Human spatial navigation: Cognitive maps, sexual dimorphism, and neural substrates

Current Opinion in Neurobiology

Volumn 9, Issue 2, 1999, Pages 171-177

  Maguire, Eleanor A ^a   Burgess, Neil ^b   O'Keefe, John ^b  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

COGNITION; ENVIRONMENT; HIPPOCAMPUS; HUMAN; NERVE CELL NETWORK; PRIORITY JOURNAL; REVIEW; SEX DIFFERENCE; SPATIAL ORIENTATION; VIRTUAL REALITY;

EID: 0032960010     PISSN: 09594388     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0959-4388(99)80023-3     Document Type: Article

References (76)

1. Tolman E.C. Cognitive maps in rats and man. Psychol Rev. 55:1948;189-208.
2. O'Keefe J Dostrovsky J. The hippocampus as a spatial map: preliminary evidence from unit activity in the freely-moving rat. Brain Res. 34:1971;171-175.
3. O'Keefe J., Nadel L. The Hippocampus as a Cognitive Map. 1978;Clarendon Press, Oxford.
4. Muller R.U. A quarter of a century of place cells. Neuron. 17:1996;813-822.
5. Taube J.S. Head direction cells and the neuropsychological basis for a sense of direction. Prog Neurobiol. 55:1998;225-256. A thorough review of in vivo electrophysiological studies in rats showing cells coding explicitly for the animal's head direction. The relationship of these findings to human's sense of direction is explored briefly.
6. McNaughton B.L., Barnes C.A., Gerrard J.L., Gothard K., Jung M.W., Knierim J.J., Kudrimoti H., Qin Y., Skaggs W.E., Suster M., Weaver K.L. Deciphering the hippocampal polyglot: the hippocampus as a path integration system. J Exp Biol. 199:1996;173-185.
7. Lipp H.P., Wolfer D.P. Genetically modified mice and cognition. Curr Opin Neurobiol. 8:1998;272-280.
8. Claydon N.S., Dickinson A. Episodic-like memory during cache recovery by scrub jays. Nature. 395:1998;272-274. A demonstration of all the elements of episodic memory in food-storing birds. The existence of something analogous to episodic memory in nonhumans has been notoriously hard to prove. In this study, recall of the time, place and content of an event (e.g. caching of the food) could be inferred from the behaviour of the birds in retrieving two types of stored food, one of which decays faster than the other.
9. Sherry D.F., Duff S.J. Behavioural and neural basis of orientation in food-storing birds. J Exp Biol. 199:1996;165-172.
10. Robertson R.G., Rolls E.T., Georges-Francois P. Spatial view cells in the primate hippocampus: effects of removal of view details. J Neurophysiol. 79:1998;1145-1156. This study describes cells in region CA1 of primate hippocampus that respond whenever the monkey looks at a particular location in the testing room, independent of its visual characteristics (e.g. tested by drawing a curtain across it or switching off the lights).
11. Nishijo H., Ono T., Eifuku S., Tamura R. The relationship between monkey hippocampus place-related neural activity and action in space. Neurosci Lett. 226:1997;57-60. Reports place-related neural activity in the primate hippocampal formation when the monkey controls its own movements around the testing room (on a robot), but not when the experimenter controls the movements.
12. Snyder L.H., Grieve K.L., Brotchie P., Andersen R.A. Separate body- and world-referenced representations of visual space in parietal cortex. Nature. 394:1998;887-891. Recording from neurons in area 7a of monkey posterior parietal cortex, the authors observed 'gain-field' modulation of the animal's response to a visual stimulus encoding the stimulus location in the testing room. This contrasts with gain-field encoding of the location of the stimulus relative to parts of the body (e.g. trunk, head, etc.) in other parietal areas. Interestingly, area 7a is the part of parietal cortex with strong projections to the parahippocampal and presubicular cortices.
13. Moffat S.D., Hampson E., Hatzipanteli Navigation in a 'virtual' maze: sex differences and correlation with psychometric measures of spatial ability in humans. Evol Hum Behav. 9:1998;73-87. Male and female human subjects learned to take a route through a corridor-based, landmark-free virtual reality maze over five trials. A significant advantage was found for male performance in terms of the number of errors committed and time taken, despite correction for the males' extra experience of similar computer games.
14. McCarthy R.A., Evans J.J., Hodges J.R. Topographic amnesia: spatial memory disorder, perceptual dysfunction, or category specific semantic memory impairment? J Neurol Neurosurg Psychiatry. 60:1996;318-325.
15. Habib M., Sirigu A. Pure topographical disorientation: a definition and anatomical basis. Cortex. 23:1987;73-85.
16. Maguire E.A., Cipolotti L. The selective sparing of topographical memory. J Neurol Neurosurg Psychiatry. 65:1998;903-909. The authors report a patient in the advanced stages of Pick's disease who showed severely impaired recall and recognition of verbal and visual material on standard tests including geographical knowledge, but spared landmark and scene recognition and preserved ability to navigate through large-scale spaces. This demonstrates the double dissociation between navigation and table-top spatial tasks.
17. Peruch P., Gaunet F. Virtual environments as a promising tool for investigating human spatial cognition. Curr Psychol Cogn. 17:1998;881-899.
18. Ruddle R.A., Payne S.J., Jones D.M. Navigating buildings in 'desk-top' virtual environments: experimental investigations using extended navigational experience. J Exp Psychol. 3:1997;143-159. Shows that, with practice, people can learn to navigate inside a simulated building as accurately as in the real building. The addition of everyday objects as landmarks improved performance, whereas cubes with abstract coloured patterns on them did not (an interesting parallel to findings reported in [57]).
19. Regian J.W., Yadrick R.M. Assessment of configurational knowledge of naturally- and artificially-acquired large-scale space. J Environ Psychol. 14:1994;211-223.
20. Witmer B.G., Bailey J.H., Knerr B.W. Virtual spaces and real world places: transfer of route knowledge. Int J Human-Computer Studies. 45:1996;413-428.
21. Arthur E.J., Hancock P.A., Chrysler S.T. The perception of spatial layout in real and virtual worlds. Ergonomics. 40:1997;69-77.
22. Waller D., Hunt E., Knapp D. The transfer of spatial knowledge in virtual environment training. Presence. 7:1998;129-143.
23. Held R., Durlach N. Telepresence. Presence. 1:1992;109-112.
24. Witmer BG, Singer MJ: Measuring Presence in Virtual Environments. ARI Technical Report 1014. Alexandria, Virginia: US Army Research Institute for the Behavioral and Social Sciences; 1994.
25. •], shows that human subjects can learn a virtual reality version of the Morris water-maze using only distal visual cues. Consistent with the idea that subjects form a cognitive map of the maze, the authors found that the subjects took short cuts from novel start locations and that their performance was unimpaired by removal of subsets of the distal visual cues but was impaired by rearrangement of the cues or removal of all of them.
26. Morris R.G.M. Spatial localization does not require the presence of local cues. Learn Motiv. 12:1981;239-260.
27. Cressant A., Muller R.U., Poucet B. Failure of centrally-placed objects to control the firing fields of hippocampal place cells. J Neurosci. 17:1997;2531-2542.
28. Morris R.G.M., Garrard P., Rawlins J.N.P., O'Keefe J. Place navigation impaired in rats with hippocampal lesions. Nature. 297:1982;681-683.
29. Pearce J.M., Roberts A.D.L., Good M. Hippocampal lesions disrupt navigation based on cognitive maps but not heading vectors. Nature. 396:1998;75-77. Reports that hippocampal lesions do not impair a rat's performance in returning to the hidden platform in the Morris water maze when its location is defined by a directional bearing from a single intramaze cue, but they do impair performance in the standard set-up in which the location is defined relative to the constellation of distal cues.
