Skip to main content

The Hippocampus and the Sense of Smell

  • Chapter
Chemical Signals in Vertebrates 6

Abstract

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).

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  • 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 

  • 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 

  • Brodai, A., 1947, The hippocampus and the sense of smell. A review, Brain 70: 179–222.

    Article  Google Scholar 

  • Devor, M., 1973, Components of mating behavior dissociated by lateral olfactory tract transection in male hamsters, Brain Res, 64: 437–441.

    Article  PubMed  CAS  Google Scholar 

  • 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 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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 

  • Eichenbaum, H., Otto, T., and Cohen, N.J., 1992, The hippocampus: What does it do? Ann. Rev. Neurosci. in press.

    Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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 

  • 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 

  • Larson, J., and Lynch, G., 1986, Induction of synaptic potentiation in hippocampus by patterned stimulation involves two events, Science 232: 985–988.

    CAS  Google Scholar 

  • 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 

  • Lynch, G., 1986, Synapses, Circuits, and the Beginnings of Memory. Cambridge MA: MIT Press.

    Google Scholar 

  • Lynch, G., Muller, D., Seubert, P., and Larson, J., 1988, Long-term potentiation: Persisting problems and recent results, Brain Res. Bull. 21: 363–372.

    CAS  Google Scholar 

  • 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 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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 

  • 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 

  • 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 

  • 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 

  • 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.

    CAS  Google Scholar 

  • 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 

  • 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 

  • 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.

    CAS  Google Scholar 

  • Rawlins, J.N.P., 1985, Associations across time: The hippocampus as a temporary memory store, Brain Behay. Sci., 8, 479–496.

    Google Scholar 

  • 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 

  • 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 

  • Slotnick, B.M., 1985, Olfactory discrimination in rats with anterior amygdales lesions, Behay. Neurosci. 99, 956–963.

    Google Scholar 

  • Squire, L.R., 1987, Memory and Brain. New York, NY: Oxford.

    Google Scholar 

  • 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 

  • Teyler, T.J., and DiScenna, P., 1986, The hippocampal memory indexing theory, Behay. Neurosci 100, 147–154.

    Google Scholar 

  • 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 

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

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 1992 Springer Science+Business Media New York

About this chapter

Cite this chapter

Eichenbaum, H., Otto, T. (1992). The Hippocampus and the Sense of Smell. In: Doty, R.L., Müller-Schwarze, D. (eds) Chemical Signals in Vertebrates 6. Springer, Boston, MA. https://doi.org/10.1007/978-1-4757-9655-1_12

Download citation

  • DOI: https://doi.org/10.1007/978-1-4757-9655-1_12

  • Publisher Name: Springer, Boston, MA

  • Print ISBN: 978-1-4757-9657-5

  • Online ISBN: 978-1-4757-9655-1

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics