A mechanistic approach to individual differences in spatial learning, memory, and navigation

Psychology of Learning and Motivation - Advances in Research and Theory

Volumn 59, Issue , 2013, Pages 223-259

  Shelton, Amy L ^a   Marchette, Steven A ^a   Furman, Andrew J ^a  

^a JOHNS HOPKINS UNIVERSITY   (United States)

Author keywords

Aging; Landmark route survey framework; Morris water maze; Navigation; Radial arm maze; Spatial learning

Indexed keywords

EID: 84877954860     PISSN: 00797421     EISSN: None     Source Type: Book Series    
DOI: 10.1016/B978-0-12-407187-2.00006-X     Document Type: Chapter

References (90)

1. Allen G.L., Kirasic K.C., Dobson S.H., Long R.G., Beck S. Predicting environmental learning from spatial abilities: an indirect route. Intelligence 1996, 22(3):327-355.
2. Astur R.S., Taylor L.B., Mamelak A.N., Philpott L., Sutherland R.J. Humans with hippocampus damage display severe spatial memory impairments in a virtual Morris water task. Behavioural Brain Research 2002, 132(1):77-84.
3. Barnes C.A., Nadel L., Honig W.K. Spatial memory deficit in senescent rats. Canadian Journal of Psychology 1980, 34(1):29.
4. Bellassen V., Iglói K., de Souza L.C., Dubois B., Rondi-Reig L. Temporal order memory assessed during spatiotemporal navigation as a behavioral cognitive marker for differential Alzheimer's disease diagnosis. Journal of Neuroscience 2012, 32(6):1942-1952.
5. Bell S., Saucier D. Relationship among environmental pointing accuracy, mental rotation, sex, and hormones. Environment and Behavior 2004, 36(2):251-265.
6. Bird C.M., Burgess N. The hippocampus and memory: insights from spatial processing. Nature Reviews Neuroscience 2008, 9(3):182-194.
7. Bohbot V.D., Iaria G., Petrides M. Hippocampal function and spatial memory: evidence from functional neuroimaging in healthy participants and performance of patients with medial temporal lobe resections. Neuropsychology 2004, 18(3):418.
8. Bohbot V.D., Kalina M., Stepankova K., Spackova N., Petrides M., Nadel L.Y.N.N. Spatial memory deficits in patients with lesions to the right hippocampus and to the right parahippocampal cortex. Neuropsychologia 1998, 36(11):1217-1238.
9. Brown T.I., Ross R.S., Tobyne S.M., Stern C.E. Cooperative interactions between hippocampal and striatal systems support flexible navigation. NeuroImage 2012, 60(2):1316.
10. Carlson L.A., Hölscher C., Shipley T.F., Dalton R.C. Getting lost in buildings. Current Directions in Psychological Science 2010, 19(5):284-289.
11. Chan E., Baumann O., Bellgrove M.A., Mattingley J.B. From objects to landmarks: the function of visual location information in spatial navigation. Frontiers in Psychology 2012, 3:304.
12. Chang Q., Gold P.E. Inactivation of dorsolateral striatum impairs acquisition of response learning in cue-deficient, but not cue-available, conditions. Behavioral Neuroscience 2004, 118(2):383.
13. Chrastil E.R. Neural evidence supports a novel framework for spatial navigation. Psychonomic Bulletin & Review 2012.
14. Clark, S., Marchette, S. A., Furman, A. J., & Shelton, A. L. Talking while walking: investigating the effects of verbal distraction on human navigation performance and strategy selection, in preparation.
15. Clark A.S., Mitre M.C., Brinck-Johnsen T. Anabolic-androgenic steroid and adrenal steroid effects on hippocampal plasticity. Brain Research 1995, 679(1):64-71.
16. Cornwell B.R., Johnson L.L., Holroyd T., Carver F.W., Grillon C. Human hippocampal and parahippocampal theta during goal-directed spatial navigation predicts performance on a virtual Morris water maze. Journal of Neuroscience 2008, 28(23):5983-5990.
17. Davis D.M., Jacobson T.K., Aliakbari S., Mizumori S.J.Y. Differential effects of estrogen on hippocampal-and striatal-dependent learning. Neurobiology of Learning and Memory 2005, 84(2):132-137.
18. De Leon M.J., George A.E., Golomb J., Tarshish C., Convit A., Kluger A., et al. Frequency of hippocampal formation atrophy in normal aging and Alzheimer's disease. Neurobiology of Aging 1997, 18(1):1-11.
19. Devan B.D., White N.M. Parallel information processing in the dorsal striatum: relation to hippocampal function. Journal of Neuroscience 1999, 19(7):2789-2798.
