Crowded environments reduce spatial memory in older but not younger adults

  • Niamh A. Merriman
  • Jan Ondřej
  • Alicia Rybicki
  • Eugenie Roudaia
  • Carol O’Sullivan
  • Fiona N. Newell
Original Article

Abstract

Previous studies have reported an age-related decline in spatial abilities. However, little is known about whether the presence of other, task-irrelevant stimuli during learning further affects spatial cognition in older adults. Here we embedded virtual environments with moving crowds of virtual human pedestrians (Experiment 1) or objects (Experiment 2) whilst participants learned a route and landmarks embedded along that route. In subsequent test trials we presented clips from the learned route and measured spatial memory using three different tasks: a route direction task (i.e. whether the video clip shown was a repetition or retracing of the learned route); an intersection direction task; and a task involving identity of the next landmark encountered. In both experiments, spatial memory was tested in two separate sessions: first following learning of an empty maze environment and second using a different maze which was populated. Older adults performed worse than younger adults in all tasks. Moreover, the presence of crowds during learning resulted in a cost in performance to the spatial tasks relative to the ‘no crowds’ condition in older adults but not in younger adults. In contrast, crowd distractors did not affect performance on the landmark sequence task. There was no age-related cost on performance with object distractors. These results suggest that crowds of human pedestrians selectively capture older adults’ attention during learning. These findings offer further insights into how spatial memory is affected by the ageing process, particularly in scenarios which are representative of real-world situations.

References

  1. Antonova, E., Parslow, D., Brammer, M., Dawson, G. R., Jackson, S. H., & Morris, R. G. (2009). Age-related neural activity during allocentric spatial memory. Memory, 17(2), 125–143. doi:10.1080/09658210802077348.PubMedCrossRefGoogle Scholar
  2. Arena, A., Hutchinson, C. V., & Shimozaki, S. S. (2012). The effects of age on the spatial and temporal integration of global motion. Vision Research, 58C, 27–32. doi:10.1016/j.visres.2012.02.004.CrossRefGoogle Scholar
  3. Arnold, A. E., Burles, F., Krivoruchko, T., Liu, I., Rey, C. D., Levy, R. M., & Iaria, G. (2013). Cognitive mapping in humans and its relationship to other orientation skills. Experimental Brain Research, 224(3), 359–372. doi:10.1007/s00221-012-3316-0.PubMedCrossRefGoogle Scholar
  4. Baddeley, A. D. (1986). Working memory. Oxford: Oxford University Press. doi:10.1002/acp.2350020209.Google Scholar
  5. Benedict, R. H. B., & Zgaljardic, D. J. (1998). Practice effects during repeated administrations of memory tests with and without alternate forms. Journal of Clinical and Experimental Neuropsychology, 20(3), 339–352. doi:10.1076/jcen.20.3.339.822.PubMedCrossRefGoogle Scholar
  6. Bennett, P. J., Sekuler, R., & Sekuler, A. B. (2007). The effects of aging on motion detection and direction identification. Vision Research, 47(6), 799–809. doi:10.1016/j.visres.2007.01.001.PubMedCrossRefGoogle Scholar
  7. Berard, J., Fung, J., & Lamontagne, A. (2012). Impact of aging on visual reweighting during locomotion. Clinical Neurophysiology, 123(7), 1422–1428. doi:10.1016/j.clinph.2011.11.081.PubMedCrossRefGoogle Scholar
