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.

  • Article
  • Published:

Distribution of spatial and nonspatial information in dorsal hippocampus

Abstract

The hippocampus in the mammalian brain is required for the encoding of current and the retention of past experience. Previous studies have shown that the hippocampus contains neurons that encode information required to perform spatial and nonspatial short-term memory tasks. A more detailed understanding of the functional anatomy of the hippocampus would provide important insight into how such encoding occurs. Here we show that hippocampal neurons in the rat are distributed anatomically in distinct segments along the length of the hippocampus. Each longitudinal segment contains clusters of neurons that become active when the animal performs a task with spatial attributes. Within these same segments are ordered arrangements of neurons that encode the nonspatial aspects of the task appropriate to those spatial features. Thus, anatomical segregation of spatial information, together with the interleaved representation of nonspatial information, represents a structural framework that may help to resolve conflicting views of hippocampal function.

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: Multi-electrode recording during delayed-nonmatch-to-sample (DNMS) task.
Figure 2: Anatomical localization of cell firing correlates.
Figure 3: Distribution of conjunctive and trial-type cells mapped onto position and phase cell gradients shown in Fig. 2c.

Similar content being viewed by others

References

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

    Google Scholar 

  2. Olton,D. S., Becker,J. T. & Handelmann,G. E. Hippocampus, space and memory. Behav. Brain Sci. 2, 313–352 (1979).

    Article  Google Scholar 

  3. Rawlins,J. N. P. & Olton,D. S. The septo-hippocampal system and cognitive mapping. Behav. Brain Res. 5, 331–358 (1982).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  5. Cohen,N. J. & Eichenbaum, H. The theory that wouldn't die: a critical look at the spatial mapping theory of hippocampal function. Hippocampus 1, 265–268 (1991).

    Article  CAS  Google Scholar 

  6. Morris,R. G. & Frey,U. Hippocampal synaptic plasticity: role in spatial learning or the automatic recording of attended experience? Phil. Trans. R. Soc. Lond. B. Biol. Sci. 29, 1489–1503 (1997).

    Article  ADS  Google Scholar 

  7. Muller,R. U., Stead,M. & Pach,J. The hippocampus as a cognitive graph. J. Gen. Physiol. 107, 663–694 (1996).

    Article  CAS  Google Scholar 

  8. Tulving,E. & Markowitsch,H. J. Memory beyond the hippocampus. Curr. Opin. Neurobiol. 7, 209–216 (1997).

    Article  CAS  Google Scholar 

  9. 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 

  10. Squire,L. R. & Zola,S. M. Episodic memory, semantic memory, and amnesia. Hippocampus 8, 205–211 (1998).

    Article  CAS  Google Scholar 

  11. Cohen,N. J. et al. Hippocampal system and declarative (relational) memory: Summarizing the data from functional neuroimaging studies. Hippocampus 9, 83–98 (1999).

    Article  CAS  Google Scholar 

  12. Muller,R. A quarter of a century of place cells. Neuron 17, 813–822 (1996).

    Article  CAS  Google Scholar 

  13. Shapiro,M. L., Tanila,H. & Eichenbaum,H. Cues that hippocampal place cells encode: dynamic and hierarchical representation of local and distal stimuli. Hippocampus 7, 624–642 (1997).

    Article  CAS  Google Scholar 

  14. 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 

  15. Touretzky,D. S. & Redish,A. D. Theory of rodent navigation based on interacting representations of space. Hippocampus 6, 247–270 (1996).

    Article  CAS  Google Scholar 

  16. Samsonovich,A. & McNaughton,B. L. Path integration and cognitive mapping in a continuous attractor neural network model. J. Neurosci. 17, 5900–5920 (1997).

    Article  CAS  Google Scholar 

  17. Lepage,M., Habib,R. & Tulving,E. Hippocampal PET activations of memory encoding and retrieval: The HIPER model. Hippocampus 8, 313–322 (1998).

    Article  CAS  Google Scholar 

  18. Gabrielli,J. D., Brewer,J. B. & Poldrack,R. A. Images of medial temporal lobe functions in human learning and memory. Neurobiol. Learn. Mem. 70, 275–283 (1998).

    Article  Google Scholar 

  19. Schacter,D. L. & Wagner,A. D. Medial temporal lobe activation in fMRI and PET studies of episodic encoding and retrieval. Hippocampus 9, 7–24 (1999).

    Article  CAS  Google Scholar 

  20. Burwell,R. D., Wittner,M. P. & Amaral,D. G. Perirhinal and postrhinal cortices of the rat: a review of the neuroanatomical literature and comparison with findings from the monkey brain. Hippocampus 5, 390–408 (1995).

    Article  CAS  Google Scholar 

  21. Moser,M. B. & Moser,E. I. Distributed encoding and retrieval of spatial memory in the hippocampus. J. Neurosci. 18, 7535–7542 (1998).

    Article  CAS  Google Scholar 

  22. Hampson,R. E., Byrd,D. R., Konstantopoulos,J. K., Bunn,T. & Deadwyler,S. A. Hippocampal place fields and spike-train correlation: Relationship between degree of place field overlap and cross-correlation. Hippocampus 6, 281–293 (1996).

    Article  CAS  Google Scholar 

  23. Eichenbaum,H., Wiener,S. I., Shapiro,M. L. & Cohen,N. J. The organization of spatial coding in the hippocampus: A study of neural ensemble activity. J. Neurosci. 9, 2764–2775 (1989).

    Article  CAS  Google Scholar 

  24. Eichenbaum,H. Thinking about cell assemblies. Science 261, 993–994 (1993).

    Article  ADS  CAS  Google Scholar 

  25. Hampson,R. E., Jarrard,L. E. & Deadwyler,S. A. Effects of ibotenate hippocampal destruction on delayed matching and nonmatching to sample behavior in rats. J. Neurosci. 19, 1492–1507 (1999).