20. Driscoll I., Hamilton D.A., Petropoulos H., Yeo R.A., Brooks W.M., Baumgartner R.N., et al. The aging hippocampus: cognitive, biochemical and structural findings. Cerebral Cortex 2003, 13(12):1344-1351.
21. Driscoll I., Hamilton D.A., Yeo R.A., Brooks W.M., Sutherland R.J. Virtual navigation in humans: the impact of age, sex, and hormones on place learning. Hormones and Behavior 2005, 47(3):326-335.
22. Elliott A.E., Packard M.G. Intra-amygdala anxiogenic drug infusion prior to retrieval biases rats towards the use of habit memory. Neurobiology of Learning and Memory 2008, 90(4):616-623.
23. Featherstone R.E., McDonald R.J. Dorsal striatum and stimulus-response learning: lesions of the dorsolateral, but not dorsomedial, striatum impair acquisition of a simple discrimination task. Behavioural Brain Research 2004, 150(1):15-23.
24. Featherstone R.E., McDonald R.J. Lesions of the dorsolateral or dorsomedial striatum impair performance of a previously acquired simple discrimination task. Neurobiology of Learning and Memory 2005, 84(3):159-167.
25. Fields A.W., Shelton A.L. Individual skill differences and large-scale environmental learning. Journal of Experimental Psychology: Learning, Memory, and Cognition 2006, 32(3):506.
26. Furman A.J., Marchette S.A., Shelton A.L. Individual differences in navigational style and its relationship to volitional strategy shifting 2013, Manuscript submitted for publication.
27. Gallagher M., Burwell R., Burchinal M.R. Severity of spatial learning impairment in aging: development of a learning index for performance in the Morris water maze. Behavioral Neuroscience 1993, 107(4):618.
28. Gallagher M., Pelleymounter M.A. Spatial learning deficits in old rats: a model for memory decline in the aged. Neurobiology of Aging 1988, 9:549-556.
29. Gold P.E., Korol D.L. Hormones and memory. Encyclopedia of behavioral neuroscience 2010, Vol. 2:57-64. Academic Press, Oxford. G. Koob, M. Le Moal, R.F. Thompson (Eds.).
30. Hamilton D.A., Driscoll I., Sutherland R.J. Human place learning in a virtual Morris water task: some important constraints on the flexibility of place navigation. Behavioural Brain Research 2002, 129(1):159-170.
31. Hartley T., Maguire E.A., Spiers H.J., Burgess N. The well-worn route and the path less traveled: distinct neural bases of route following and wayfinding in humans. Neuron 2003, 37(5):877-888.
32. Hegarty M., Richardson A.E., Montello D.R., Lovelace K., Subbiah I. Development of a self-report measure of environmental spatial ability. Intelligence 2002, 30(5):425-447.
33. Hund A.M., Minarik J.L. Getting from here to there: spatial anxiety, wayfinding strategies, direction type, and wayfinding efficiency. Spatial Cognition and Computation 2006, 6(3):179-201.
34. Iaria G., Palermo L., Committeri G., Barton J.J. Age differences in the formation and use of cognitive maps. Behavioural Brain Research 2009, 196(2):187-191.
35. Iaria G., Petrides M., Dagher A., Pike B., Bohbot V.D. Cognitive strategies dependent on the hippocampus and caudate nucleus in human navigation: variability and change with practice. Journal of Neuroscience 2003, 23(13):5945-5952.
36. Ishikawa T., Montello D.R. Spatial knowledge acquisition from direct experience in the environment: individual differences in the development of metric knowledge and the integration of separately learned places. Cognitive Psychology 2006, 52(2):93-129.
37. Jack C.R., Petersen R.C., Xu Y., O'Brien P.C., Smith G.E., Ivnik R.J., et al. Rate of medial temporal lobe atrophy in typical aging and Alzheimer's disease. Neurology 1998, 51(4):993-999.
38. Kelly J.W., McNamara T.P., Bodenheimer B., Carr T.H., Rieser J.J. Individual differences in using geometric and featural cues to maintain spatial orientation: cue quantity and cue ambiguity are more important than cue type. Psychonomic Bulletin & Review 2009, 16(1):176-181.
39. Kim J.J., Lee H.J., Han J.S., Packard M.G. Amygdala is critical for stress-induced modulation of hippocampal long-term potentiation and learning. Journal of Neuroscience 2001, 21(14):5222-5228.
40. Kim J.J., Yoon K.S. Stress: metaplastic effects in the hippocampus. Trends in Neurosciences 1998, 21(12):505-509.
41. Kirasic K.C. Age differences in adults' spatial abilities, learning environmental layout, and wayfinding behavior. Spatial Cognition and Computation 2000, 2(2):117-134.
42. Kirasic K.C., Mathes E.A. Effects of different means for conveying environmental information on elderly adults' spatial cognition and behavior. Environment and Behavior 1990, 22(5):591-607.
43. Korol D.L. Role of estrogen in balancing contributions from multiple memory systems. Neurobiology of Learning and Memory 2004, 82(3):309-323.
44. Lawton C.A. Gender differences in way-finding strategies: relationship to spatial ability and spatial anxiety. Sex Roles 1994, 30(11):765-779.
45. Lawton C.A. Strategies for indoor wayfinding: the role of orientation. Journal of Environmental Psychology 1996, 16(2):137-145.
46. Lawton C.A., Charleston S.I., Zieles A.S. Individual-and gender-related differences in indoor wayfinding. Environment and Behavior 1996, 28(2):204-219.
47. Maguire E.A., Burgess N., Donnett J.G., Frackowiak R.S., Frith C.D., O'Keefe J. Knowing where and getting there: a human navigation network. Science 1998, 280(5365):921-924.
48. Mahmood O., Adamo D., Briceno E., Moffat S.D. Age differences in visual path integration. Behavioural Brain Research 2009, 205(1):88-95.
49. Marchette S.A., Bakker A., Shelton A.L. Cognitive mappers to creatures of habit: differential engagement of place and response learning mechanisms predicts human navigational behavior. Journal of Neuroscience 2011, 31(43):15264-15268.
50. Marchette S.A., Yerramsetti A., Burns T.J., Shelton A.L. Spatial memory in the real world: long-term representations of everyday environments. Memory & Cognition 2011, 39(8):1401-1408.
51. Meulenbroek O., Petersson K.M., Voermans N., Weber B., Fernández G. Age differences in neural correlates of route encoding and route recognition. NeuroImage 2004, 22(4):1503-1514.
52. Moffat S.D. Aging and spatial navigation: what do we know and where do we go?. Neuropsychology Review 2009, 19(4):478-489.
53. Moffat S.D., Elkins W., Resnick S.M. Age differences in the neural systems supporting human allocentric spatial navigation. Neurobiology of Aging 2006, 27(7):965-972.
54. Moffat S.D., Kennedy K.M., Rodrigue K.M., Raz N. Extrahippocampal contributions to age differences in human spatial navigation. Cerebral Cortex 2007, 17(6):1274-1282.
55. Moffat S.D., Resnick S.M. Effects of age on virtual environment place navigation and allocentric cognitive mapping. Behavioral Neuroscience 2002, 116(5):851.
56. Morris R.G. Spatial localization does not require the presence of local cues. Learning and Motivation 1981, 12(2):239-260.
57. Morris R. Developments of a water-maze procedure for studying spatial learning in the rat. Journal of Neuroscience Methods 1984, 11(1):47-60.
58. Morris R.G.M., Garrud P., Rawlins J.N.P., O'Keefe J. Place navigation impaired in rats with hippocampal lesions. Nature 1982, 297(5868):681-683.
59. Naghdi N., Majlessi N., Bozorgmehr T. The effect of intrahippocampal injection of testosterone enanthate (an androgen receptor agonist) and anisomycin (protein synthesis inhibitor) on spatial learning and memory in adult, male rats. Behavioural Brain Research 2005, 156(2):263-268.
60. Newman M.C., Kaszniak A.W. Spatial memory and aging: performance on a human analog of the Morris water maze. Aging, Neuropsychology, and Cognition 2000, 7(2):86-93.
61. Olton D.S., Collison C., Werz M.A. Spatial memory and radial arm maze performance of rats. Learning and Motivation 1977, 8(3):289-314.
62. Packard M.G. Anxiety, cognition, and habit: a multiple memory systems perspective. Brain Research 2009, 1293:121-128.
63. Packard M.G., McGaugh J.L. Inactivation of hippocampus or caudate nucleus with lidocaine differentially affects expression of place and response learning. Neurobiology of Learning and Memory 1996, 65(1):65-72.
64. Packard M.G., Wingard J.C. Amygdala and " emotional" modulation of the relative use of multiple memory systems. Neurobiology of Learning and Memory 2004, 82(3):243-252.
65. Pazzaglia F., De Beni R. Strategies of processing spatial information in survey and landmark-centred individuals. European Journal of Cognitive Psychology 2001, 13(4):493-508.