  8. Berard, J. R., Fung, J., McFadyen, B. J., & Lamontagne, A. (2009). Aging affects the ability to use optic flow in the control of heading during locomotion. Experimental Brain Research, 194(2), 183–190. doi:10.1007/s00221-008-1685-1.PubMedCrossRefGoogle Scholar
  9. Billino, J., Bremmer, F., & Gegenfurtner, K. R. (2008). Differential aging of motion processing mechanisms: evidence against general perceptual decline. Vision Research, 48(10), 1254–1261. doi:10.1016/j.visres.2008.02.014.PubMedCrossRefGoogle Scholar
  10. Burns, P. C. (1999). Navigation and the mobility of older drivers. The Journals of Gerontology. Series B: Psychological Sciences and Social Sciences, 54(1), S49–S55. doi:10.1093/geronb/54B.1.S49.CrossRefGoogle Scholar
  11. Byrne, P., Becker, S., & Burgess, N. (2007). Remembering the past and imagining the future: a neural model of spatial memory and imagery. Psychological Review, 114(2), 340–375. doi:10.1037/0033-295X.114.2.340.PubMedPubMedCentralCrossRefGoogle Scholar
  12. Castelli, L., Latini Corazzini, L., & Geminiani, G. C. (2008). Spatial navigation in large-scale virtual environments: gender differences in survey tasks. Computers in Human Behavior, 24(4), 1643–1667. doi:10.1016/j.chb.2007.06.005.CrossRefGoogle Scholar
  13. Chao, L. L., & Knight, R. T. (1997). Prefrontal deficits in attention and inhibitory control with aging. Cerebral Cortex, 7(1), 63–69. doi:10.1093/cercor/7.1.63.PubMedCrossRefGoogle Scholar
  14. Clapp, W. C., Rubens, M. T., & Gazzaley, A. (2010). Mechanisms of working memory disruption by external interference. Cerebral Cortex, 20(4), 859–872. doi:10.1093/cercor/bhp150.PubMedCrossRefGoogle Scholar
  15. Clapp, W. C., Rubens, M. T., Sabharwal, J., & Gazzaley, A. (2011). Deficit in switching between functional brain networks underlies the impact of multitasking on working memory in older adults. Proceedings of the National Academy of Sciences of the United States of America, 108(17), 7212–7217. doi:10.1073/pnas.1015297108.PubMedPubMedCentralCrossRefGoogle Scholar
  16. Davidson, D. J., Zacks, R. T., & Williams, C. C. (2003). Stroop interference, practice, and aging. Aging, Neuropsychology and Cognition, 10(2), 85–98. doi:10.1076/anec.10.2.85.14463.PubMedPubMedCentralCrossRefGoogle Scholar
  17. Davis, S. W., Dennis, N. A., Daselaar, S. M., Fleck, M. S., & Cabeza, R. (2008). Que PASA? The posterior-anterior shift in aging. Cerebral Cortex, 18(5), 1201–1209. doi:10.1093/cercor/bhm155.PubMedCrossRefGoogle Scholar
  18. Downing, P. E., Bray, D., Rogers, J., & Childs, C. (2004). Bodies capture attention when nothing is expected. Cognition, 93(1), 27–38. doi:10.1016/j.cognition.2003.10.010.CrossRefGoogle Scholar
  19. Driscoll, I., Hamilton, D. A., Petropoulos, H., Yeo, R. A., Brooks, W. M., Baumgartner, R. N., & Sutherland, R. J. (2003). The aging hippocampus: cognitive, biochemical and structural findings. Cerebral Cortex, 13(12), 1344–1351. doi:10.1093/cercor/bhg081.PubMedCrossRefGoogle Scholar
  20. Dulaney, C. L., & Rogers, W. A. (1994). Mechanisms underlying reduction in Stroop interference with practice for young and old adults. Journal of Experimental Psychology. Learning, Memory, and Cognition, 20(2), 470–484. doi:10.1037/0278-7393.20.2.470.PubMedCrossRefGoogle Scholar
