Abstract
The ability to accurately recall locations and navigate our environment relies on multiple cognitive mechanisms. The behavioural and neural correlates of spatial navigation have been repeatedly examined using different types of mazes and tasks with animals. Accurate performances of many of these tasks have proven to depend on specific circuits and brain structures and some have become the standard test of memory in many disease models. With the introduction of virtual reality (VR) to neuroscience research, VR tasks have become a popular method of examining human spatial memory and navigation. However, the types of VR tasks used to examine navigation across laboratories appears to greatly differ, from open arena mazes and virtual towns to driving simulators. Here, we examined over 200 VR navigation papers, and found that the most popular task used is the virtual analogue of the Morris water maze (VWM). Although we highlight the many advantages of using the VWM task, there are also some major difficulties related to the widespread use of this behavioural method. Despite the task’s popularity, we demonstrate an inconsistency of use – particularly with respect to the environmental setup and procedures. Using different versions of the virtual water maze makes replication of findings and comparison of results across researchers very difficult. We suggest the need for protocol and design standardisation, alongside other difficulties that need to be addressed, if the virtual water maze is to become the ‘gold standard’ for human spatial research similar to its animal counterpart.
-
Author contributions: All the authors have accepted responsibility for the entire content of this submitted manuscript and approved submission.
-
Research funding: None declared.
-
Conflict of interest statement: The authors declare no conflicts of interest regarding this article.
References
Aadland, J., Beatty, W.W., and Maki, R.H. (1985). Spatial memory of children and adults assessed in the radial maze. Dev. Psychobiol. 18: 163–172, https://doi.org/10.1002/dev.420180208.Search in Google Scholar
Aida, J., Chau, B., and Dunn, J. (2018). Immersive virtual reality in traumatic brain injury rehabilitation: a literature review. NeuroRehabilitation 42: 441–448, https://doi.org/10.3233/nre-172361.Search in Google Scholar
Antonova, E., Parslow, D., Brammer, M., Simmons, A., Williams, S., Dawson, G.R., and Morris, R. (2011). Scopolamine disrupts hippocampal activity during allocentric spatial memory in humans: an fMRI study using a virtual reality analogue of the Morris water maze. J. Psychopharmacol. 25: 1256–1265, https://doi.org/10.1177/0269881110379285.Search in Google Scholar
Aronov, D., and Tank, D.W. (2014). Engagement of neural circuits underlying 2D spatial navigation in a rodent virtual reality system. Neuron 84: 442–456, https://doi.org/10.1016/j.neuron.2014.08.042.Search in Google Scholar
Astur, R.S., Taylor, L.B., Mamelak, A.N., Philpott, L., and Sutherland, R.J. (2002). Humans with hippocampus damage display severe spatial memory impairments in a virtual Morris water task. Behav. Brain Res. 132: 77–84, https://doi.org/10.1016/s0166-4328(01)00399-0.Search in Google Scholar
Astur, R.S., Tropp, J., Sava, S., Constable, R.T., and Markus, E.J. (2004). Sex differences and correlations in a virtual Morris water task, a virtual radial arm maze, and mental rotation. Behav. Brain Res. 151: 103–115, https://doi.org/10.1016/j.bbr.2003.08.024.Search in Google Scholar
Barnes, C.A. (1979). Memory deficits associated with senescence: a neurophysiological and behavioural study in the rat. J. Comp. Physiol. Psychol. 93: 74–104, https://doi.org/10.1037/h0077579.Search in Google Scholar
Barnhart, C.D., Yang, D., and Lein, P.J. (2015). Using the Morris water maze to assess spatial learning and memory in weanling mice. PloS One 10: e0124521, https://doi.org/10.1371/journal.pone.0124521.Search in Google Scholar
Barrash, J., Damasio, H., Adolphs, R., and Tranel, D. (2000). The neuroanatomical correlates of route learning impairment. Neuropsychologia 38: 820–836, https://doi.org/10.1016/s0028-3932(99)00131-1.Search in Google Scholar
Barry, D.N., and Commins, S. (2019). A novel control condition for spatial learning in the Morris water maze. J. Neurosci. Methods 318: 1–5, https://doi.org/10.1016/j.jneumeth.2019.02.015.Search in Google Scholar PubMed
Bécu, M., Sheynikhovich, D., Tatur, G., Agathos, C.P., Bologna, L.L., Sahel, J.-A., and Arleo, A. (2020). Age-related preference for geometric spatial cues during real-world navigation. Nat. Hum. Behav. 4: 88–99, https://doi.org/10.1038/s41562-019-0718-z.Search in Google Scholar
Bianchini, F., Incoccia, C., Palermo, L., Piccardi, L., Zompanti, L., Sabatini, U., Peran, P., and Guariglia, C. (2010). Developmental topographical disorientation in a healthy subject. Neuropsychologia 48: 1563–1573, https://doi.org/10.1016/j.neuropsychologia.2010.01.025.Search in Google Scholar
