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.
Subscribe to Journal
Get full journal access for 1 year
only $3.90 per issue
All prices are NET prices.
VAT will be added later in the checkout.
Rent or Buy article
Get time limited or full article access on ReadCube.
All prices are NET prices.
O'Keefe,J. A. & Nadel,L. The Hippocampus as a Cognitive Map (Clarendon, Oxford, 1978).
Olton,D. S., Becker,J. T. & Handelmann,G. E. Hippocampus, space and memory. Behav. Brain Sci. 2, 313–352 (1979).
Rawlins,J. N. P. & Olton,D. S. The septo-hippocampal system and cognitive mapping. Behav. Brain Res. 5, 331–358 (1982).
Nadel,L. The hippocampus and space revisited. Hippocampus 1, 221–229 (1991).
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).
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).
Muller,R. U., Stead,M. & Pach,J. The hippocampus as a cognitive graph. J. Gen. Physiol. 107, 663–694 (1996).
Tulving,E. & Markowitsch,H. J. Memory beyond the hippocampus. Curr. Opin. Neurobiol. 7, 209–216 (1997).
Vargha-Khadem,F. et al. Differential effects of early hippocampal pathology on episodic and semantic memory. Science 277, 376–380 (1997).
Squire,L. R. & Zola,S. M. Episodic memory, semantic memory, and amnesia. Hippocampus 8, 205–211 (1998).
Cohen,N. J. et al. Hippocampal system and declarative (relational) memory: Summarizing the data from functional neuroimaging studies. Hippocampus 9, 83–98 (1999).
Muller,R. A quarter of a century of place cells. Neuron 17, 813–822 (1996).
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).
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).
Touretzky,D. S. & Redish,A. D. Theory of rodent navigation based on interacting representations of space. Hippocampus 6, 247–270 (1996).
Samsonovich,A. & McNaughton,B. L. Path integration and cognitive mapping in a continuous attractor neural network model. J. Neurosci. 17, 5900–5920 (1997).
Lepage,M., Habib,R. & Tulving,E. Hippocampal PET activations of memory encoding and retrieval: The HIPER model. Hippocampus 8, 313–322 (1998).
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).
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).
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).
Moser,M. B. & Moser,E. I. Distributed encoding and retrieval of spatial memory in the hippocampus. J. Neurosci. 18, 7535–7542 (1998).
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).
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).
Eichenbaum,H. Thinking about cell assemblies. Science 261, 993–994 (1993).
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).
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).
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).
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).
Pedhazur,E. J. & Schmelkin,L. P. Measurement, Design and Analysis: An Integrated Approach (Erlbaum, Hillsdale, New Jersey, 1991).
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).
Wood,E., Dudchenko,P. A. & Eichenbaum,H. The global record of memory in hippocampal neuronal activity. Nature 397, 613–616 (1999).
Moser,M. B. & Moser,E. I. Functional differentiation in the hippocampus. Hippocampus 8, 608–619 (1998).
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).
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).
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).
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).
Amaral,D. G. & Witter,M. P. The three-dimensional organization of the hippocampal formation: a review of anatomical data. Neuroscience 31, 571–591 (1989).
Andersen,P., Bliss,T. V. P. & Skrede,K. K. Lamellar organization of hippocampal excitatory pathways. Exp. Brain Res. 13, 222–238 (1971).
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).
Wallenstein,G. V., Eichenbaum,H. & Hasselmo,M. E. The hippocampus as an associator of discontiguous events. Trends Neurosci. 21, 317–323 (1998).
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).
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).
Kohonen,T. & Hari,R. Where the abstract feature maps of the brain might come from. Trends Neurosci. 22, 135–139 (1999).
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).
Burgess,N. & O'Keefe,J. Neuronal computations underlying the firing of place cells and their role in navigation. Hippocampus 6, 749–762 (1996).
Rawlins,J. N. P. A place for space and smells. Nature 397, 561–563 (1999).
Deadwyler,S. A. & Hampson,R. E. Ensemble activity and behavior: What's the code? Science 270, 1316–1318 (1995).
Deadwyler,S. A. & Hampson,R. E. Annu. Rev. Neurosci. 20, 217–244 (1997).
We thank D. Byrd, J. Konstantopoulos, J. Brooks and T. Bunn for technical assistance. This work was supported by the NIDA and NIMH.
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) doi:10.1038/45154
Neurobiology of Learning and Memory (2019)
Journal of Neural Engineering (2018)
Frontiers in Systems Neuroscience (2018)
Scientific Reports (2018)