  21. Dumas, J. A., & Hartman, M. (2003). Adult age differences in temporal and item memory. Psychology and Aging, 18(3), 573–586. doi:10.1037/0882-7974.18.3.573.PubMedCrossRefGoogle Scholar
  22. Duncan, J., & Humphreys, G. W. (1989). Visual search and stimulus similarity. Psychological Review, 96(3), 433–458. doi:10.1037/0033-295X.96.3.433.PubMedCrossRefGoogle Scholar
  23. Eichenbaum, H., & Cohen, N. J. (2014). Can we reconcile the declarative memory and spatial navigation views on hippocampal function? Neuron, 83(4), 764–770. doi:10.1016/j.neuron.2014.07.032.PubMedPubMedCentralCrossRefGoogle Scholar
  24. Fabiani, M., & Friedman, D. (1997). Dissociations between memory for temporal order and recognition memory in aging. Neuropsychologia, 35(2), 129–141. doi:10.1016/S0028-3932(96)00073-5.PubMedCrossRefGoogle Scholar
  25. Foster, D. J., & Wilson, M. A. (2006). Reverse replay of behavioural sequences in hippocampal place cells during the awake state. Nature, 440, 680–683. doi:10.1038/nature04587.PubMedCrossRefGoogle Scholar
  26. Gazzaley, A., Cooney, J. W., Rissman, J., & D’Esposito, M. (2005). Top-down suppression deficit underlies working memory impairment in normal aging. Nature Neuroscience, 8(10), 1298–1300. doi:10.1038/nn1543.PubMedCrossRefGoogle Scholar
  27. Gazzaley, A., Sheridan, M. A., Cooney, J. W., & D’Esposito, M. (2007). Age-related deficits in component processes of working memory. Neuropsychology, 21(5), 532–539. doi:10.1037/0894-4105.21.5.532.PubMedCrossRefGoogle Scholar
  28. Harris, M. A., Wiener, J. M., & Wolbers, T. (2012). Aging specifically impairs switching to an allocentric navigational strategy. Frontiers in Aging Neuroscience, 4(29), 1–9. doi:10.3389/fnagi.2012.00029.Google Scholar
  29. Hartley, T., Maguire, E. A., Spiers, H. J., & Burgess, N. (2003). The well-worn route and the path less traveled: distinct neural bases of route following and wayfinding in humans. Neuron, 37(5), 877–888. doi:10.1016/S0896-6273(03)00095-3.PubMedCrossRefGoogle Scholar
  30. Hasher, L., & Zacks, R. (1988). Working memory, comprehension and aging: A review and a new view. In G. K. Bower (Ed.), The psychology of learning and motivation (pp. 192–225). New York, NY: Academic Press. doi:10.1016/S0079-7421(08)60041-9.
  31. Head, D., & Isom, M. (2010). Age effects on wayfinding and route learning skills. Behavioural Brain Research, 209(1), 49–58. doi:10.1016/j.bbr.2010.01.012.PubMedCrossRefGoogle Scholar
  32. Hegarty, M., Richardson, A. E., Montello, D. R., Lovelace, K., & Subbiah, I. (2002). Development of a self-report measure of environmental spatial ability. Intelligence, 30, 425–447. doi:10.1016/S0160-2896(02)00116-2.CrossRefGoogle Scholar
  33. Hommel, B., Li, K. Z. H., & Li, S.-C. (2004). Visual search across the life span. Developmental Psychology, 40(4), 545–558. doi:10.1037/0012-1649.40.4.545.PubMedCrossRefGoogle Scholar
  34. Iaria, G., Palermo, L., Committeri, G., & Barton, J. J. S. (2009). Age differences in the formation and use of cognitive maps. Behavioural Brain Research, 196(2), 187–191. doi:10.1016/j.bbr.2008.08.040.PubMedCrossRefGoogle Scholar
  35. Isingrini, M., Perrotin, A., Souchay, C., Sossin, W. S., Lacaille, J.-C., Castellucci, V. F., & Belleville, S. (2008). Aging, metamemory regulation and executive functioning. Progress in Brain Research, 169, 377–392. doi:10.1016/S0079-6123(07)00024-6.PubMedCrossRefGoogle Scholar
