Abstract
Hippocampal neurons provide a population code for location1. In young rats, environments are reliably ‘mapped’ by groups of neurons that have firing locations (‘place fields’2) that can be stable for several months3. Old animals exhibit deficits in spatial memory, raising the question of whether the quality or stability of their hippocampal ‘cognitive maps’4 is altered. By recording from large groups of neurons, we observed the hippocampal spatial code to be multistable. In young rats, the place field maps were reliable both within and between episodes in a familiar environment. In old rats, place field maps were accurate and stable during an episode, but frequently exhibited complete rearrangements between episodes. In a spatial memory task, both young and old rats exhibited bimodal performance, consistent with map multistability early in training. However, the performance of young rats became almost unimodal with further training, whereas that of old rats remained markedly bimodal. The multistability of the hippocampal map provides an insight into the dynamics of neural coding in high-level cortical structures and their changes during ageing, and may provide an explanation for the frequent failure of place recognition in elderly humans.
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References
Wilson, M. A. & McNaughton, B. L. Dynamics of the hippocampal ensemble code for space. Science 261, 1055 –1058 (1993).
O'Keefe, J. & Dostrovsky, J. The hippocampus as a spatial map. Preliminary evidence from unit activty in the freely-moving rat. Brain Res. 34, 171–175 ( 1971).
Thompson, L. T. & Best, P. J. Long-term stability of place-field activity of single units recorded from the dorsal hippocampus of freely behaving rats. Brain Res. 509, 299–308 (1990).
O'Keefe, J. & Nadel, L. The Hippocampus as a Cognitive Map (Clarendon, Oxford, (1978)).
Uttl, B. & Graf, P. Episodic spatial memory in adulthood. Psychol. Aging 8, 257 ( 1993).
Rapp, P. R. et al. Spatial learning and memory in freely moving monkeys. Soc. Neurosci. Abstr. 21, 1710 ( 1995).
Barnes, C. A. Memory deficits associated with senescence: A neurophysiological and behavioral study in the rat. J. Comp. Physiol. Psychol. 931, 74–104 (1979).
Barnes, C. A. Normal aging: Regionally specific changes in hippocampal synaptic transmission. Trends Neurosci. 17, 13– 18 (1994).
Geinisman, Y. et al. Hippocampal markers of age-related memory dysfunction: behavioral, electrophysiological and morphological perspectives. Prog. Neurobiol. 45, 223–252 ( 1995).
Landfield, P. W. Hippocampal neurobiological mechanisms of age-related memory dysfunction. Neurobiol. Aging 9, 571– 579 (1988).
deToledo-Morrell, L. et al. Age-dependent alterations in hippocampal synaptic plasticity: relation to memory disorders. Neurobiol. Aging 9, 581–590 (1988).
Markus, E. J. et al . Spatial information content and reliability of hippocampal CA1 neurons. Hippocampus 4, 410– 421 (1994).
Mizumori, S. J. Y., Lavoie, A. M. & Kalyani, A. Redistribution of spatial representation in the hippocampus of aged rats performing a spatial memory task. Behav. Neurosci. 110, 1006 (1996).
Shen, J. thesis, Univ. Arizona((1996)).
Quirk, G. J., Muller, R. U. & Kubie, J. L. The firing of hippocampal place cells in the dark depends on the rat's recent experience. J. Neurosci. 10, 2008–2017 (1990).
McNaughton, B. L. et al. Deciphering the hippocampal polyglot: The hippocampus as a path integration system. J. Exp. Biol. 199, 173–185 (1996).
McNaughton, B. L., Leonard, B. & Chen, L. Cortical-hippocampal interactions and cognitive mapping: A hypothesis based on reintegration of the parietal and inferotemporal pathways for visual processing. Psychobiology 17, 230–235 (1989).
Muller, R. U., Kubie, J. L. & Saypoff, R. The hippocampus as a cognitive graph: Abridged version. Hippocampus 1, 243–246 (1991).
Shapiro, M. L. & Hetherington, P. A. Asimple network model simulates hippocampal place fields: parametric analyses and physiological predictions. Behav. Neurosci. 107, 34–50 (1993).
Tsodyks, M. & Sejnowski, T. Int. J. Neural Syst. 6, 81–86 (1995).
Gothard, K. M., Skaggs, W. E. & McNaughton, B. L. Dynamics of mismatch correction in the hippocampal ensemble code for space: Interaction between path integration and environmental cues. J. Neurosci. 16, 8027– 8042 (1996).
Knierim, J. J., Kudrimoti, H. S. & McNaughton, B. L. Place cells, head direction cells, and the learning of landmark stability. J. Neurosci. 15, 1648–1659 (1995).
Skaggs, W. E. et al . in Advances in Neural Information Processing Systems Vol. 5(eds Hanson, S. J., Cowan, J. D. & Giles, C. L.) 1030 –1037 (Morgan Kaufmann, New York, ( 1993)).
Samsonovich, A. thesis, Univ. Arizona((1997)).
Gallagher, M., Burwell, R. & Burchinal, M. Severity of spatial learning impairment in aging: Development of a learning index for performance in the Morris water maze. Behav. Neurosci. 107, 618–626 (1993).
Spencer, R. L., O'Steen, W. K. & McEwen, B. S. Water maze performance of aged Sprague-Dawley rats in relation to retinal morphologic measures. Behav. Brain Res. 68, 139–150 ( 1995).
Barnes, C. A., McNaughton, B. L. & O'Keefe, J. Loss of place specificity in hippocampal complex-spike cells of senescent rat. Neurobiol. Aging 4, 113–119 (1983).
Nadel, L., Willner, J. & Kurz, E. M. in Context and Learning (eds Tomie, P. D. B. & Tomie, A.) 385–406 (Earlbaum, Hillsdale, New Jersey, (1985).
Morris, R. G. M. et al. Place navigation impaired in rats with hippocampal lesions. Nature 297, 681–683 (1982).
Kubie, J. L. & Ranck, J. B. J in Neurobiology of the Hippocampus (ed. Seifert, W.) 433–447 (Academic, London, (1983)).
Acknowledgements
We thank R. D'Monte, J. L. Gerrard, W. E. Skaggs, K. Stengel, J. Wang and K.L.Weaver for assistance with data acquisition and analysis; P. J. Best, D. Chialvo, L. Nadel, W. E. Skaggs and F. A. Wilson for comments on the manuscript, and D. Clayman for instigating the NIA extramural program through which this work was supported. This work was supported by NIA and NIMH.
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Barnes, C., Suster, M., Shen, J. et al. Multistability of cognitive maps in the hippocampus of old rats. Nature 388, 272–275 (1997). https://doi.org/10.1038/40859
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DOI: https://doi.org/10.1038/40859
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