Bingman, V.P., Ioalé, P., Casini, G., and Bagnoli, P. (1988). Unimpaired acquisition of spatial reference memory, but impaired homing performance in hippocampal-ablated pigeons. Behav. Brain Res. 27: 179–187, https://doi.org/10.1016/0166-4328(88)90043-5.Search in Google Scholar
Bingman, V.P., Ioale, P., Casini, G., and Bagnoli, P. (1990). The avian hippocampus: evidence for a role in the development of the homing pigeon navigational map. Behav. Neurosci. 104: 906, https://doi.org/10.1037/0735-7044.104.6.906.Search in Google Scholar
Bischof, W.F., and Boulanger, P. (2003). Spatial navigation in virtual reality environments: an EEG analysis. Cyberpsychol. Behav. 6: 487–495, https://doi.org/10.1089/109493103769710514.Search in Google Scholar
Bohbot, V.D.R., Ruzicka, E., Nadel, L., Kalina, M., Stepánková, K., and Bures, J. (2002). Rat spatial memory tasks adapted for humans: characterization in subjects with intact brain and subjects with selective medial temporal lobe thermal lesions. Physiol. Res. 52: 49–65.Search in Google Scholar
Bohil, C.J., Alicea, B., and Biocca, F.A. (2011). Virtual reality in neuroscience research and therapy. Nat. Rev. Neurosci. 12: 752–762, https://doi.org/10.1038/nrn3122.Search in Google Scholar
Bolhuis, J.J., Bijlsma, S., and Ansmink, P. (1986). Exponential decay of spatial memory of rats in a radial maze. Behav. Neural. Biol. 46: 115–122, https://doi.org/10.1016/s0163-1047(86)90584-4.Search in Google Scholar
Boulanger, P., Torres, D., and Bischof, W.F. (2004). MANDALA: a reconfigurable VR environment for studying spatial navigation in humans using EEG. EGVE EGVE04: 61–70, https://doi.org/10.2312/EGVE/EGVE04/061-070.Search in Google Scholar
Bures, J., Fenton, A.A., Kaminsky, Yu., and Ziniuk, L. (1997). Place cells and place navigation. Proc. Natl. Acad. Sci. USA 94: 343–350, https://doi.org/10.1073/pnas.94.1.343.Search in Google Scholar PubMed PubMed Central
Bures, J., and Fenton, A.A. (2000). Neurophysiology of spatial cognition. News Physiol. Sci. 15: 233–240, https://doi.org/10.1152/physiologyonline.2000.15.5.233.Search in Google Scholar PubMed
Cánovas, R., Espínola, M., Iribarne, L., and Cimadevilla, J.M. (2008). A new virtual task to evaluate human place learning. Behav. Brain Res. 190: 112–118, https://doi.org/10.1016/j.bbr.2008.02.024.Search in Google Scholar PubMed
Cimadevilla, J.M., Cánovas, R., Iribarne, L., Soria, A., and López, L. (2011). A virtual-based task to assess place avoidance in humans. J. Neurosci. Methods 196: 45–50, https://doi.org/10.1016/j.jneumeth.2010.12.026.Search in Google Scholar PubMed
Cimadevilla, J.M., Conejo Jiménez, N.M., Miranda García, R., and Arias Pérez, J.L. (2004). Sex differences in the Morris water maze in young rats: temporal dimensions. Psicothema 16: 611–614.Search in Google Scholar
Cimadevilla, J.M., Roldán, M.D., Paris, M., Arnedo, M., and Roldán, S. (2014). Spatial learning in a virtual reality-based task is altered in very preterm children. J. Clin. Exp. Neuropsychol. 36: 1002–8, https://doi.org/10.1080/13803395.2014.963520.Search in Google Scholar PubMed
Cogné, M., Taillade, M., N’Kaoua, B., Tarruella, A., Klinger, E., Larrue, F., Sauzéon, H., Joseph, P.-A., and 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. Ann. Phys. Rehabil. Med. 60: 164–176, https://doi.org/10.1016/j.rehab.2015.12.004.Search in Google Scholar PubMed
Commins, S. (2018). Behavioural neuroscience. Cambridge, UK: Cambridge University Press.10.1017/9781316221655Search in Google Scholar
Commins, S., Duffin, J., Chaves, K., Leahy, D., Corcoran, K., and Caffrey, M., et al. (2020). NavWell: a simplified virtual-reality platform for spatial navigation and memory experiments. Behav. Res. Methods 52: 1189–1207, https://doi.org/10.3758/s13428-019-01310-5.Search in Google Scholar PubMed
Commins, S., and Kirby, B.P. (2019). The complexities of behavioural assessment in neurodegenerative disorders: a focus on Alzheimer’s disease. Pharmacol. Res. 147: 104363, https://doi.org/10.1016/j.phrs.2019.104363.Search in Google Scholar PubMed
Commins, S., McCormack, K., Callinan, E., Fitzgerald, H., Molloy, E., and Young, K. (2013). Manipulation of visual information does not change the accuracy of distance estimation during a blindfolded walking task. Hum. Mov. Sci. 32: 794–807, https://doi.org/10.1016/j.humov.2013.04.003.Search in Google Scholar PubMed
Cornwell, B.R., Salvadore, G., Colon-Rosario, V., Latov, D.R., Holroyd, T., Carver, F.W., Coppola, R., Manji, H.K., Zarate, C.A.Jr., and Grillon, C. (2010). Abnormal hippocampal functioning and impaired spatial navigation in depressed individuals: evidence from whole-head magnetoencephalography. Am. J. Psychiatry 167: 836–844, https://doi.org/10.1176/appi.ajp.2009.09050614.Search in Google Scholar PubMed PubMed Central
Coutrot, A., Schmidt, S., Coutrot, L., Pittman, J., Hong, L., Wiener, J.M., Hölscher, C., Dalton, R.C., Hornberger, M., and Spiers, H.J. (2019). Virtual navigation tested on a mobile app is predictive of real-world wayfinding navigation performance. PloS One 14: e0213272, https://doi.org/10.1371/journal.pone.0213272.Search in Google Scholar PubMed PubMed Central