  36. Jensen, O., & Lisman, J. E. (2005). Hippocampal sequence-encoding driven by a cortical multi-item working memory buffer. Trends in Neurosciences, 28(2), 67–72. doi:10.1016/j.tins.2004.12.001.PubMedCrossRefGoogle Scholar
  37. Konishi, K., Etchamendy, N., Roy, S., Marighetto, A., Rajah, N., & Bohbot, V. D. (2013). 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, 23(11), 1005–1014. doi:10.1002/hipo.22181.PubMedCrossRefGoogle Scholar
  38. Kramer, A. F., Hahn, S., & Gopher, D. (1999). Task coordination and aging: Explorations of executive control processes in the task switching paradigm. Acta Psychologica, 101(2–3), 339–378. doi:10.1016/S0001-6918(99)00011-6.PubMedCrossRefGoogle Scholar
  39. Lambrey, S., Doeller, C., Berthoz, A., & Burgess, N. (2012). Imagining being somewhere else: Neural basis of changing perspective in space. Cerebral Cortex, 22(1), 166–174. doi:10.1093/cercor/bhr101.PubMedCrossRefGoogle Scholar
  40. Lavie, N. (1995). Perceptual load as a necessary condition for selective attention. Journal of Experimental Psychology: Human Perception and Performance, 21(3), 451–468. doi:10.1037/0096-1523.21.3.451 PubMedGoogle Scholar
  41. Lavie, N. (2010). Attention, distraction, and cognitive control under load. Current Directions in Psychological Science, 19(3), 143–148. doi:10.1177/0963721410370295.CrossRefGoogle Scholar
  42. Lavie, N., & De Fockert, J. (2005). The role of working memory in attentional capture. Psychonomic Bulletin & Review, 12(4), 669–674. doi:10.3758/BF03196756.CrossRefGoogle Scholar
  43. Lavie, N., Hirst, A., de Fockert, J. W., & Viding, E. (2004). Load theory of selective attention and cognitive control. Journal of Experimental Psychology: General, 133(3), 339–354. doi:10.1037/0096-3445.133.3.339.CrossRefGoogle Scholar
  44. Loomis, J. M., Klatzky, R. L., Golledge, R. G., Cicinelli, J. G., Pellegrino, J. W., & Fry, P. A. (1993). Nonvisual navigation by blind and sighted: Assessment of path integration ability. Journal of Experimental Psychology: General, 122(1), 73–91. doi:10.1037/0096-3445.122.1.73.CrossRefGoogle Scholar
  45. Lustig, C., Hasher, L., & Tonev, S. T. (2006). Distraction as a determinant of processing speed. Psychonomic Bulletin & Review, 13(4), 619–625. doi:10.3758/BF03193972.CrossRefGoogle Scholar
  46. Madden, D. J., Whiting, W. L., & Huettel, S. A. (2010). Age-related changes in neural activity during visual perception and attention. In R. Cabeza, L. Nyberg, & D. Park (Eds.), Cognitive neuroscience of aging: Linking cognitive and cerebral aging (pp. 157–185). New York: Oxford University Press.Google Scholar
  47. Maguire, E. A., Burgess, N., Donnett, J. G., Frackowiak, R. S. J., Frith, C. D., & O’Keefe, J. (1998). Knowing where and getting there: A human navigation network. Science, 280(5365), 921–924. doi:10.1126/science.280.5365.921.PubMedCrossRefGoogle Scholar
  48. Maylor, E. A., & Lavie, N. (1998). The influence of perceptual load on age differences in selective attention. Psychology and Aging, 13(4), 563–574. doi:10.1037/0882-7974.13.4.563.PubMedCrossRefGoogle Scholar
  49. McCarley, J. S., Yamani, Y., Kramer, A. F., & Mounts, J. R. W. (2012). Age, clutter, and competitive selection. Psychology and Aging, 27(3), 616–626. doi:10.1037/a0026705.PubMedCrossRefGoogle Scholar