30. •].
31. Fenton A.A., Arolfo M.P., Nerad L., Bures J. Place navigation in the Morris water maze under minimum and redundant extra-maze cue conditions. Behav Neural Biol. 62:1994;178-189.
32. O'Keefe J., Conway D.H. Hippocampal place units in the freely moving rat: why they fire where they fire. Exp Brain Res. 31:1978;573-590.
33. Suzuki S., Augerinos G., Black A.H. Stimulus control of spatial behavior on the eight-arm radial maze. Learn Motiv. 11:1980;1-8.
34. Pico R.M., Gerbrandt L.K., Pondel M., Ivy G. During stepwise cue deletion, rat place behaviors correlate with place unit responses. Brain Res. 330:1985;369-372.
35. Gillner S., Mallot H.A. Navigation and acquisition of spatial knowledge in a virtual maze. J Cogn Neurosci. 10:1998;445-463. Shows that humans can form a cognitive-map-like representation of space from the local visual information available during exploration of a virtual reality town. The subjects demonstrated an ability to generate novel routes and short-cuts, estimate the distances between places, and draw a bird's-eye plan of the town.
36. Ruddle R.A., Payne S.J., Jones D.M. Navigating large-scale 'desk-top' virtual buildings: effects of orientation aids and familiarity. Presence. 7:1998;179-192.
37. Tlauka M., Wilson P.N. The effect of landmarks on route-learning in a computer-simulated environment. J Environ Psychol. 14:1994;305-313.
38. Siegal, A.W., White, S.H.: The development of spatial representations of large-scale environments. In Advances in Child Development and Behavior, vol 10. Edited by Reese H. New York: Academic Press; 1975:10-55.
39. Astur R.S., Ortiz M.L., Sutherland R.J. A characterization of performance by men and women in a virtual Morris water task: a large and reliable sex difference. Behav Brain Res. 93:1998;185-190.
40. Sandstrom N.J., Kaufman J., Huettel S.A. Males and females use different distal cues in a virtual environment navigation task. Cogn Brain Res. 6:1998;351-360. Male and female subjects learned a virtual reality version of a Morris water maze that contained distal visual cues within a trapezoidal room. When tested with the same cues within an octagonal room, male and female subjects did not show a significant difference in performance. However, removing the distal cues, or varying their locations randomly, impaired the performance of females significantly more than the males, who were better able to make use of the trapezoidal shape of the room.
41. Galea L.A.M., Kimura D. Sex differences in route-learning. Pers Individ Differ. 14:1992;53-65.
42. Lawton C.A. Gender differences in way-finding strategies: relationship to spatial ability and spatial anxiety. Sex Roles. 30:1994;765-779.
43. Williams C.L., Meck W.H. The organizational effects of gonadal steroids on sexually dimorphic spatial ability. Psychoneuroendocrinology. 16:1991;155-176.
44. Dabbs J.M. Jr., Chang E.-L., Strong R.A., Milun R. Spatial ability, navigation strategy, and geographic knowledge among men and women. Evol Human Behav. 19:1998;89-98.
45. Schmitz S. Gender-related strategies in environmental development: effects of anxiety on wayfinding in and representation of a three-dimensional maze. J Environ Psychol. 17:1997;215-228. Girls and boys aged 10-17 years old explored a maze-like environment arranged in a large building over two floors. Anxiety was assessed prior to the task, and task-specific fear was assessed during the task. Subjects explored the maze five times. Following run four, they had to draw or write representations of the maze. Overall, girls were more anxious and fearful than boys and were slower to move through the maze. Interestingly, no sex differences emerged in the number of maze elements recalled. In general, subjects who were more anxious and fearful traversed the maze more slowly and remembered more landmarks but fewer directions than less anxious subjects.