Crusio, W.E., Schwegler, H., and Lipp, H.P. (1987). Radial-maze performance and structural variation of the hippocampus in mice: a correlation with mossy fibre distribution. Brain Res. 425: 182–185, https://doi.org/10.1016/0006-8993(87)90498-7.Search in Google Scholar
Devan, B.D., Parente, R., Coppola, J.M., Hendricks, M.A., and Johnson, C. (2018). Reproducibility of incentive motivation effects on standard place task performance of the virtual Morris water maze in humans: neuropsychological implications. JASNH 15: 14–22.Search in Google Scholar
D’Hooge, R., and De Deyn, P.P. (2001). Applications of the Morris water maze in the study of learning and memory. Brain Res. Rev. 36: 60–90, https://doi.org/10.1016/s0165-0173(01)00067-4.Search in Google Scholar
Daugherty, A.M., Bender, A.R., Yuan, P., and Raz, N. (2016). Changes in search path complexity and length during learning of a virtual water maze: age differences and differential associations with hippocampal subfield volumes. Cereb. Cortex 26: 2391–2401, https://doi.org/10.1093/cercor/bhv061.Search in Google Scholar PubMed PubMed Central
Daugherty, A.M., and Raz, N. (2017). A virtual water maze revisited: two-year changes in navigation performance and their neural correlates in healthy adults. NeuroImage 146: 492–506, https://doi.org/10.1016/j.neuroimage.2016.09.044.Search in Google Scholar PubMed PubMed Central
Daugherty, A.M., Yuan, P., Dahle, C.L., Bender, A.R., Yang, Y., and Raz, N. (2015). Path complexity in virtual water maze navigation: differential associations with age, sex, and regional brain volume. Cereb. Cortex 25: 3122–3131, https://doi.org/10.1093/cercor/bhu107.Search in Google Scholar PubMed PubMed Central
Deacon, R.M., Bannerman, D.M., and Rawlins, N.P. (2001). Conditional discriminations based on external and internal cues in rats with cytotoxic hippocampal lesions. Behav. Neurosci. 115: 43–57, https://doi.org/10.1037/0735-7044.115.1.43.Search in Google Scholar PubMed
Deacon, R.M.J., and Rawlins, J.N.P. (2006). T-maze alternation in the rodent. Nat. Protoc. 1: 7–12, https://doi.org/10.1038/nprot.2006.2.Search in Google Scholar PubMed
Diersch, N., and Wolbers, T. (2019). The potential of virtual reality for spatial navigation research across the adult lifespan. J. Exp. Biol. 222: jeb187252, https://doi.org/10.1242/jeb.187252.Search in Google Scholar PubMed
Driscoll, I., Hamilton, D.A., Yeo, R.A., Brooks, W.M., and Sutherland, R.J. (2005). Virtual navigation in humans: the impact of age, sex, and hormones on place learning. Horm. Behav. 47: 326–335, https://doi.org/10.1016/j.yhbeh.2004.11.013.Search in Google Scholar PubMed
Duff, S.J., and Hampson, E. (2001). A sex difference on a novel spatial working memory task in humans. Brain Cognit. 47: 470–493, https://doi.org/10.1006/brcg.2001.1326.Search in Google Scholar PubMed
Ehinger, B.V., Fischer, P., Gert, A.L., Kaufhold, L., Weber, F., Pipa, G., and König, P. (2014). Kinesthetic and vestibular information modulate alpha activity during spatial navigation: a mobile EEG study. Front. Hum. Neurosci. 8: 71, https://doi.org/10.3389/fnhum.2014.00071.Search in Google Scholar
Eichenbaum, H., Stewart, C., and Morris, R.G. (1990). Hippocampal representation in place learning. J. Neurosci. 10: 3531–3542, https://doi.org/10.1523/jneurosci.10-11-03531.1990.Search in Google Scholar
Ekstrom, A.D., Kahana, M.J., Caplan, J.B., Fields, T.A., Isham, E.A., Newman, E.L., and Fried, I. (2003). Cellular networks underlying human spatial navigation. Nature 425: 184–188, https://doi.org/10.1038/nature01964.Search in Google Scholar
Epstein, R., Patai, E., Julian, J., and Spiers, H.J. (2017). The cognitive map in humans: spatial navigation and beyond. Nat. Neurosci. 20: 1504–1513, https://doi.org/10.1038/nn.4656.Search in Google Scholar
Ferrara, M., Iaria, G., Tempesta, D., Curcio, G., Moroni, F., Marzano, C., De Gennaro, L., and Pacitti, C. (2008). Sleep to find your way: the role of sleep in the consolidation of memory for navigation in humans. Hippocampus 18: 844–851, https://doi.org/10.1002/hipo.20444.Search in Google Scholar
Folley, B.S., Astur, R., Jagannathan, K., Calhoun, V.D., and Pearlson, G.D. (2010). Anomalous neural circuit function in schizophrenia during a virtual Morris water task. NeuroImage 49: 3373–3384, https://doi.org/10.1016/j.neuroimage.2009.11.034.Search in Google Scholar
Fornasari, L., Chittaro, L., Ieronutti, L., Cottini, L., Dassi, S., Cremaschi, S., Molteni, M., Fabbro, F., and Brambilla, P. (2013). Navigation and exploration of an urban virtual environment by children with autism spectrum disorder compared to children with typical development. Res. Autism Spectr. Disord. 7: 956–965, https://doi.org/10.1016/j.rasd.2013.04.007.Search in Google Scholar
Frick, K.M., Baxter, M.G., Markowska, A.L., Olton, D.S., and Price, D.L. (1995). Age-related spatial reference and working memory deficits assessed in the water maze. Neurobiol. Aging 16: 149–160, https://doi.org/10.1016/0197-4580(94)00155-3.Search in Google Scholar
Goodrich-Hunsaker, N.J., Livingstone, S.A., Skelton, R.W., and Hopkins, R.O. (2010). Spatial deficits in a virtual water maze in amnesic participants with hippocampal damage. Hippocampus 20: 481–491, https://doi.org/10.1002/hipo.20651.Search in Google Scholar
Hamilton, D.A., Driscoll, I., and Sutherland, R.J. (2002). Human place learning in a virtual Morris water task: some important constraints on the flexibility of place navigation. Behav. Brain Res. 129: 159–170, https://doi.org/10.1016/s0166-4328(01)00343-6.Search in Google Scholar
Hamilton, D.A., Johnson, T.E., Redhead, E.S., and Verney, S.P. (2009). Control of rodent and human spatial navigation by room and apparatus cues. Behav. Process. 81: 154–169, https://doi.org/10.1016/j.beproc.2008.12.003.Search in Google Scholar
Hamilton, D.A., Kodituwakku, P., Sutherland, R.J., and Savage, D.D. (2003). Children with Fetal Alcohol Syndrome are impaired at place learning but not cued-navigation in a virtual Morris water task. Behav. Brain Res. 143: 85–94, https://doi.org/10.1016/s0166-4328(03)00028-7.Search in Google Scholar
Hamilton, D.A. and Sutherland, R.J. (1999). Blocking in human place learning: evidence from virtual navigation. Psychobiology 27: 453–461.10.3758/BF03332140Search in Google Scholar
Herting, M.M., and Nagel, B.J. (2012). Aerobic fitness relates to learning on a virtual Morris Water Task and hippocampal volume in adolescents. Behav. Brain Res. 233: 517–525, https://doi.org/10.1016/j.bbr.2012.05.012.Search in Google Scholar PubMed PubMed Central
Hüfner, K., Barresi, D., Glaser, M., Linn, J., Adrion, C., Mansmann, U., Brandt, T., and Strupp, M. (2008). Vestibular paroxysmia: diagnostic features and medical treatment. Neurology 71: 1006–1014, https://doi.org/10.1212/01.wnl.0000326594.91291.f8.Search in Google Scholar PubMed
Iaria, G., and Barton, J.J. (2010). Developmental topographical disorientation: a newly discovered cognitive disorder. Exp. Brain Res. 206: 189–196, https://doi.org/10.1007/s00221-010-2256-9.Search in Google Scholar PubMed
Jacobs, J., Weidemann, C.T., Miller, J.F., Solway, A., Burke, J.F., Wei, X.-X., Suthana, N., Sperling, M.R., Sharan, A.D., and Fried, I., et al. (2013). Direct recordings of grid-like neuronal activity in human spatial navigation. Nat. Neurosci. 16: 1188–1190, https://doi.org/10.1038/nn.3466.Search in Google Scholar PubMed PubMed Central
Jones, C.M., Braithwaite, V.A., and Healy, S.D. (2003). The evolution of sex differences in spatial ability. Behav. Neurosci. 117: 403–411, https://doi.org/10.1037/0735-7044.117.3.403.Search in Google Scholar PubMed
Kallai, J., Makany, T., Karadi, K., and Jacobs, W.J. (2005). Spatial orientation strategies in Morris-type virtual water task for humans. Behav. Brain Res. 159: 187–196, https://doi.org/10.1016/j.bbr.2004.10.015.Search in Google Scholar PubMed
Kalová, E., Vlček, K., Jarolímová, E., and Bureš, J. (2005). Allothetic orientation and sequential ordering of places is impaired in early stages of Alzheimer’s disease: corresponding results in real space tests and computer tests. Behav. Brain Res. 159: 175–186, https://doi.org/10.1016/j.bbr.2004.10.016.Search in Google Scholar PubMed
Kimura, K., Reichert, J.F., Olson, A., Pouya, O.R., Wang, X., Moussavi, Z., and Kelly, D.M. (2017). Orientation in virtual reality does not fully measure up to the real-world. Sci. Rep. 7: 18109, https://doi.org/10.1038/s41598-017-18289-8.Search in Google Scholar PubMed PubMed Central
Kober, S.E., and Neuper, C. (2011). Sex differences in human EEG theta oscillations during spatial navigation in virtual reality. Int. J. Psychophysiol. 79: 347–355, https://doi.org/10.1016/j.ijpsycho.2010.12.002.Search in Google Scholar PubMed
Korthauer, L.E., Nowak, N.T., Moffat, S.D., An, Y., Rowland, L.M., Barker, P.B., Resnick, S.M., and Driscoll, I. (2016). Correlates of virtual navigation performance in older adults. Neurobiol. Aging 39: 118–127, https://doi.org/10.1016/j.neurobiolaging.2015.12.003.Search in Google Scholar PubMed PubMed Central
Kunz, L., Wang, L., Lachner-Piza, D., Zhang, H., Brandt, A., Dümpelmann, M., Reinacher, P.C., Coenen, V.A., Chen, D., and Wang, W.-X., et al. (2019). Hippocampal theta phases organize the reactivation of large-scale electrophysiological representations during goal-directed navigation. Sci. Adv. 5: eaav8192, https://doi.org/10.1126/sciadv.aav8192.Search in Google Scholar PubMed PubMed Central
Laczó, J., Andel, R., Vyhnalek, M., Vlcek, K., Magerova, H., Varjassyova, A., Tolar, M., and Hort, J. (2010). Human analogue of the Morris water maze for testing subjects at risk of Alzheimer’s disease. Neurodegener. Dis. 7: 148–152, https://doi.org/10.1159/000289226.Search in Google Scholar PubMed
Ladouce, S., Donaldson, D.I., Dudchenko, P.A., and Ietswaart, M. (2016). Understanding minds in real-world environments: toward a mobile cognition approach. Front. Hum. Neurosci. 10: 694, https://doi.org/10.3389/fnhum.2016.00694.Search in Google Scholar PubMed PubMed Central