  50. McPhee, L. C., Scialfa, C. T., Dennis, W. M., Ho, G., & Caird, J. K. (2004). Age differences in visual search for traffic signs during a simulated conversation. Human Factors, 46(4), 674–685. doi:10.1518/hfes.46.4.674.56817.PubMedCrossRefGoogle Scholar
  51. Merriman, N. A. (2015). Assessing cognitive factors and individual differences that modulate spatial navigation ability in older adults [dissertation]. Trinity College, the University of Dublin.Google Scholar
  52. Moffat, S. D. (2009). Aging and spatial navigation: What do we know and where do we go? Neuropsychology Review, 19(4), 478–489. doi:10.1007/s11065-009-9120-3.PubMedCrossRefGoogle Scholar
  53. Moffat, S. D., Elkins, W., & Resnick, S. M. (2006). Age differences in the neural systems supporting human allocentric spatial navigation. Neurobiology of Aging, 27(7), 965–972. doi:10.1016/j.neurobiolaging.2005.05.011.PubMedCrossRefGoogle Scholar
  54. Moffat, S. D., Zonderman, A. B., & Resnick, S. M. (2001). Age differences in spatial memory in a virtual environment navigation task. Neurobiology of Aging, 22(5), 787–796. doi:10.1016/S0197-4580(01)00251-2.PubMedCrossRefGoogle Scholar
  55. Nasreddine, Z. S., Phillips, N. A., Bédirian, V., Charbonneau, S., Whitehead, V., Collin, I., & Chertkow, H. (2005). The Montreal Cognitive Assessment, MoCA: a brief screening tool for mild cognitive impairment. Journal of the American Geriatrics Society, 53(4), 695–699. doi:10.1111/j.1532-5415.2005.53221.x.PubMedCrossRefGoogle Scholar
  56. Norman, J. F., Crabtree, C. E., Clayton, A. M., & Norman, H. F. (2005). The perception of distances and spatial relationships in natural outdoor environments. Perception, 34(11), 1315–1324. doi:10.1068/p5304.PubMedCrossRefGoogle Scholar
  57. O’Keefe, J., & Nadel, L. (1978). The hippocampus as a cognitive map. Oxford: Oxford University Press.Google Scholar
  58. Park, D. C., & Reuter-Lorenz, P. (2009). The adaptive brain: Aging and neurocognitive scaffolding. Annual Review of Psychology, 60, 173–196. doi:10.1146/annurev.psych.59.103006.093656.PubMedPubMedCentralCrossRefGoogle Scholar
  59. Pilz, K. S., Bennett, P. J., & Sekuler, A. B. (2010). Effects of aging on biological motion discrimination. Vision Research, 50(2), 211–219. doi:10.1016/j.visres.2009.11.014.PubMedCrossRefGoogle Scholar
  60. Postle, B. R., Desposito, M., & Corkin, S. (2005). Effects of verbal and nonverbal interference on spatial and object visual working memory. Memory & Cognition, 33(2), 203–212. doi:10.3758/BF03195309.CrossRefGoogle Scholar
  61. Pratt, J., Radulescu, P. V., Guo, R. M., & Abrams, R. A. (2010). It’s alive! animate motion captures visual attention. Psychological Science, 21(11), 1724–1730. doi:10.1177/0956797610387440.PubMedCrossRefGoogle Scholar
  62. 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(November), 1676–1689. doi:10.1093/cercor/bhi044.PubMedCrossRefGoogle Scholar
  63. Repovš, G., & Baddeley, A. (2006). The multi-component model of working memory: Explorations in experimental cognitive psychology. Neuroscience, 139(1), 5–21. doi:10.1016/j.neuroscience.2005.12.061.PubMedCrossRefGoogle Scholar
  64. Reuter-Lorenz, P. A., & Sylvester, C. Y. C. (2010). The cognitive neuroscience of working memory and aging. In R. Cabeza, L. Nyberg, & D. Park (Eds.), Cognitive neuroscience of aging: Linking cognitive and cerebral aging (pp. 186–217). New York, NY: Oxford University Press.Google Scholar