    Article  CAS  Google Scholar 

  26. Hampson,R. E., Rogers,G., Lynch,G. & Deadwyler,S. A. Facilitative effects of the ampakine CX516 on short-term memory in rats: Enhancement of delayed-nonmatch-to-sample performance. J. Neurosci. 18, 2740–2747 (1998).

    Article  CAS  Google Scholar 

  27. Hampson,R. E. & Deadwyler,S. A. Ensemble codes involving hippocampal neurons are at risk during delayed performance tests. Proc. Natl Acad. Sci. USA 93, 13487–13493 (1996).

    Article  ADS  CAS  Google Scholar 

  28. Hampson,R. E., Rogers,G., Lynch,G. & Deadwyler,S. A. Facilitative effects of the ampakine CX516 on short-term memory in rats: Correlations with hippocampal ensemble activity. J. Neurosci. 18, 2748–2763 (1998).

    Article  CAS  Google Scholar 

  29. Pedhazur,E. J. & Schmelkin,L. P. Measurement, Design and Analysis: An Integrated Approach (Erlbaum, Hillsdale, New Jersey, 1991).

    Google Scholar 

  30. Colombo,M., Fernandez,T., Nakamura,K. & Gross,C. G. Functional differentiation along the anterior-posterior axis of the hippocampus in monkeys. J. Neurophysiol. 80, 1002–1005 (1998).

    Article  CAS  Google Scholar 

  31. Wood,E., Dudchenko,P. A. & Eichenbaum,H. The global record of memory in hippocampal neuronal activity. Nature 397, 613–616 (1999).

    Article  ADS  CAS  Google Scholar 

  32. Moser,M. B. & Moser,E. I. Functional differentiation in the hippocampus. Hippocampus 8, 608–619 (1998).

    Article  CAS  Google Scholar 

  33. Hirsch,J. A., Alonso,J. M., Reid,R. C. & Martinez,L. M. Synaptic integration in striate cortical simple cells. J. Neurosci. 18, 9517–9528 (1998).

    Article  CAS  Google Scholar 

  34. Hubel,D. H. & Wiesel,T. N. Receptive fields, binocular interaction and functional architecture in the cat's visual cortex. J. Physiol. (Lond.) 160, 106–154 (1962).

    Article  CAS  Google Scholar 

  35. Ishizuka,N., Weber,J. & Amaral,D. G. Organization of intrahippocampal projections originating from CA3 pyramidal cells in the rat. J. Comp. Neurol. 295, 580–623 (1990).

    Article  CAS  Google Scholar 

  36. Li,X. G., Somogyi,P., Ylinen,A. & Buzsaki,G. The hippocampal CA3 network: an in vivo intracellular labeling study. J. Comp. Neurol. 339, 181–208 (1994).

    Article  CAS  Google Scholar 

  37. Amaral,D. G. & Witter,M. P. The three-dimensional organization of the hippocampal formation: a review of anatomical data. Neuroscience 31, 571–591 (1989).

    Article  CAS  Google Scholar 

  38. Andersen,P., Bliss,T. V. P. & Skrede,K. K. Lamellar organization of hippocampal excitatory pathways. Exp. Brain Res. 13, 222–238 (1971).

    CAS  PubMed  Google Scholar 

  39. Dolorfo,C. L. & Amaral,D. G. Entorhinal cortex of the rat: topographic organization of the cells of origin of the perforant path projection to the dendrate gyrus. J. Comp. Neurol. 398, 25–48 (1998).

    Article  CAS  Google Scholar 

  40. Wallenstein,G. V., Eichenbaum,H. & Hasselmo,M. E. The hippocampus as an associator of discontiguous events. Trends Neurosci. 21, 317–323 (1998).

    Article  CAS  Google Scholar 

  41. 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 

  42. McClelland,J. L. Complementary learning systems in the brain. A connectionist approach to explicit and implicit cognition and memory. Ann. NY Acad. Sci. 843, 153–169 (1998).

    Article  ADS  CAS  Google Scholar 

  43. Kohonen,T. & Hari,R. Where the abstract feature maps of the brain might come from. Trends Neurosci. 22, 135–139 (1999).

    Article  CAS  Google Scholar 

  44. Stern,C. E. et al. The hippocampal formation participates in novel picture encoding: evidence from functional magnetic resonance imaging. Proc. Natl Acad. Sci. USA 93, 8660–8665 (1996).

    Article  ADS  CAS  Google Scholar 

  45. Burgess,N. & O'Keefe,J. Neuronal computations underlying the firing of place cells and their role in navigation. Hippocampus 6, 749–762 (1996).

    Article  CAS  Google Scholar 

  46. Rawlins,J. N. P. A place for space and smells. Nature 397, 561–563 (1999).

    Article  ADS  CAS  Google Scholar 

  47. Deadwyler,S. A. & Hampson,R. E. Ensemble activity and behavior: What's the code? Science 270, 1316–1318 (1995).

    Article  ADS  CAS  Google Scholar 

  48. Deadwyler,S. A. & Hampson,R. E. Annu. Rev. Neurosci. 20, 217–244 (1997).

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank D. Byrd, J. Konstantopoulos, J. Brooks and T. Bunn for technical assistance. This work was supported by the NIDA and NIMH.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Sam A. Deadwyler.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Hampson, R., Simeral, J. & Deadwyler, S. Distribution of spatial and nonspatial information in dorsal hippocampus. Nature 402, 610–614 (1999). https://doi.org/10.1038/45154

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/45154

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