Virtual Morris water maze: opportunities and challenges.

Conor Thornberry, Jose M Cimadevilla, Sean Commins
Author Information
  1. Conor Thornberry: Department of Psychology, Maynooth University, John Hume Building, North Campus, Maynooth, Co Kildare W23 F2H6, Ireland.
  2. Jose M Cimadevilla: Department of Psychology and Health Research Center, University of Almeria, 04120 La Cañada, Almería, Spain.
  3. Sean Commins: Department of Psychology, Maynooth University, John Hume Building, North Campus, Maynooth, Co Kildare W23 F2H6, Ireland.

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.

Keywords

References

  1. 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.
  2. 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.
  3. 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.
  4. 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.
  5. 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.
  6. 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.
  7. 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.
  8. 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.
  9. 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.
  10. 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.
  11. 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.
  12. 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.
  13. 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.
  14. 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.
  15. 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.
  16. 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.
  17. 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.
  18. 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.
  19. 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.
  20. 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.
  21. 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.
  22. 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.
  23. 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.
  24. 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.
  25. 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.
  26. 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.
  27. Commins, S. (2018). Behavioural neuroscience. Cambridge, UK: Cambridge University Press.
  28. 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.
  29. 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.
  30. 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.
  31. 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.
  32. 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.
  33. 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.
  34. 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.
  35. 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.
  36. 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.
  37. 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.
  38. 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.
  39. 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.
  40. 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.
  41. 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.
  42. 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.
  43. 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.
  44. 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.
  45. 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.
  46. 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.
  47. 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.
  48. 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.
  49. 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.
  50. 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.
  51. 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.
  52. 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.
  53. 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.
  54. 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.
  55. 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.
  56. Hamilton, D.A. and Sutherland, R.J. (1999). Blocking in human place learning: evidence from virtual navigation. Psychobiology 27: 453–461.
  57. 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.
  58. 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.
  59. 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.
  60. 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.
  61. 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.
  62. 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.
  63. 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.
  64. 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.
  65. 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.
  66. 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.
  67. 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.
  68. 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.
  69. 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.
  70. 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.
  71. 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.
  72. 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.
  73. 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.
  74. 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.
  75. 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.
  76. 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.
  77. 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.
  78. 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.
  79. 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.
  80. 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.
  81. 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.
  82. 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.
  83. 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.
  84. 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.
  85. 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.
  86. 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.
  87. 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.
  88. 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.
  89. 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.
  90. 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.
  91. 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.
  92. 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.
  93. 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.
  94. Nunez, J. (2008). Morris water maze experiment. JoVE 19: 897, https://doi.org/10.3791/897.
  95. 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.
  96. 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.
  97. Olton, D.S. (1979). Mazes, maps, and memory. Am. Psychol. 34: 583–596, https://doi.org/10.1037/0003-066x.34.7.583.
  98. 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.
  99. 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.
  100. 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.
  101. 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.
  102. 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.
  103. 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.
  104. 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.
  105. 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.
  106. 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.
  107. 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.
  108. 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.
  109. 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.
  110. 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.
  111. 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.
  112. 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.
  113. 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.
  114. 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.
  115. 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.
  116. 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.
  117. 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.
  118. 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.
  119. 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.
  120. 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.
  121. 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.
  122. 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.
  123. 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.
  124. 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.
  125. 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.
  126. 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.
  127. 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.
  128. Tolman, E.C. (1949). There is more than one kind of learning. Psychol. Rev. 56: 144, https://doi.org/10.1037/h0055304.
  129. 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.
  130. 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.
  131. 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.
  132. 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.
  133. 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.
  134. 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.
  135. 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.
  136. 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.
  137. 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.
  138. 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.
  139. 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.
  140. 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.
  141. 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.
  142. 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.
  143. 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.
  144. 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.
  145. 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.
  146. 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.
  147. 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.
  148. 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.

MeSH Term

Animals
Humans
Maze Learning
Mental Recall
Morris Water Maze Test
Spatial Navigation
Virtual Reality

Word Cloud

Created with Highcharts 10.0.0virtualspatialnavigationwatermazetasksVRmanybecomememorybehaviouralexaminedusingdifferenttypesmazesrealityresearchpopularmethodhumanusedacrosstaskMorrisVWMdifficultiesneedabilityaccuratelyrecalllocationsnavigateenvironmentreliesmultiplecognitivemechanismsneuralcorrelatesrepeatedlyanimalsAccurateperformancesprovendependspecificcircuitsbrainstructuresstandardtestdiseasemodelsintroductionneuroscienceexaminingHoweverexaminelaboratoriesappearsgreatlydifferopenarenatownsdrivingsimulators200papersfoundanalogueAlthoughhighlightadvantagesalsomajorrelatedwidespreaduseDespitetask'spopularitydemonstrateinconsistencyuse -particularlyrespectenvironmentalsetupproceduresUsingversionsmakesreplicationfindingscomparisonresultsresearchersdifficultsuggestprotocoldesignstandardisationalongsideaddressed'goldstandard'similaranimalcounterpartVirtualmaze:opportunitieschallenges

Similar Articles

Cited By