46. Hermer L., Spelke E.S. A geometric process for spatial reorientation in young children. Nature. 370:1994;57-59.
47. •] for a possible neural basis for this).
48. O'Keefe J., Burgess N. Geometric determinants of the place fields of hippocampal neurons. Nature. 381:1996;425-428.
49. Aguirre G.K., Detre J.A., Alsop D.C., D'Esposito M. The parahippocampus subserves topographical learning in man. Cereb Cortex. 6:1996;823-829.
50. Aguirre G.K., Zaharn E., D'Esposito M. Neural components of topographical representation. Proc Natl Acad Sci USA. 95:1998;839-846.
51. Maguire E.A., Frackowiak R.S.J., Frith C.D. Recalling routes around London: activation of the right hippocampus in taxi drivers. J Neurosci. 17:1997;7103-7110. A PET study in which taxi drivers described either routes between locations in London, famous landmarks, film plots or individual frames from films. The route and landmark conditions were associated with bilateral parahippocampal activation compared to a control condition, with the route condition also showing activation of the right hippocampus compared to the control condition (or any other condition).
52. Owen A.M., Milner B., Petrides M., Evans A.C. A specific role for the right parahippocampal gyrus in the retrieval of object-location: a positron emission tomography study. J Cogn Neurosci. 8:1996;588-602.
53. •] for a description of similar results). Subjects were not required to learn or remember any of the stimuli. The response to indoor scenes depended on the presence of the walls of the room being in the correct configuration (consistent with place-cell recordings in rat hippocampus that indicate the external walls of the environment as the most significant input; see [48]).
54. Aguirre G.K., D'Esposito M. Environmental knowledge is subserved by separable dorsal/ventral neural areas. J Neurosci. 17:1997;2512-2518. A fMRI study in which, having explored a virtual reality town, subjects had to recognise the location of a particular view or indicate the egocentric direction of a target location from the current view. Bilateral parahippocampal activity was observed in both tasks relative to a control condition. The direction task was associated with greater parietal activation, and the recognition task with greater lingual, fusiform and parahippocampal activation.
55. •] for a description of similar results).
56. Suzuki W.A., Miller E., Desimone R. Object and place memory in the macaque entorhinal cortex. J Neurophysiol. 78:1997;1062-1081.
57. Maguire E.A, . Frith C.D., Burgess N., Donnett J.G., O'Keefe J. Knowing where things are: parahippocampal involvement in encoding object locations in virtual large-scale space. J Cogn Neurosci. 10:1998;61-76. A PET study of the exploration of virtual environments. Right parahippocampal activation was observed during exploration of a richly textured environment containing everyday objects, but not during exploration of a plain maze of empty rooms and corridors.
58. Vargha-Khadem F., Gadian D.G., Watkins K.E., Connolly A., Van Paesschen W., Mishkin M. Differential effects of early hippocampal pathology on episodic and semantic memory. Science. 277:1997;376-380. A study of three patients with bilateral hippocampal pathology (but apparent sparing of the surrounding cortical tissue) caused by anoxic events early in life. These patients showed remarkably spared factual knowledge and recognition memory, but strongly impaired episodic memory in everyday life. While not conclusive, this study indicates that the hippocampus is required for episodic memory, but not necessarily required for semantic or recognition memory.
59. Milner B. Disorders of learning and memory after temporal lobe lesions in man. Clin Neurosurg. 19:1972;421-446.
60. Tulving E. Elements of Episodic Memory. 1983;Clarendon Press, Oxford.
61. Maguire E.A., Frackowiak R.S.J., Frith C.D. Learning to find your way - a role for the human hippocampal region. Proc R Soc Lond [Biol]. 263:1996;1745-1750.
