Abstract
The hippocampus is part of a system of structures in the medial temporal lobe that are essential for memory1,2,3. One influential view of hippocampal function emphasizes its role in the acquisition and retrieval of spatial knowledge4,5. By this view, the hippocampus constructs and stores spatial maps and is therefore essential for learning and remembering places, including those learned about long ago. We tested a profoundly amnesic patient (E.P.), who has virtually complete bilateral damage to the hippocampus and extensive damage to adjacent structures in the medial temporal lobe. We asked him to recall the spatial layout of the region where he grew up, from which he moved away more than 50 years ago. E.P. performed as well as or better than age-matched control subjects who grew up in the same region and also moved away. In contrast, E.P. has no knowledge of his current neighbourhood, to which he moved after he became amnesic. Our results show that the medial temporal lobe is not the permanent repository of spatial maps, and support the view that the hippocampus and other structures in the medial temporal lobe are essential for the formation of long-term declarative memories, both spatial and non-spatial, but not for the retrieval of very remote memories, either spatial or non-spatial3,6.
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References
Scoville, W. B. & Milner, B. Loss of recent memory after bilateral hippocampal lesions. J. Neurol. Neurosurg. Psychiat. 20, 11–21 (1957).
Mishkin, M. Memory in monkeys severely impaired by combined but not separate removal of the amygdala and hippocampus. Nature 273, 297–298 (1978).
Squire, L. R. Memory and the hippocampus: a synthesis from findings with rats, monkeys, and humans. Psychol. Rev. 99, 195–231 (1992).
O'Keefe, J. & Nadel, L. The Hippocampus as a Cognitive Map (Clarendon, Oxford, 1978).
Jarrard, L. E. What does the hippocampus really do? Behav. Brain Res. 71, 1–10 (1995).
Cohen, N. J. & Eichenbaum, H. Memory, Amnesia, and the Hippocampal System (MIT Press, Cambridge, Massachusetts, 1993).
Reed, J. M. & Squire, L. R. Retrograde amnesia for facts and events: Findings from four new cases. J. Neurosci. 18, 3943–3954 (1998).
Hamann, S. B. & Squire, L. R. Intact perceptual memory in the absence of conscious memory. Behav. Neurosci. 111, 850–854 (1997).
Reed, J. M., Hamann, S. B., Stefanacci, L. & Squire, L. R. When amnesic patients perform well on recognition memory tasks. Behav. Neurosci. 111, 1163–1170 (1997).
Batschelet, E. Statistical Methods for the Analysis of Problems in Animal Orientation and Certain Biological Rhythms (American Institute of Biological Sciences, Washington DC, 1965).
O'Keefe, J. & Dostrovsky, J. The hippocampus as a spatial map: Preliminary evidence from unit activity in the freely-moving rat. Brain Res. 34, 171–175 (1971).
Smith, M. L. & Milner, B. The role of the right hippocampus in the recall of spatial location. Neuropsychologia 19, 781–793 (1981).
Cave, C. B. & Squire, L. R. Equivalent impairment of spatial and nonspatial memory following damage to the human hippocampus. Hippocampus 1, 329–340 (1991).
Maguire, E. A., Burke, T., Phillips, J. & Staunton, H. Topographical disorientation following unilateral temporal lobe lesions in humans. Neuropsychologia 34, 993–1001 (1996).
Morris, R. G. M., Garrud, P., Rawlins, J. N. P. & O'Keefe, J. Place navigation in rats with hippocampal lesions. Nature 297, 681–683 (1982).
Aguirre, G. K., Detre, J. A., Alsop, D. C. & D'Esposito, M. D. The parahippocampus subserves topographical learning in man. Cereb. Cort. 6, 823–829 (1996).
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. 263, 1745–1750 (1996).
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).
Maguire, E. A.et al. Knowing where and getting there: A human navigation network. Science 280, 921–924 (1998).
Nadel, L. & Moscovitch, M. Memory consolidation, retrograde amnesia and the hippocampal complex. Curr. Opin. Neurobiol. 7, 217–227 (1997).
De Renzi, E., Faglioni, P. & Villa, P. Topographical amnesia. J. Neurol. Neurosurg. Psychiat. 40, 498–505 (1977).
Paterson, A. & Zangwill, O. L. Acase of topographical disorientation associated with a unilateral cerebral lesion. Brain 68, 188–211 (1945).
Levine, D. N., Warach, J. & Farah, M. Two visual systems in imagery: Dissociation of “what” and “where” in imagery disorders due to bilateral posterior cerebral lesions. Neurology 35, 1010–1018 (1985).
Bottini, G., Cappa, S., Geminiani, G. & Sterzi, R. Topographic disorientation — a case report. Neuropsychologia 28, 309–312 (1990).
Incisa della Rochetta, A., Cipolotti, L. & Warrington, EK. Topographical disorientation: Selective impairment of locomotor space? Cortex 32, 727–735 (1996).
Pai, M.-C. Topographic disorientation: Two cases. J. Formos. Med. Assoc. 96, 660–663 (1997).
Takahashi, N., Kawamura, M., Shiota, J., Kasahata, N. & Hirayama, K. Pure topographic disorientation due to right retrosplenial lesion. Neurology 49, 464–469 (1997).
Wechsler, D. Wechsler Memory Scale-III. Administration and Scoring Manual (Psychological Corporation, San Antonio, Texas, 1997).
Acknowledgements
We thank J. Zouzounis, L. Stefanacci, J. Frascino and the Hayward Area Historical Society for assistance. This work was supported by the Medical Research Service of the Department of Veterans Affairs, NIMH, and the McDonnell-Pew Center for Cognitive Neuroscience.
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Teng, E., Squire, L. Memory for places learned long ago is intact after hippocampal damage. Nature 400, 675–677 (1999). https://doi.org/10.1038/23276
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DOI: https://doi.org/10.1038/23276
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