Lee, J.Y., Kho, S., Yoo, H.B., Park, S., Choi, J.S., and Kwon, J.S., et al. (2014). Spatial memory impairments in amnestic mild cognitive impairment in a virtual radial arm maze. Neuropsychiatr. Dis. Treat. 10: 653, https://doi.org/10.2147/ndt.s58185.Search in Google Scholar
Lee, S.A., Miller, J.F., Watrous, A.J., Sperling, M.R., Sharan, A., Worrell, G.A., and Lega, B. (2018). Electrophysiological signatures of spatial boundaries in the human subiculum. J. Neurosci. 38: 3265–3272, https://doi.org/10.1523/jneurosci.3216-17.2018.Search in Google Scholar
León, I., Tascón, L., and Cimadevilla, J.M. (2016). Age and gender-related differences in a spatial memory task in humans. Behav. Brain Res. 306: 8–12, https://doi.org/10.1016/j.bbr.2016.03.008.Search in Google Scholar PubMed
Levy, L.J., Astur, R.S., and Frick, K.M. (2005). Men and women differ in object memory but not performance of a virtual radial maze. Behav. Neurosci. 119: 853–862, https://doi.org/10.1037/0735-7044.119.4.853.Search in Google Scholar PubMed
Livingstone, S.A., and Skelton, R.W. (2007). Virtual environment navigation tasks and the assessment of cognitive deficits in individuals with brain injury. Behav. Brain Res. 185: 21–31, https://doi.org/10.1016/j.bbr.2007.07.015.Search in Google Scholar
Livingstone-Lee, S.A., Murchison, S., Zeman, P.M., Gandhi, M., van Gerven, D., Stewart, L., Livingston, N.J., and Skelton, R.W. (2011). Simple gaze analysis and special design of a virtual Morris water maze provides a new method for differentiating egocentric and allocentric navigational strategy choice. Behav. Brain Res. 225: 117–125, https://doi.org/10.1016/j.bbr.2011.07.005.Search in Google Scholar
Lloyd, J., Persaud, N.V., and Powell, T.E. (2009). Equivalence of real-world and virtual-reality route learning: a pilot study. Cyberpsychol. Behav. 12: 423–427, https://doi.org/10.1089/cpb.2008.0326.Search in Google Scholar
Machado, M.L., Lefèvre, N., Philoxene, B., Le Gall, A., Madeleine, S., Fleury, P., Smith, P.F., and Besnard, S. (2019). New software dedicated to virtual mazes for human cognitive investigations. J. Neurosci. Methods 327: 108388, https://doi.org/10.1016/j.jneumeth.2019.108388.Search in Google Scholar
Maguire, E.A., Frackowiak, R.S., and Frith, C.D. (1997). Recalling routes around London: activation of the right hippocampus in taxi drivers. J. Neurosci. 17: 7103–7110, https://doi.org/10.1523/jneurosci.17-18-07103.1997.Search in Google Scholar
Maguire, E.A., Nannery, R., and Spiers, H.J. (2006). Navigation around London by a taxi driver with bilateral hippocampal lesions. Brain 129: 2894–2907, https://doi.org/10.1093/brain/awl286.Search in Google Scholar
Maguire, E.A., Woollett, K., and Spiers, H.J. (2006). London taxi drivers and bus drivers: a structural MRI and neuropsychological analysis. Hippocampus 16: 1091–1101, https://doi.org/10.1002/hipo.20233.Search in Google Scholar
McDonald, R.J., and White, N.M. (1994). Parallel information processing in the water maze: evidence for independent memory systems involving dorsal striatum and hippocampus. Behav. Neural. Biol. 61: 260–270, https://doi.org/10.1016/s0163-1047(05)80009-3.Search in Google Scholar
Meade, M.E., Meade, J.G., Sauzeon, H., and Fernandes, M.A. (2019). Active navigation in virtual environments benefits spatial memory in older adults. Brain Sci. 9: 47, https://doi.org/10.3390/brainsci9030047.Search in Google Scholar PubMed PubMed Central
Moffat, S.D. (2009). Aging and spatial navigation: what do we know and where do we go? Neuropsychol. Rev. 19: 478, https://doi.org/10.1007/s11065-009-9120-3.Search in Google Scholar PubMed
Moffat, S.D., and Resnick, S.M. (2002). Effects of age on virtual environment place navigation and allocentric cognitive mapping. Behav. Neurosci. 116: 851–859, https://doi.org/10.1037/0735-7044.116.5.851.Search in Google Scholar
Monacelli, A.M., Cushman, L.A., Kavcic, V., and Duffy, C.J. (2003). Spatial disorientation in Alzheimer’s disease: the remembrance of things passed. Neurology 61: 1491–1497, https://doi.org/10.1212/wnl.61.11.1491.Search in Google Scholar
Morris, R. (1984). Developments of a water-maze procedure for studying spatial learning in the rat. J. Neurosci. Methods 11: 47–60, https://doi.org/10.1016/0165-0270(84)90007-4.Search in Google Scholar
Morris, R.G., Garrud, P., Rawlins, J.N., and O’Keefe, J. (1982). Place navigation impaired in rats with hippocampal lesions. Nature 297: 681–683, https://doi.org/10.1038/297681a0.Search in Google Scholar
Morris, R.G.M. (1981). Spatial localization does not require the presence of local cues. Learn. Motiv. 12: 239–260, https://doi.org/10.1016/0023-9690(81)90020-5.Search in Google Scholar
Morris, R.G.M., Schenk, F., Tweedie, F., and Jarrard, L.E. (1990). Ibotenate lesions of hippocampus and/or subiculum: dissociating components of allocentric spatial learning. Eur. J. Neurosci. 2: 1016–1028, https://doi.org/10.1111/j.1460-9568.1990.tb00014.x.Search in Google Scholar PubMed
Mueller, S.C., Jackson, C.P.T., and Skelton, R.W. (2008). Sex differences in a virtual water maze: an eye tracking and pupillometry study. Behav. Brain Res. 193: 209–215, https://doi.org/10.1016/j.bbr.2008.05.017.Search in Google Scholar PubMed