  65. Rich, E. L., & Shapiro, M. (2009). Rat prefrontal cortical neurons selectively code strategy switches. The Journal of Neuroscience, 29(22), 7208–7219. doi:10.1523/jneurosci.6068-08.2009.PubMedPubMedCentralCrossRefGoogle Scholar
  66. Rodgers, M. K., Sindone, J. A., III, & Moffat, S. D. (2012). Effects of age on navigation strategy. Neurobiology of Aging, 33(1), 202e15–e22. doi:10.1016/j.neurobiolaging.2010.07.021.CrossRefGoogle Scholar
  67. Rosenbaum, R. S., Winocur, G., Binns, M. A., & Moscovitch, M. (2012). Remote spatial memory in aging: All is not lost. Frontiers in Aging Neuroscience, 4(25), 1–10. doi:10.3389/fnagi.2012.00025.Google Scholar
  68. Roudaia, E., Bennett, P. J., Sekuler, A. B., & Pilz, K. S. (2009). Spatiotemporal properties of apparent-motion perception in aging. Journal of Vision, 9(8), 695. doi:10.1167/10.14.5.Introduction.CrossRefGoogle Scholar
  69. Salthouse, T. A., Babcock, R. L., & Shaw, R. J. (1991). Effects of adult age on structural and operational capacities in working memory. Psychology and Aging, 6(1), 118–127. doi:10.1037/0882-7974.6.1.118.PubMedCrossRefGoogle Scholar
  70. Schaefer, S., Schellenbach, M., Lindenberger, U., & Woollacott, M. (2015). Walking in high-risk settings: Do older adults still prioritize gait when distracted by a cognitive task? Experimental Brain Research, 233(1), 79–88. doi:10.1007/s00221-014-4093-8.PubMedCrossRefGoogle Scholar
  71. Sholl, M. J., Kenny, R. J., & DellaPorta, K. A. (2006). Allocentric-heading recall and its relation to self-reported sense-of-direction. Journal of Experimental Psychology. Learning, Memory, and Cognition, 32(3), 516–533. doi:10.1037/0278-7393.32.3.516.PubMedCrossRefGoogle Scholar
  72. Siegel, J. W., & White, S. H. (1975). The development of spatial representations of large-scale environments. Advances in Child Development and Behavior, 10, 9–55. doi:10.1016/S0065-2407(08)60007-5.PubMedCrossRefGoogle Scholar
  73. Spiers, H. J. (2008). Keeping the goal in mind: Prefrontal contributions to spatial navigation. Neuropsychologia, 46(7), 2106–2108. doi:10.1016/j.neuropsychologia.2008.01.028.PubMedPubMedCentralCrossRefGoogle Scholar
  74. Spiers, H. J., & Barry, C. (2015). Neural systems supporting navigation. Current Opinion in Behavioral Sciences, 1, 47–55. doi:10.1016/j.cobeha.2014.08.005.CrossRefGoogle Scholar
  75. Taillade, M., Sauzéon, H., Arvind Pala, P., Déjos, M., Larrue, F., Gross, C., & N’Kaoua, B. (2013a). Age-related wayfinding differences in real large-scale environments: Detrimental motor control effects during spatial learning are mediated by executive decline? PLoS ONE, 8(7), e67193. doi:10.1371/journal.pone.0067193.PubMedPubMedCentralCrossRefGoogle Scholar
  76. Taillade, M., Sauzéon, H., Déjos, M., Arvind Pala, P., Larrue, F., Wallet, G., & N’Kaoua, B. (2013b). Executive and memory correlates of age-related differences in wayfinding performances using a virtual reality application. Aging, Neuropsychology and Cognition, 20(3), 298–319. doi:10.1080/13825585.2012.706247.PubMedCrossRefGoogle Scholar
  77. Tolman, E. C. (1948). Cognitive maps in rats and men. Psychological Review, 55(4), 189–208. doi:10.1037/h0061626.PubMedCrossRefGoogle Scholar
  78. Trick, L. M., Toxopeus, R., & Wilson, D. (2010). The effects of visibility conditions, traffic density, and navigational challenge on speed compensation and driving performance in older adults. Accident Analysis and Prevention, 42(6), 1661–1671. doi:10.1016/j.aap.2010.04.005.PubMedCrossRefGoogle Scholar