66. Poldrack R.A., Packard M.G. Competition among multiple memory systems: converging evidence from animal and human brain studies. Neuropsychologia 2003, 41(3):245-251.
67. Rapp P.R., Rosenberg R.A., Gallagher M. An evaluation of spatial information processing in aged rats. Behavioral Neuroscience 1987, 101(1):3.
68. Restle F. Discrimination of cues in mazes: a resolution of the " place-vs.-response" question. Psychological Review 1957, 64(4):217.
69. Ritchie B.F., Aeschliman B., Pierce P. Studies in spatial learning. VIII. Place performance and the acquisition of place dispositions. Journal of Comparative and Physiological Psychology 1950, 43(2):73.
70. Roof R.L., Havens M.D. Testosterone improves maze performance and induces development of a male hippocampus in females. Brain Research 1992, 572(1-2):310-313.
71. Rosenzweig E.S., Barnes C.A. Impact of aging on hippocampal function: plasticity, network dynamics, and cognition. Progress in Neurobiology 2003, 69(3):143-179.
72. Sadowski R.N., Jackson G.R., Wieczorek L., Gold P.E. Effects of stress, corticosterone, and epinephrine administration on learning in place and response tasks. Behavioural Brain Research 2009, 205(1):19-25.
73. Sandstrom N.J., Kaufman J., Huettel S.A. Males and females use different distal cues in a virtual environment navigation task. Cognitive Brain Research 1998, 6(4):351-360.
74. Sandstrom N.J., Kim J.H., Wasserman M.A. Testosterone modulates performance on a spatial working memory task in male rats. Hormones and Behavior 2006, 50(1):18-26.
75. Saucier D.M., Green S.M., Leason J., MacFadden A., Bell S., Elias L.J. Are sex differences in navigation caused by sexually dimorphic strategies or by differences in the ability to use the strategies?. Behavioral Neuroscience 2002, 116(3):403.
76. Schwabe L., Schächinger H., de Kloet E.R., Oitzl M.S. Corticosteroids operate as a switch between memory systems. Journal of Cognitive Neuroscience 2010, 22(7):1362-1372.
77. Shelton A.L., Gabrieli J.D. Neural correlates of encoding space from route and survey perspectives. Journal of Neuroscience 2002, 22(7):2711-2717.
78. Shelton A.L., Gabrieli J.D. Neural correlates of individual differences in spatial learning strategies. Neuropsychology 2004, 18(3):442.
79. Siegel A.W., White S.H. The development of spatial representations of large-scale environments. Advances in Child Development and Behavior 1975, 10:9-55.
80. Skelton R.W., Ross S.P., Nerad L., Livingstone S.A. Human spatial navigation deficits after traumatic brain injury shown in the arena maze, a virtual Morris water maze. Brain Injury 2006, 20(2):189-203.
81. Spiers H.J., Maguire E.A. A navigational guidance system in the human brain. Hippocampus 2007, 17(8):618-626.
82. Stewart C.A., Morris R.G.M. The watermaze. Behavioral neuroscience. A practical approach 1993, Vol. 1:107-122. IRL Press, Oxford. A. Saghal (Ed.).
83. Taylor H.A., Naylor S.J., Chechile N.A. Goal-specific influences on the representation of spatial perspective. Memory & Cognition 1999, 27(2):309-319.
84. Tolman E.C. Cognitive maps in rats and men. Psychological Review 1948, 55(4):189.
85. Tolman E.C., Ritchie B.F., Kalish D. Studies in spatial learning. II. Place learning versus response learning. Journal of Experimental Psychology 1946, 36(3):221.
86. Tolman E.C., Ritchie B.F., Kalish D. Studies in spatial learning. V. Response learning vs. place learning by the non-correction method. Journal of Experimental Psychology 1947, 37(4):285.
87. Waller D., Lippa Y. Landmarks as beacons and associative cues: their role in route learning. Memory & Cognition 2007, 35(5):910-924.
88. Warren S.G., Juraska J.M. Spatial and nonspatial learning across the rat estrous cycle. Behavioral Neuroscience 1997, 111(2):259.
89. Wolbers T., Hegarty M. What determines our navigational abilities?. Trends in Cognitive Sciences 2010, 14(3):138-146.
90. Yerramsetti A., Marchette S.A., Shelton A.L. Accessibility versus accuracy in retrieving spatial memory: evidence for suboptimal assumed headings. Journal of Experimental Psychology: Learning, Memory, and Cognition 2012, Advance online publication. http://dx.doi.org/10.1037/a0030905.