Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Letter
  • Published:

The global record of memory in hippocampal neuronal activity

Abstract

In humans the hippocampal region of the brain is crucial for declarative1 or episodic2 memory for a broad range of materials. In contrast, there has been controversy over whether the hippocampus mediates a similarly general memory function in other species, or whether it is dedicated to spatial memory processing3,4,5,6. Evidence for the spatial view is derived principally from the observations of ‘place cells’—hippocampal neurons that fire whenever the animal is in a particular location in its environment7,8, or when it perceives a specific stimulus or performs a specific behaviour in a particular place3,4. We trained rats to perform the same recognition memory task in several distinct locations in a rich spatial environment and found that the activity of many hippocampal neurons was related consistently to perceptual, behavioural or cognitive events, regardless of the location where these events occurred. These results indicate that non-spatial events are fundamental elements of hippocampal representation, and support the view that, across species, the hippocampus has a broad role in information processing associated with memory.

This is a preview of subscription content, access via your institution

Access options

Rent or buy this article

Prices vary by article type

from$1.95

to$39.95

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Continuous non-matching to sample task.
Figure 2: Examples of task-related firing patterns of hippocampal neurons.
Figure 3: Different groups of hippocampal neurons discriminate odours, positions, match/non-match trial types and approach period.

Similar content being viewed by others

References

  1. Cohen, N. J. & Squire, L. R. Preserved learning and retention of pattern analyzing skill in amnesia: dissociation of knowing how and knowing that. Science 210, 207–210 (1980).

    Article  ADS  CAS  Google Scholar 

  2. Vargha-Khadem, F. et al. Differential effects of early hippocampal pathology on episodic and semantic memory. Science 277, 376–380 (1997).

    Article  CAS  Google Scholar 

  3. O'Keefe, J. & Nadel, L. The Hippocampus as a Cognitive Map (Oxford University Press, London, (1978)).

    Google Scholar 

  4. Nadel, L. The hippocampus and space revisited. Hippocampus 1, 221–229 (1991) and accompanying debate, 230–291.

    Article  CAS  Google Scholar 

  5. Cohen, N. J. & Eichenbaum, H. Memory, Amnesia and the Hippocampal System (MIT Press, Cambridge, Massachusetts, (1993)).

  6. Jarrard, L. E. On the role of the hippocampus in learning and memory in the rat. Behav. Neural Biol. 60, 9–26 (1993).

    Article  CAS  Google Scholar 

  7. 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).

    Article  CAS  Google Scholar 

  8. Muller, R. U., Kubie, J. L. & Ranck, J. B. Spatial firing patterns of hippocampal complex-spike cells in a fixed environment. J. Neurosci. 7, 1935–1950 (1987).

    Article  CAS  Google Scholar 

  9. Ranck, J. B. Studies on single neurons in dorsal hippocampal formation and septum in unrestrained rats. Part 1. Behavioral correlates and firing repertoires. Exp. Neurol. 41, 461–531 (1973).

    Article  Google Scholar 

  10. Berger, T. W., Rinaldi, P. C., Weisz, D. J. & Thompson, R. F. Single-unit analysis of different hippocampal cell types during classical conditioning of rabbit nicitating membrane response. J. Neurophysiol. 50, 1197–1219 (1983).

    Article  CAS  Google Scholar 

  11. Weiss, C., Kronforst-Collins, M. A. & Disterhoft, J. F. Activity of hippocampal pyramidal neurons during trace eyeblink conditioning. Hippocampus 6, 192–209 (1996).

    Article  CAS  Google Scholar 

  12. Wible, C. G. et al. Mnemonic correlates of unit activity in the hippocampus. Brain Res. 399, 97–110 (1986).

    Article  CAS  Google Scholar 

  13. Eichenbaum, H., Kuperstein, M., Fagan, A. & Nagode, J. Cue-sampling and goal-approach correlates of hippocampal unit activity in rats performing an odour-discrimination task. J. Neurosci. 7, 716–732 (1987).

    Article  CAS  Google Scholar 

  14. Wiener, S. I., Paul, C. A. & Eichenbaum, H. Spatial and behavioral correlates of hippocampal neuronal activity. J. Neurosci. 9, 2737–2763 (1989).

    Article  CAS  Google Scholar 

  15. Deadwyler, S. A., Bunn, T. & Hampson, R. E. Hippocampal ensemble activity during spatial delayed-nonmatch-to-sample performance in rats. J. Neurosci. 16, 354–372 (1996).

    Article  CAS  Google Scholar 

  16. Rolls, E. T., Cahusac, P. M. B., Feigenbaum, J. D. & Miyashita, Y. Responses of single neurons in the hippocampus of the macaque related to recognition memory. Exp. Brain Res. 93, 299–306 (1993).

    Article  CAS  Google Scholar 

  17. Wilson, F. A. W., Riches, I. P. & Brown, M. W. Hippocampus and medial temporal cortex: Neuronal activity related to behavioral responses during the performance of memory tasks by primates. Behav. Brain Res. 40, 7–28 (1990).

    Article  CAS  Google Scholar 

  18. Otto, T. & Eichenbaum, H. Neuronal activity in the hippocampus during delayed non-match to sample performance in rats: evidence for hippocampal processing in recognition memory. Hippocampus 2, 323–334 (1992).

    Article  CAS  Google Scholar 

  19. Sakurai, Y. Involvement of auditory cortical and hippocampal neurons in auditory working memory and reference memory in the rat. J. Neurosci. 14, 2606–2623 (1994).

    Article  CAS  Google Scholar 

  20. Young, B. J., Fox, G. D. & Eichenbaum, H. Correlates of hippocampal complex-spike activity in rats performing a nonspatial radial maze task. J. Neurosci. 14, 6553–6563 (1994).

    Article  CAS  Google Scholar 

  21. Gothard, K. M., Skaggs, W. E., Moore, K. M. & McNaughton, B. L. Binding of hippocampal CA1 neural activity to multiple reference frames in a landmark-based navigation task. J. Neurosci. 16, 823–835 (1996).

    Article  CAS  Google Scholar 

  22. 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, 8027–8040 (1996).

    Article  CAS  Google Scholar 

  23. O'Keefe, J. & Burgess, N. Geometric determinants of the place fields of hippocampal neurons. Nature 381, 425–428 (1996).

    Article  ADS  CAS  Google Scholar 

  24. Bunsey, M. & Eichenbaum, H. Conservation of hippocampal memory function in rats and humans. Nature 379, 255–257 (1996).

    Article  ADS  CAS  Google Scholar 

  25. Morris, R. G. M. & Frey, U. Hippocampal synaptic plasticity: role in spatial learning or the automatic recording of attended experience? Phil. Trans. R. Soc. Lond. B 352, 1489–1503 (1997).

    Article  ADS  CAS  Google Scholar 

  26. Tanila, H., Shapiro, M., Gallagher, M. & Eichenbaum, H. Brain aging: changes in the nature of information coding by the hippocampus. J. Neurosci. 17, 5155–5166 (1997).

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank J. O'Keefe for helping to design the experiment, and M. Burchinal for statistical advice. This work was supported by NIMH and NIA.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Howard Eichenbaum.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Wood, E., Dudchenko, P. & Eichenbaum, H. The global record of memory in hippocampal neuronal activity. Nature 397, 613–616 (1999). https://doi.org/10.1038/17605

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/17605

This article is cited by

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing