allocentric impairments deficits in Alzheimer’s disease: An experimental study with virtual reality. Frontiers in Aging Neuroscience. 2015;7:88. doi: 10.3389/fnagi.2015.00088.
    1. Taillade M, N’Kaoua B, Sauzéon H. Age-related differences and cognitive correlates of self-reported and direct navigation performance: The effect of real and virtual test conditions manipulation. Frontiers in Psychology. 2016;6:2034. doi: 10.3389/fpsyg.2015.02034.
    1. Taillade M, Sauzéon H, Arvind Pala P, Déjos M, Larrue F, Gross C, N’Kaoua B. Age-related wayfinding differences in real large-scale environments: Detrimental motor control effects during spatial learning are mediated by executive decline? PLoS ONE. 2013;8:e67193. doi: 10.1371/journal.pone.0067193.
    1. Voermans NC, Petersson KM, Daudey L, Weber B, Van Spaendonck KP, Kremer HP, Fernández G. Interaction between the human hippocampus and the caudate nucleus during route recognition. Neuron. 2004;43:427–435. doi: 10.1016/j.neuron.2004.07.009.
    1. Waller D, Lippa Y. Landmarks as beacons and associative cues: Their role in route learning. Memory & Cognition. 2007;35:910–924. doi: 10.3758/BF03193465.
    1. Watanabe M. Distinctive features of spatial perspective-taking in the elderly. International Journal of Aging and Human Development. 2011;72:225–241. doi: 10.2190/AG.72.3.d.
    1. Weston, P. S., Nicholas, J. M., Lehmann, M., Ryan, N. S., Liang, Y., Macpherson, K., . . . Fox, N. C. (2016). Presymptomatic cortical thinning in familial Alzheimer disease: A longitudinal MRI study. Neurology, 87, 2050–2057.
    1. Wickham H. ggplot2: Elegant graphics for data analysis. New York, NY: Springer; 2016.
    1. Wiener JM, de Condappa O, Harris MA, Wolbers T. Maladaptive bias for extrahippocampal navigation strategies in aging humans. Journal of Neuroscience. 2013;33:6012–6017. doi: 10.1523/JNEUROSCI.0717-12.2013.
    1. Wiener JM, Kmecova H, de Condappa O. Route repetition and route retracing: Effects of cognitive aging. Frontiers in Aging Neuroscience. 2012;4:7. doi: 10.3389/fnagi.2012.00007.
    1. Wolbers T, Wiener JM. Challenges for identifying the neural mechanisms that support spatial navigation: the impact of spatial scale. Frontiers in Human Neuroscience. 2014;8:571. doi: 10.3389/fnhum.2014.00571.
    1. Wood RA, Moodley KK, Lever C, Minati L, Chan D. Allocentric spatial memory testing predicts conversion from mild cognitive impairment to dementia: An initial proof-of-concept study. Frontiers in Neurology. 2016;7:215. doi: 10.3389/fneur.2016.00215.
    1. Zhong JY, Kozhevnikov M. Relating allocentric and egocentric survey-based representations to the self-reported use of a navigation strategy of egocentric spatial updating. Journal of Environmental Psychology. 2016;46:154–175. doi: 10.1016/j.jenvp.2016.04.007.
    1. Zhong, J. Y., Magnusson, K. R., Swarts, M. E., Clendinen, C. A., Reynolds, N. C., Moffat, S. D. (2017). The application of a rodent-based Morris water maze (MWM) protocol to an investigation of age-related differences in human spatial learning. Behavioral Neuroscience 131 (6):470-482.
    1. Zhong JY, Moffat SD. Age-related differences in associative learning of landmarks and heading directions in a virtual navigation task. Frontiers in Aging Neuroscience. 2016;8:122. doi: 10.3389/fnagi.2016.00122.
    1. Zhong JY, Moffat SD. Extrahippocampal contributions to age-related changes in spatial navigation ability. Frontiers in Human Neuroscience. 2018;12:272. doi: 10.3389/fnhum.2018.00272.

Source: PubMed

3
Se inscrever