Remote spatial memory in an amnesic person with extensive bilateral hippocampal lesions

Abstract

The hippocampus may have a time-limited role in memory, being needed only until information is permanently stored elsewhere, or this region may permanently represent long-term allocentric spatial information or cognitive maps in memory. To test these ideas, we investigated remote spatial memory in K.C., a patient with bilateral hippocampal lesions and amnesia for autobiographical events. In his spatial knowledge, general aspects were preserved, but details were lost, a pattern that resembled his memory loss in other domains. K.C. performed normally on allocentric spatial tests of his neighborhood and the world. He had difficulty, however, in recognizing and identifying non-salient neighborhood landmarks, and in recognizing city locations on world maps. This suggests that the hippocampus is not crucial for maintenance and retrieval of remotely formed spatial representations of major landmarks, routes, distances and directions, but is necessary for specifying location details, regardless of when they were acquired.

Access optionsAccess options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

Figure 1: Magnetic resonance imaging slices showing K.C.'s pathology.

References

  1. 1

    Teng, E. & Squire, L. R. Memory for places learned long ago is intact after hippocampal damage. Nature 400, 675–677 (1999).

  2. 2

    O'Keefe, J. & Nadel, L. The Hippocampus as a Cognitive Map (Clarendon, Oxford, 1978).

  3. 3

    Milner, B. Visually-guided maze-learning in man: Effects of bilateral hippocampal, bilateral frontal and unilateral cerebral lesions. Neuropsychologia 3, 317–338 (1965).

  4. 4

    Smith, M. L. & Milner, B. The role of the right hippocampus in the recall of spatial location. Neuropsychologia 19, 781–793 (1981).

  5. 5

    Maguire, E. A., Frackowiak, R. S. J. & Frith, C. D. Learning to find your way: A role for the human hippocampal formation. Proc. R. Soc. Lond. Biol. Sci. 263, 1745–1750 (1996).

  6. 6

    Nadel, L. & Moscovitch, M. Memory consolidation, retrograde amnesia and the hippocampal complex. Curr. Opin. Neurobiol. 7, 217–227 (1997).

  7. 7

    Moscovitch, M., Yaschyshyn, T., Ziegler, M. & Nadel, L. in Memory, Consciousness and the Brain: The Tallinn Conference (ed. Tulving, E.) 331–345 (Psychology Press, New York, 1999).

  8. 8

    Fujii, T., Moscovitch, M. & Nadel, L. in The Handbook of Neuropsychology Vol. 4 (eds. Boller, F. & Grafman, J.) (Elsevier, Amsterdam, in press).

  9. 9

    Tulving, E., Schacter, D. L., McLachlan, D. R. & Moscovitch, M. Priming of semantic autobiographical knowledge: A case study of retrograde amnesia. Brain Cogn. 8, 3–20 (1988).

  10. 10

    Tulving, E., Hayman, C. A. G. & Macdonald, C. A. Long-lasting perceptual priming and semantic learning in amnesia: A case experiment. J. Exp. Psychol. Learn. Mem. Cogn. 17, 595–617 (1991).

  11. 11

    Beatty, W. W. The Fargo Map Test: A standardized method for assessing remote memory for visuospatial information. J. Clin. Psychol. 44, 61–67 (1988).

  12. 12

    Milner, B., Corkin, S. & Teuber, H. L. Further analysis of the hippocampal amnesic syndrome: 14-year follow-up study of H.M. Neuropsychologia 6, 215–234 (1968).

  13. 13

    Beatty, W. W., Salmon, D. P., Bernstein, N. & Butters, N. Remote memory in a patient with amnesia due to hypoxia. Psychol. Med. 17, 657–665 (1987).

  14. 14

    Zola-Morgan, S., Squire, L. R. & Amaral, D. G. Human amnesia and the medial temporal region: enduring memory impairment following a bilateral lesion limited to field CA1 of the hippocampus. J. Neurosci. 6, 2950–2967 (1986).

  15. 15

    De Renzi, E. in Handbook of Clinical Neurology: Clinical Neuropsychology Vol. 1 (ed. Frederiks, J. A. M.) 405–422 (Elsevier, Amsterdam, 1985).

  16. 16

    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, 7103–7110 (1997).

  17. 17

    Aguirre, G. K. & D'Esposito, M. Topographical disorientation: a synthesis and taxonomy. Brain 122, 1613–1628 (1999).

  18. 18

    Habib, M. & Sirigu, A. Pure topographical disorientation: A definition and anatomical basis. Cortex 23, 73–85 (1987).

  19. 19

    Epstein, R. & Kanwisher, N. A cortical representation of the local visual environment. Nature 392, 598–601 (1998).

  20. 20

    Bohbot, V. et al. Lesions to the right parahippocampal cortex cause spatial memory deficits in humans. Neuropsychologia 36, 1217–1238 (1998).

  21. 21

    Suzuki, K., Yamadori, A., Hayakaw, Y. & Fujii, T. Pure topographical disorientation related to dysfunction of the viewpoint dependent visual system. Cortex 34, 589–599 (1998).

  22. 22

    Cammalleri, R. x Transient topographical amnesia and cingulate cortex damage: a case report. Neuropsychologia 34, 321–326 (1996).

  23. 23

    Katayama, K., Takahashi, N., Ogawara, K. & Hattori, T. Pure topographical disorientation due to right posterior cingulate lesion. Cortex 35, 279–282 (1999).

  24. 24

    Pearce, J. M., Roberts, A. D. L. & Good, M. Hippocampal lesions disrupt navigation based on cognitive maps but not heading vectors. Nature 396, 75–77 (1998).

  25. 25

    Kubie, J. L., Sutherland, R. J. & Muller, R.U. Hippocampal lesions produce a temporally-graded retrograde amnesia on a dry version of the Morris swimming task. Psychobiology 27, 313–330 (1999).

  26. 26

    Nadel, L. & Moscovitch, M. Hippocampal contributions to cortical plasticity. Neuropharmacology 37, 431–439 (1998).

  27. 27

    Riedel, G. et al. Reversible neural inactivation reveals hippocampal participation in several memory processes. Nat. Neurosci. 2, 898–905 (1999).

  28. 28

    Westmacott, R., Moscovitch, M. & Leach, L. Different patterns of autobiographical memory loss in medial temporal lobe amnesia and semantic dementia: A challenge to consolidation theory. Neurocase (in press).

  29. 29

    Tolman, E. C. Cognitive maps in rats and man. Psychol. Rev. 55, 189–208 (1948).

  30. 30

    Golledge, R. G., Smith, T. R., Pellegrino, J. W., Doherty, S. & Marshall, S. P. A conceptual model and empirical analysis of children's acquisition of spatial knowledge. J. Envir. Psychol. 5, 125–152 (1985).

  31. 31

    Smith, M. L. Recall of spatial location by the amnesic patient H.M. Brain Cogn. 7, 178–183 (1988).

Download references

Acknowledgements

We thank E. Tulving, I. Whishaw and G. Winocur for advice and discussions. This work was supported by a Medical Research Council of Canada (MRC) grant to M.M. and G.W. and formed part of R.S.R.'s University of Toronto Master's Thesis (June 1999).

Author information

Correspondence to R. Shayna Rosenbaum or Morris Moscovitch.

Rights and permissions

Reprints and Permissions

About this article

Further reading