Muffatto, V., Meneghetti, C., and De Beni, R. (2016). Not all is lost in older adults’ route learning: the role of visuo-spatial abilities and type of task. J. Environ. Psychol. 47: 230–241, https://doi.org/10.1016/j.jenvp.2016.07.003.Search in Google Scholar
Newhouse, P., Newhouse, C., and Astur, R.S. (2007). Sex differences in visual-spatial learning using a virtual water maze in pre-pubertal children. Behav. Brain Res. 183: 1–7, https://doi.org/10.1016/j.bbr.2007.05.011.Search in Google Scholar PubMed
Newman, E.L., Caplan, J.B., Kirschen, M.P., Korolev, I.O., Sekuler, R., and Kahana, M.J. (2007). Learning your way around town: how virtual taxicab drivers learn to use both layout and landmark information. Cognition 104: 231–253, https://doi.org/10.1016/j.cognition.2006.05.013.Search in Google Scholar PubMed
Nunez, J. (2008). Morris water maze experiment. JoVE 19: 897, https://doi.org/10.3791/897.Search in Google Scholar
O’Keefe, J., Nadel, L., Keighley, S., and Kill, D. (1975). Fornix lesions selectively abolish place learning in the rat. Exp. Neurol. 48: 152–166.10.1016/0014-4886(75)90230-7Search in Google Scholar
Olton, D.S., and Samuelson, R.J. (1976). Remembrance of places passed: spatial memory in rats. J. Exp. Psychol. Anim. Behav. Process. 2: 97, https://doi.org/10.1037/0097-7403.2.2.97.Search in Google Scholar
Olton, D.S. (1979). Mazes, maps, and memory. Am. Psychol. 34: 583–596, https://doi.org/10.1037/0003-066x.34.7.583.Search in Google Scholar
Overman, W.H., Pate, B.J., Moore, K., and Peuster, A. (1996). Ontogeny of place learning in children as measured in the radial arm maze, Morris search task and open field task. Behav. Neurosci. 110: 1205–1228, https://doi.org/10.1037/0735-7044.110.6.1205.Search in Google Scholar
Packard, M.G., and McGaugh, J.L. (1996). Inactivation of hippocampus or caudate nucleus with lidocaine differentially affects expression of place and response learning. Neurobiol. Learn. Mem. 65: 65–72, https://doi.org/10.1006/nlme.1996.0007.Search in Google Scholar PubMed
Park, J.L., Dudchenko, P.A., and Donaldson, D.I. (2018). Navigation in real-world environments: new opportunities afforded by advances in mobile brain imaging. Front. Hum. Neurosci. 12: 361, https://doi.org/10.3389/fnhum.2018.00361.Search in Google Scholar PubMed PubMed Central
Piper, B.J., Acevedo, S.F., Craytor, M.J., Murray, P.W., and Raber, J. (2010). The use and validation of the spatial navigation Memory Island test in primary school children. Behav. Brain Res. 210: 257–262, https://doi.org/10.1016/j.bbr.2010.02.040.Search in Google Scholar PubMed PubMed Central
Possin, K.L., Sanchez, P.E., Anderson-Bergman, C., Fernandez, R., Kerchner, G.A., Johnson, E.T., Davis, A., Lo, I., Bott, N.T., and Kiely, T., et al. (2016). Cross-species translation of the Morris maze for Alzheimer’s disease. J. Clin. Invest. 126: 779–783, https://doi.org/10.1172/jci78464.Search in Google Scholar
Redhead, E.S., and Hamilton, D.A. (2009). Evidence of blocking with geometric cues in a virtual watermaze. Learn. Motiv. 40: 15–34, https://doi.org/10.1016/j.lmot.2008.06.002.Search in Google Scholar
Redhead, E.S., Hamilton, D.A., Parker, M.O., Chan, W., and Allison, C. (2013). Overshadowing of geometric cues by a beacon in a spatial navigation task. Learn. Behav. 41: 179–191, https://doi.org/10.3758/s13420-012-0096-0.Search in Google Scholar PubMed
Reisel, W.D., and Banai, M. (2002). Comparison of a multidimensional and a global measure of job insecurity: predicting job attitudes and work behaviors. Psychol. Rep. 90: 913–922, https://doi.org/10.2466/pr0.2002.90.3.913.Search in Google Scholar PubMed
Ribeiro, N., Sagnier, C., Quaglino, V., Gounden, Y., and Loup-Escande, E. (2020). Effect of a short rest period on associative and relational memory performance: a virtual reality study. Int. J. Virtual Real. 20: 21–32, https://doi.org/10.20870/ijvr.2020.20.1.3186.Search in Google Scholar
Richardson, A.E., Montello, D.R., and Hegarty, M. (1999). Spatial knowledge acquisition from maps and from navigation in real and virtual environments. Mem. Cognit. 27: 741–750, https://doi.org/10.3758/bf03211566.Search in Google Scholar PubMed
Rodgers, M.K., Sindone, J.A., and Moffat, S.D. (2012). Effects of age on navigation strategy. Neurobiol. Aging 33: 202.e15-e22, https://doi.org/10.1016/j.neurobiolaging.2010.07.021.Search in Google Scholar PubMed PubMed Central
Rodriguez-Andres, D., Mendez-Lopez, M., Juan, M., and Perez-Hernandez, E. (2018). A virtual object-location task for children: gender and videogame experience influence navigation; age impacts memory and completion time. Front. Psychol. 9: 451, https://doi.org/10.3389/fpsyg.2018.00451.Search in Google Scholar PubMed PubMed Central
Rogers, N., San Martín, C., Ponce, D., Henriquez, M., Valdes, J.L., and Behrens, M.I. (2017). Virtual spatial navigation correlates with the Moca score in amnestic mild cognitive impairment patients. J. Neurol. Sci. 381: 116–117, https://doi.org/10.1016/j.jns.2017.08.365.Search in Google Scholar