62. Ghaem O., Mellet E., Crivello F., Tzourio N., Mazoyer B., Berthoz A., Denis M. Mental navigation along memorized routes activates the hippocampus, precuneus, and insula. Neuroreport. 8:1997;739-744. A PET study in which subjects either imagined walking along a segment of a path they had walked the day before, or imagined the appearance of a landmark seen from the route. Both tasks activated a network of brain regions compared to rest, including right and left hippocampal areas. The mentally simulated walking activated left medial hippocampal regions compared to the landmark visualisation task.
63. Maguire E.A., Burgess N., Donnett J.G., Frackowiak R.S.J., Frith C.D., O'Keefe J. Knowing where, and getting there: a human navigation network. Science. 280:1998;921-924. A PET study of navigation within a complex virtual reality town. Activation of the right hippocampus was observed when subjects navigated between previously visited locations compared to following a path of arrows. Activation of the right hippocampus and inferior right parietal cortex was correlated with the accuracy of navigation. Interpretation of these results related the hippocampal activity to determining the allocentric direction towards the target, and parietal activation to determining the egocentric turns required to get there.
64. Burgess N., O'Keefe J. Neuronal computations underlying the firing of place cells and their role in navigation. Hippocampus. 7:1996;749-762.
65. Maguire E.A., Burke T., Phillips J., Staunton H. Topographical disorientation following unilateral temporal lobe surgery in humans. Neuropsychologia. 34:1996;993-1001.
66. Farrell M.J. Topographical disorientation. Neurocase. 2:1996;509-520.
67. Smith M.L., Milner B. The role of the right hippocampus in the recall of spatial location. Neuropsychologia. 19:1981;781-793.
68. Bohbot V.D., Kalina M., Stepankova K., Spackova N., Petrides M., Nadel N. Spatial memory deficits in patients with lesions to the right hippocampus and to the right parahippocampal cortex. Neuropsychologia. 36:1998;1217-1238. A study of patients with well-localised lesions within different areas of the medial temporal lobes, showing that the right parahippocampal cortex is critically involved in topographical memory, as tested by returning to a hidden goal location after a delay (similar to the water maze). The right hippocampus was found to be critically involved in spatial memory, as tested by recall of the locations of objects in a room, and in reproduction of the Rey-Osterrieth figure after a delay.
69. Lepage M., Habib R., Tulving E. Hippocampal PET activations of memory encoding and retrieval: the HIPER model. Hippocampus. 8:1998;313-322. A meta-analysis of PET studies showing activation of hippocampal and nearby medial temporal lobe areas during episodic memory encoding or retrieval. The authors observed a tendency for encoding to be associated with anterior hippocampal activations and retrieval to be associated with posterior activations.
70. •] might not be attributable to encoding per se.
71. Moser M., Moser E., Forrest E., Andersen P., Morris R.G.M. Spatial learning with the minislab in the dorsal hippocampus. Proc Natl Acad Sci USA. 92:1995;9697-9701.
72. Moser M.B., Moser E.I. Distributed encoding and retrieval of spatial memory in the hippocampus. J Neurosci. 18:1998;7535-7542.
73. Hock B.J., Bunsey M.D. Differential effects of dorsal and ventral hippocampal lesions. J Neurosci. 18:1998;7027-7032.
74. Baxendale S.A., Kitchen N.D., Thompson P.J., Harkness W.F., Shorvon S.D. Postoperative hippocampal remnant shrinkage and memory decline: a dynamic process. Epilepsia. 1999;. in press.
75. Burgess N., Jeffery K.J., O'Keefe J. The Hippocampal and Parietal Foundations of Spatial Cognition. 1999;Oxford University Press, Oxford. An edited volume of recent research into how the hippocampal and parietal regions of the brain support spatial cognition, either alone or in cooperation. The chapters consider brain damage and functional imaging of the human brain, electrophysiological recording of single neurons in rats and primates, and computer simulation of the action of the networks of neurons. The introduction includes a theoretical framework in which to consider the spatial and mnemonic functions of the two areas.
76. Smith P.F. Vestibular-hippocampal interactions. Hippocampus. 7:1997;465-471.