  79. Vakil, E., Weise, M., & Shmuel, E. (1997). Direct and indirect memory measures of temporal order: Younger versus older adults. The International Journal of Aging & Human Development, 45(3), 195–206. doi:10.2190/N54R-9Q1M-27F3-GTRY.CrossRefGoogle Scholar
  80. van Asselen, M., Fritschy, E., & Postma, A. (2006). The influence of intentional and incidental learning on acquiring spatial knowledge during navigation. Psychological Research, 70(2), 151–156. doi:10.1007/s00426-004-0199-0.PubMedCrossRefGoogle Scholar
  81. Vogeley, K., & Fink, G. R. (2003). Neural correlates of the first-person-perspective. Trends in Cognitive Sciences, 7(1), 38–42. doi:10.1016/S1364-6613(02)00003-7.PubMedCrossRefGoogle Scholar
  82. Warren, W. H., Blackwell, A. W., & Morris, M. W. (1989). Age differences in perceiving the direction of self-motion from optical flow. Journal of Gerontology: Psychological Sciences, 44(5), P147–P153.CrossRefGoogle Scholar
  83. Wegman, J., Fonteijn, H. M., van Ekert, J., Tyborowska, A., Jansen, C., & Janzen, G. (2014). Gray and white matter correlates of navigational ability in humans. Human Brain Mapping, 35, 2561–2572. doi:10.1002/hbm.22349.PubMedCrossRefGoogle Scholar
  84. Wiener, J. M., Kmecova, H., & de Condappa, O. (2012a). Route repetition and route retracing: Effects of cognitive aging. Frontiers in Aging Neuroscience, 4(7), 1–7. doi:10.3389/fnagi.2012.00007.Google Scholar
  85. Wiener, J. M., Hölscher, C., Büchner, S., & Konieczny, L. (2012b). Gaze behaviour during space perception and spatial decision making. Psychological Research, 76(6), 713–729. doi:10.1007/s00426-011-0397-5.PubMedCrossRefGoogle Scholar
  86. Wiener, J. M., de Condappa, O., Harris, M. A., & Wolbers, T. (2013). Maladaptive bias for extrahippocampal navigation strategies in aging humans. The Journal of Neuroscience, 33(14), 6012–6017. doi:10.1523/jneurosci.0717-12.2013.PubMedCrossRefGoogle Scholar
  87. Wolbers, T., & Büchel, C. (2005). Dissociable retrosplenial and hippocampal contributions to successful formation of survey representations. The Journal of Neuroscience, 25(13), 3333–3340. doi:10.1523/jneurosci.4705-04.2005.PubMedCrossRefGoogle Scholar
  88. Wolbers, T., & Hegarty, M. (2010). What determines our navigational abilities? Trends in Cognitive Sciences, 14(3), 138–146. doi:10.1016/j.tics.2010.01.001.PubMedCrossRefGoogle Scholar
  89. Wolbers, T., Weiller, C., & Büchel, C. (2004). Neural foundations of emerging route knowledge in complex spatial environments. Cognitive Brain Research, 21(3), 401–411. doi:10.1016/j.cogbrainres.2004.06.013.PubMedCrossRefGoogle Scholar
  90. Yantis, S., & Hillstrom, A. P. (1994). Stimulus-driven attentional capture: Evidence from equiluminant visual objects. Journal of Experimental Psychology: Human Perception and Performance, 20(1), 95–107. doi:10.1037/0096-1523.20.1.95.PubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Niamh A. Merriman
    • 1
  • Jan Ondřej
    • 2
  • Alicia Rybicki
    • 1
  • Eugenie Roudaia
    • 1
  • Carol O’Sullivan
    • 2
  • Fiona N. Newell
    • 1
  1. 1.School of Psychology and Institute of Neuroscience, Lloyd BuildingTrinity College DublinDublin 2Ireland
  2. 2.Graphics, Vision and Visualisation Group, School of Computer Science and StatisticsTrinity College DublinDublin 2Ireland

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