Rose, F.D., Brooks, B.M., and Rizzo, A.A. (2005). Virtual reality in brain damage rehabilitation: review. Cyberpsychol. Behav. 8: 241–262, https://doi.org/10.1089/cpb.2005.8.241.Search in Google Scholar PubMed
Ruddle, R.A., Payne, S.J., and Jones, D.M. (1997). Navigating buildings in “desk-top” virtual environments: experimental investigations using extended navigational experience. J. Exp. Psychol. Appl. 3: 143, https://doi.org/10.1037/1076-898x.3.2.143.Search in Google Scholar
Salgado-Pineda, P., Landin-Romero, R., Portillo, F., Bosque, C., Pomes, A., Spanlang, B., Franquelo, J.C., Teixido, C., Sarró, S., and Salvador, R., et al. (2016). Examining hippocampal function in schizophrenia using a virtual reality spatial navigation task. Schizophr. Res. 172: 86–93, https://doi.org/10.1016/j.schres.2016.02.033.Search in Google Scholar PubMed
Schmidt-Hieber, C., and Häusser, M. (2013). Cellular mechanisms of spatial navigation in the medial entorhinal cortex. Nat. Neurosci. 16: 325–331, https://doi.org/10.1038/nn.3340.Search in Google Scholar
Schoenfeld, R., Moenich, N., Mueller, F.-J., Lehmann, W., and Leplow, B. (2010). Search strategies in a human water maze analogue analyzed with automatic classification methods. Behav. Brain Res. 208: 169–177, https://doi.org/10.1016/j.bbr.2009.11.022.Search in Google Scholar
Schoenfeld, R., Schiffelholz, T., Beyer, C., Leplow, B., and Foreman, N. (2017). Variants of the Morris water maze task to comparatively assess human and rodent place navigation. Neurobiol. Learn. Mem. 139: 117–127, https://doi.org/10.1016/j.nlm.2016.12.022.Search in Google Scholar
Sharma, G., Kaushal, Y., Chandra, S., Singh, V., Mittal, A.P., and Dutt, V. (2017). Influence of landmarks on way finding and brain connectivity in immersive virtual reality environment. Front. Psychol. 8: 1220, https://doi.org/10.3389/fpsyg.2017.01514.Search in Google Scholar
Shipman, S.L., and Astur, R.S. (2008). Factors affecting the hippocampal BOLD response during spatial memory. Behav. Brain Res. 187: 433–441, https://doi.org/10.1016/j.bbr.2007.10.014.Search in Google Scholar
Skelton, R.W., Bukach, C.M., Laurance, H.E., Thomas, K.G., and Jacobs, J.W. (2000). Humans with traumatic brain injuries show place-learning deficits in computer-generated virtual space. J. Clin. Exp. Neuropsychol. 22: 157–175, https://doi.org/10.1076/1380-3395(200004)22:2;1-1;ft157.10.1076/1380-3395(200004)22:2;1-1;FT157Search in Google Scholar
Skelton, R.W., Ross, S.P., Nerad, L., and Livingstone, S.A. (2006). Human spatial navigation deficits after traumatic brain injury shown in the arena maze, a virtual Morris water maze. Brain Inj. 20: 189–203, https://doi.org/10.1080/02699050500456410.Search in Google Scholar
Slobounov, S.M., Ray, W., Johnson, B., Slobounov, E., and Newell, K.M. (2015). Modulation of cortical activity in 2D versus 3D virtual reality environments: an EEG study. Int. J. Psychophysiol. 95: 254–260, https://doi.org/10.1016/j.ijpsycho.2014.11.003.Search in Google Scholar
Small, W.S. (1901). Experimental study of the mental processes of the rat. II. Am. J. Psychol. 12: 206–239, https://doi.org/10.2307/1412534.Search in Google Scholar
Sousa Santos, B., Dias, P., Pimentel, A., Baggerman, J.-W., Ferreira, C., Silva, S., and Madeira, J. (2008). Head-mounted display versus desktop for 3D navigation in virtual reality: a user study. Multimed. Tool. Appl. 41: 161, https://doi.org/10.1007/s11042-008-0223-2.Search in Google Scholar
Spiers, H.J., and Maguire, E.A. (2006). Spontaneous mentalizing during an interactive real world task: an fMRI study. Neuropsychologia 44: 1674–1682, https://doi.org/10.1016/j.neuropsychologia.2006.03.028.Search in Google Scholar
Spiers, H.J., and Maguire, E.A. (2008). The dynamic nature of cognition during wayfinding. J. Environ. Psychol. 28: 232–249, https://doi.org/10.1016/j.jenvp.2008.02.006.Search in Google Scholar
Sutherland, R.J. and Rudy, J.W. (1988). Place learning in the Morris place navigation task is impaired by damage to the hippocampal formation even if the temporal demands are reduced. Psychobiology 16: 157–163.10.3758/BF03333120Search in Google Scholar
Thorndyke, P.W., and Hayes-Roth, B. (1982). Differences in spatial knowledge acquired from maps and navigation. Cognit. Psychol. 14: 560–589, https://doi.org/10.1016/0010-0285(82)90019-6.Search in Google Scholar
Tolman, E.C. (1949). There is more than one kind of learning. Psychol. Rev. 56: 144, https://doi.org/10.1037/h0055304.Search in Google Scholar PubMed
Tu, S., Spiers, H.J., Hodges, J.R., Piguet, O., and Hornberger, M. (2017). Egocentric versus allocentric spatial memory in behavioural variant frontotemporal dementia and Alzheimer’s disease. J. Alzheim. Dis. 59: 883–892, https://doi.org/10.3233/jad-160592.Search in Google Scholar
van der Ham, I.J.M., and Claessen, M.H.G. (2020). How age relates to spatial navigation performance: functional and methodological considerations. Ageing Res. Rev. 58: 101020, https://doi.org/10.1016/j.arr.2020.101020.Search in Google Scholar PubMed
van der Ham, I.J.M., Faber, A.M.E., Venselaar, M., van Kreveld, M.J., and Löffler, M. (2015). Ecological validity of virtual environments to assess human navigation ability. Front. Psychol. 6: 637, https://doi.org/10.3389/fpsyg.2015.00637.Search in Google Scholar PubMed PubMed Central
van der Ham, I.J.M., van Zandvoort, M.J.E., Meilinger, T., Bosch, S.E., Kant, N., and Postma, A. (2010). Spatial and temporal aspects of navigation in two neurological patients. Neuroreport 21: 685–689, https://doi.org/10.1097/wnr.0b013e32833aea78.Search in Google Scholar PubMed
Veling, W., Moritz, S., and van der Gaag, M. (2014). Brave new worlds—review and update on virtual reality assessment and treatment in psychosis. Schizophr. Bull. 40: 1194–1197, https://doi.org/10.1093/schbul/sbu125.Search in Google Scholar PubMed PubMed Central
Vinson, N.G. (1999). Design guidelines for landmarks to support navigation in virtual environments. In: Proceedings of the SIGCHI conference on human factors in computing systems, pp. 278–285.10.1145/302979.303062Search in Google Scholar
Vorhees, C.V., and Williams, M.T. (2006). Morris water maze: procedures for assessing spatial and related forms of learning and memory. Nat. Protoc. 1: 848–858, https://doi.org/10.1038/nprot.2006.116.Search in Google Scholar
Vorhees, C.V., and Williams, M.T. (2014). Assessing spatial learning and memory in rodents. ILAR J. 55: 310–332, https://doi.org/10.1093/ilar/ilu013.Search in Google Scholar
Watanabe, S., and Bischof, H.J. (2004). Effects of hippocampal lesions on acquisition and retention of spatial learning in zebra finches. Behav. Brain Res. 155: 147–152, https://doi.org/10.1016/j.bbr.2004.04.007.Search in Google Scholar
Weniger, G., and Irle, E. (2008). Allocentric memory impaired and egocentric memory intact as assessed by virtual reality in recent-onset schizophrenia. Schizophr. Res. 101: 201–209, https://doi.org/10.1016/j.schres.2008.01.011.Search in Google Scholar
Weniger, G., Ruhleder, M., Lange, C., Wolf, S., and Irle, E. (2011). Egocentric and allocentric memory as assessed by virtual reality in individuals with amnestic mild cognitive impairment. Neuropsychologia 49: 518–527, https://doi.org/10.1016/j.neuropsychologia.2010.12.031.Search in Google Scholar
Whishaw, I.Q. (1985). Formation of a place learning-set by the rat: a new paradigm for neurobehavioral studies. Physiol. Behav. 35: 139–143, https://doi.org/10.1016/0031-9384(85)90186-6.Search in Google Scholar
Wiener, J.M., Carroll, D., Moeller, S., Bibi, I., Ivanova, D., Allen, P., and Wolbers, T. (2020). A novel virtual-reality-based route-learning test suite: assessing the effects of cognitive aging on navigation. Behav. Res. Methods 52: 630–640, https://doi.org/10.3758/s13428-019-01264-8.Search in Google Scholar PubMed PubMed Central
Williams, M.T., Morford, L.L., Wood, S.L., Wallace, T.L., Fukumura, M., Broening, H.W., and Vorhees, C.V. (2003). Developmental D-methamphetamine treatment selectively induces spatial navigation impairments in reference memory in the Morris water maze while sparing working memory. Synapse 48: 138–148, https://doi.org/10.1002/syn.10159.Search in Google Scholar PubMed
Woollett, K., Spiers, H.J., and Maguire, E.A. (2009). Talent in the taxi: a model system for exploring expertise. Philos. Trans. R. Soc. Lond. B Biol. Sci. 364: 1407–1416, https://doi.org/10.1098/rstb.2008.0288.Search in Google Scholar PubMed PubMed Central
Woolley, D.G., Laeremans, A., Gantois, I., Mantini, D., Vermaercke, B., Op de Beeck, H.P., Swinnen, S.P., Wenderoth, N., Arckens, L., and D’Hooge, R. (2013). Homologous involvement of striatum and prefrontal cortex in rodent and human water maze learning. Proc. Natl. Acad. Sci. USA 110: 3131–3136, https://doi.org/10.1073/pnas.1217832110.Search in Google Scholar
Woolley, D.G., Vermaercke, B., Op de Beeck, H., Wagemans, J., Gantois, I., D’Hooge, R., Swinnen, S.P., and Wenderoth, N. (2010). Sex differences in human virtual water maze performance: novel measures reveal the relative contribution of directional responding and spatial knowledge. Behav. Brain Res. 208: 408–414, https://doi.org/10.1016/j.bbr.2009.12.019.Search in Google Scholar
Worsley, C.L., Recce, M., Spiers, H.J., Marley, J., Polkey, C.E., and Morris, R.G. (2001). Path integration following temporal lobectomy in humans. Neuropsychologia 39: 452–464, https://doi.org/10.1016/s0028-3932(00)00140-8.Search in Google Scholar
Yip, C.K., and Man, D.W.K. (2009). Validation of a computerized cognitive assessment system for persons with stroke: a pilot study. Int. J. Rehabil. Res. 32: 270–278, https://doi.org/10.1097/mrr.0b013e32832c0dbb.Search in Google Scholar PubMed
Zhong, J.Y., Magnusson, K.R., Swarts, M.E., Clendinen, C.A., Reynolds, N.C., and 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. Behav. Neurosci. 131: 470–482, https://doi.org/10.1037/bne0000219.Search in Google Scholar PubMed PubMed Central
© 2021 Walter de Gruyter GmbH, Berlin/Boston
