The Hippocampus and the Sense of Smell



Brodal, in a 1947 review from which we boldly borrow the title of the present paper, outlined some of the critical evidence that ultimately led to the demise of the notion that the hippocampus was a part of the olfactory brain, or “rhinencephalon” as it was called according to the prevailing view of the time. Since then it has become abundantly clear that the hippocampus processes information from many input sources (cf. Deacon et al., 1983). Nevertheless, converging data from neuroanatomical, physiological, and behavioral studies indicate that the olfactory system projects heavily onto and has especially immediate access to the hippocampal system, suggesting that the olfactory-hippocampal pathway may be particularly useful for explorations of sensory-limbic interactions leading to the higher order coding of perceptual information. As will be described below, the intimate anatomical associations between the olfactory and hippocampal systems are paralleled by 1) the critical role played by the hippocampal system in odor-guided learning and memory, 2) the strong influence of olfactory processing over the physiological activity in the hippocampus both at the level of rhythmic EEG activity and at the level of neuronal firing patterns, and 3) the role these physiological processes may play in the induction of synaptic plasticity supporting memory formation. Thus, in the spirit of a “renaissance of the rhinencephalon” (Macrides, 1977), we will argue that olfaction is a particularly advantageous model system for studies of “sensory” processing by the hippocampus across behavioral, neuronal, and synaptic levels of analysis. Our data on studies at each of these levels of analysis will be discussed in turn (see also Otto and Eichenbaum, 1992b).


Entorhinal Cortex Probe Trial Theta Rhythm Odor Pair Odor Discrimination 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Bermudez-Rattoni, F., Keifer, S.W., Grijalva, C.V., and Garcia, J., 1982, Basal and central amygdala involvement in the acquisition of taste and odor aversions, Soc. Neurosci. Abst., 4, 501.Google Scholar
  2. Bermudez-Rattoni, F., Rusiniak, K.W., and Garcia, J., 1983, Flavor-illness aversions: Potentiation of odor by taste is disrupted by application of novocaine to the amygdala, Behay. Neurol. Biol., 37:61–75.Google Scholar
  3. Brodai, A., 1947, The hippocampus and the sense of smell. A review, Brain 70: 179–222.CrossRefGoogle Scholar
  4. Devor, M., 1973, Components of mating behavior dissociated by lateral olfactory tract transection in male hamsters, Brain Res, 64: 437–441.PubMedCrossRefGoogle Scholar
  5. Eichenbaum, H., Cohen, N.J., Otto, T., and Wible, C.G., 1992b, Memory representation in the hippocampus: Functional domain and functional organization. In Memory: Organization and Locus of Channe L.R. Squire, G. Lynch, N.M. Weinberger, and J.L. McGaugh, Eds., Oxford University Press.Google Scholar
  6. Eichenbaum, H., Fagan, A., and Cohen, N.J., 1986, Normal olfactory discrim- ination learning set and facilitation of reversal learning after medial-temporal damage in rats: Implications for an account of pre-served learning abilities in amnesia, J. Neurosci. 6: 1876–1884.PubMedGoogle Scholar
  7. Eichenbaum, H., Fagan, A., Mathews, P., and Cohen, N.J., 1988, Hippocampal system dysfunction and odor discrimination learning in rats: Impair-ment or facilitation depending on representational demands, Behay. Neurosci. 102:331–339.Google Scholar
  8. Eichenbaum, H., Kuperstein, M., Fagan, A., and Nagode, J., 1987, Cue-sampling and goal-approach correlates of hippocampal unit activity in rats performing an odor-discrimination task, J. Neurosci. 7: 716–732.PubMedGoogle Scholar
  9. Eichenbaum, H., Mathews, P., and Cohen, N.J., 1989, Further studies of hippocampal representation during odor discrimination learning. Behay. Neurosci. 103:1207–1216.Google Scholar
  10. Eichenbaum, H., Otto, T., and Cohen, N.J., 1992, The hippocampus: What does it do? Ann. Rev. Neurosci. in press.Google Scholar
  11. Eichenbaum, H., Shedlack, K., and Eckmann, K., 1980, Thalamocortical mechanisms in olfaction, I. Effects of lesion of the mediodorsal thalamic nucleus and frontal cortex on olfactory discrimination in the rat, Brain Behay. Evol. 17: 255–275.CrossRefGoogle Scholar
  12. Jay, T.M., Glowinski, J., and Thierry, A.M., 1989, Selectivity of the hippocampal projection to the prelimbic area of the prefrontal cortex in the rat, Brain Res. 202: 337–340.Google Scholar
  13. Laroche, S., Jay, T.M., and Thierry, A., 1990, Long-term potentiation in the prefrontal cortex following stimulation of the hippocampal CA1/subicular region, Neurosci. Letters 114:184–190.Google Scholar
  14. Larson, J., and Lynch, G., 1986, Induction of synaptic potentiation in hippocampus by patterned stimulation involves two events, Science 232: 985–988.Google Scholar
  15. Larson, J., Wong, D., and Lynch, G., 1986, Patterned stimulation at the theta frequency is optimal for the induction of hippocampal long-term potentiation, Brain Res. 441: 111–118.Google Scholar
  16. Lynch, G., 1986, Synapses, Circuits, and the Beginnings of Memory. Cambridge MA: MIT Press.Google Scholar
  17. Lynch, G., Muller, D., Seubert, P., and Larson, J., 1988, Long-term potentiation: Persisting problems and recent results, Brain Res. Bull. 21: 363–372.Google Scholar
  18. Macrides, F., 1977, Dynamic aspects of central olfactory processing. In Chemical Signals in Vertebrates, D. Muller-Schwarze and M.M. Mozell (Eds.). New York: Plenum, pp. 449–514.Google Scholar
  19. Macrides, F., Eichenbaum, H.B., and Forbes, W.B., 1982, Temporal relationship between sniffing and the limbic theta rhythm during odor discrimination reversal learning, J Neurosci. 2: 1705–1717.PubMedGoogle Scholar
  20. Macrides, F., Firl, A.C., Schneider, S.P., Bartke, A., and Stein, D.G., 1976, Effects of one stage or serial transections of the lateral olfactory tracts on behavior and plasma testosterone levels in male hamsters, Brain Res., 109: 97–109.PubMedGoogle Scholar
  21. Morris, R.G.M., Davis, S., Butcher, S.P., 1990, Hippocampal synaptic plasticity and NMDA receptors: A role in information storage? Philosophic Trans. Roy. Soc., London, 329, 187–204.Google Scholar
  22. Otto, T., and Eichenbaum, H., 1991, Dissociable roles of orbitofrontal cortex and the hippocampal system in an odor-guided delayed non-matching to sample task, Soc. Neurosci. Abst. 17.Google Scholar
  23. Otto, T., and Eichenbaum, H., 1992a, Olfactory learning and memory in the rat: A “model system” for studies on the neurobiology of memory. In The Science of Olfaction, M. Serby, K. Chobor (Eds). New York: Springer-Verlag, in press.Google Scholar
  24. Otto, T., and Eichenbaum, H., 1992b, Toward a comprehensive account of hippocampal function: Studies of olfactory learning permit an integration of data across multiple levels of neurobiological analysis. In Neuropsychology of Memory, N. Butters und L.R. Squire ( Eds. ), In Press.Google Scholar
  25. Otto, T., Eichenbaum, H., Wiener, S.I., and Wible, C.G., 1991a, Learning-related patterns of CA1 spike trains parallel stimulation parameters optimal for inducing hippocampal long term potentiation, Hippocampus 1, 181–192.Google Scholar
  26. Otto, T., Eichenbaum, H., and Wible, C.G., 1990, Behavioral correlates of hippocampal unit activity in an odor-guided delayed non-matching to sample task, Soc. Neurosci. Abst. 16, 263.Google Scholar
  27. Otto, T., Schottler, F., Staubli, U., Eichenbaum, H., and Lynch, G., 1991b, The hippocampus and olfactory discrimination learning: Effects of entorhinal cortex lesions on learning-set acquisition and on odor memory in a successive-cue, go/no-go task, Behay. Neurosci. 105, 111–119.Google Scholar
  28. Pavlides, C., Greenstein, Y.J., Grudman, M., and Winson, J., 1988, Longterm potentiation in the dentate gyrus is induced preferentially on the positive phase of theta rhythm, Brain Res. 439, 383–387.Google Scholar
  29. Rawlins, J.N.P., 1985, Associations across time: The hippocampus as a temporary memory store, Brain Behay. Sci., 8, 479–496.Google Scholar
  30. Rose, G.M., and Dunwiddie, T.V., 1986, Induction of hippocampal long-term potentiation using physiologically-patterned stimulation, Neurosci. Lett. 69, 244–248.Google Scholar
  31. Rudell, A., Fox, S., and Ranck, J.B., Jr., 1980, Hippocampal excitability phase-locked to the theta rhythm in walking rats, Exp. Neurol. 68, 87–96.Google Scholar
  32. Slotnick, B.M., 1985, Olfactory discrimination in rats with anterior amygdales lesions, Behay. Neurosci. 99, 956–963.Google Scholar
  33. Squire, L.R., 1987, Memory and Brain. New York, NY: Oxford.Google Scholar
  34. Staubli, U., Ivy, G., and Lynch, G., 1984, Hippocampal denervation causes rapid forgetting of olfactory information in rats, Proc. Nat. Acad. Sci. USA, 81, 5885–5887.Google Scholar
  35. Teyler, T.J., and DiScenna, P., 1986, The hippocampal memory indexing theory, Behay. Neurosci 100, 147–154.Google Scholar
  36. VanGroen, T., and Wyss, J.M., 1990, Extrinsic projections from area CA1 of the rat hippocampus: Olfactory, cortical, subcortical, and bilateral hippocampal formation projections, J. Comp. Neurol. 303, 1–14.Google Scholar
  37. Wiener, S.I., Paul, C.A., and Eichenbaum, H., 1989, Spatial and behavioral correlates of hippocampal neuronal activity, J. Neurosci. 9, 2737–2763.PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 1992

Authors and Affiliations

  1. 1.Department of PsychologyUniversity of North Carolina at Chapel HillChapel HillUSA

Personalised recommendations