Advertisement

Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

Polysynaptic activation of the dentate gyrus of the hippocampal formation: An olfactory input via the lateral entorhinal cortex

  • 137 Accesses

  • 54 Citations

Summary

The possibility that olfactory input is transmitted to specific subregions of the hippocampal formation via the entorhinal cortex was investigated electrophysiologically by analyzing the laminar profiles of potentials evoked in the hippocampal formation by stimulation of the lateral olfactory tract (LOT). LOT stimulation resulted in long latency (14–20 ms) evoked responses in the dentate gyrus of the hippocampal formation ipsilateral to the stimulation. The variable long latency of these responses and their inability to follow stimulus rates of 40/s suggested that these potentials reflected polysynaptic activation. Analysis of the laminar profiles of the evoked potentials indicated that the responses originated from a synaptic field localized in the outer portion of the stratum moleculare of the dentate gyrus, a terminal distribution which overlaps that of the lateral entorhinal cortical (LEC) projection to the dentate gyrus. Lesions of the LEC eliminated the long latency responses in the dentate gyrus evoked by LOT stimulation. In addition, a conditioning pulse delivered either to the LOT or to the LEC produced paired pulse potentiation of the response elicited by subsequent stimulation of the other structure. No evidence was found to indicate that responses were generated in regio superior of the hippocampus proper following LOT stimulation. Taken together, these results suggest that stimulation of the LOT activates the dentate gyrus of the hippocampal formation by multisynaptic pathways which relay through the lateral portion of the entorhinal area. This finding is discussed with regard to entorhinal cortical organization and the known olfactory projections to the LEC.

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

References

  1. Berry, C.M., Hagamen, W.D., Hinsey, J.C.: Distribution of potentials following stimulation of olfactory bulb in cat. J Neurophysiol 15, 139–148 (1952)

  2. Broadwell, R.D.: Olfactory relationships of the telecephalon and diencephalon in the rabbit. II. An autoradiographic and horseradish peroxidase study of the efferent connections of the anterior olfactory nucleus. J Comp Neurol 164, 389–410 (1975)

  3. Broca, P.O.: Anatomie comparée des circonvolutions cérébrales. Le grand lobe limbique et la scissure limbique dans la série des mammifères. Rev Anthrop (Paris) 1, 385–498 (1878)

  4. Brodal, A.: The hippocampus and the sense of smell. Brain 70, 179–222 (1947)

  5. Clark, W.E. Le Gros, Meyer, M.: The terminal connections of the olfactory tract in the rabbit. Brain 70, 304–328 (1947)

  6. Cragg, B.G.: Responses of the hippocampus to stimulation of the olfactory bulb and of various afferent nerves in five mammals. Exp Neurol 2, 547–571 (1960)

  7. Cragg, B.G.: Olfactory and other afferent connections of the hippocampus in the rabbit, rat and cat. Exp Neurol 3, 588–600 (1961)

  8. Elliott-Smith, G.: On the morphology of the cerebral commissure in the vertebrate. Trans Linn Soc Lond (Zool) 8, 455–500 (1903)

  9. Fox, C.A., Schmidt, J.T.: A Marchi study of the distribution of the anterior commissure in the cat. J Comp Neurol 79, 297–314 (1943)

  10. Gergen, J.A., MacLean, P.D.: The limbic system: Photic activation of limbic cortical areas in the squirrel monkey. Ann N Y Acad Sci 117, 69–87 (1964)

  11. Gloor, P.: Electrophysiological studies on the connections of the amygdaloid nucleus in the cat. Part II: The electrophysiological properties of the amygdaloid projection system. Electroencephalogr Clin Neurophysiol 7, 243–264 (1955)

  12. Gloor, P., Vera, C.L., Sperti, L.: Electrophysiological studies of hippocampal neurons. I. Configuration and laminar analysis of the “resting” potential gradient, of the main-transient response to perforant path, fimbrial and mossy fiber volleys and of “spontaneous” activity. Electroencephalogr Clin Neurophysiol 15, 353–378 (1963)

  13. Heimer, L.: Synaptic distribution of centripetal and centrifugal nerve fibers in the olfactory system of the rat. An experimental anatomical study. J Anat 103, 413–432 (1968)

  14. Kerr, D.I.B., Dennis, B.J.: Collateral projection of the lateral olfactory tract to entorhinal cortical areas in the cat. Brain Res 35, 399–403 (1972)

  15. Krettek, J.E., Price, J.L.: Projections from the amygdaloid complex and adjacent olfactory structures to the entorhinal cortex and to the subiculum in the rat and cat. J Comp Neurol 172, 723–752 (1977)

  16. Lømo, T.: Patterns of activation in a monosynaptic cortical pathway: The perforant path input to the dentate area of the hippocampal formation. Exp Brain Res 12, 18–45 (1971a)

  17. Lømo, T.: Potentiation of monosynaptic EPSP's in the perforant path-dentate granule cell synapse. Exp Brain Res 12, 46–63 (1971b)

  18. Lorente de Nó, R.: Studies on the structure of the cerebral cortex. I. The area entorhinalis. J Psychol Neurol (Lpz) 45, 381–438 (1933)

  19. McNaughton, B.C., Barnes, C.A.: Physiological identification and analysis of dentate granule cell responses to stimulation of the medial and lateral perforant pathways in the rat. J Comp Neurol 175, 439–454 (1977)

  20. Price, J.L.: An autoradiographic study of complementary laminar patterns of termination of afferent fibers to the olfactory cortex. J Comp Neurol 150, 87–108 (1973)

  21. Ramón y Cajal, S.: “Studies on the Cerebral Cortex (Limbic Structures)” (1901). Trans. L. M. Kraft, p. 179. London: Lloyd-Luke 1955

  22. Steward, O.: Topographic organization of the projections from the entorhinal area to the hippocampal formation of the rat. J Comp Neurol 167, 285–314 (1976)

  23. Steward, O., Scoville, S.A.: Cells of origin of entorhinal cortical afferents to the hippocampus and fascia dentata of the rat. J Comp Neurol 169, 347–370 (1976)

  24. Steward, O., White, W.F., Cotman, C.W.: Potentiation of the excitatory synaptic action of commissural, associational and entorhinal afferents to dentate granule cells. Brain Res 134, 551–560 (1977)

  25. Steward, O., White, W.F., Cotman, C.W., Lynch, G.: Potentiation of excitatory synaptic transmission in the normal and in the reinnervated dentate gyrus of the rat. Exp Brain Res 26, 423–441 (1976)

  26. Van Hoesen, G.W., Pandya, D.N.: Some connections of the entorhinal (area 38) and perirhinal (area 35) cortices of the rhesus monkey. I. Temporal lobe afferents. Brain Res 95, 1–24 (1975)

  27. Van Hoesen, G.W., Pandya, D.N., Butters, N.: Some connections of the entorhinal (area 38) and perirhinal (area 35) cortices of the rhesus monkey. II. Frontal lobe afferents. Brain Res 95, 24–38 (1975)

  28. White, L.E.: Olfactory bulb projections of the rat. Anat Rec 152, 465–480 (1965)

Download references

Author information

Correspondence to O. Steward.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Wilson, R.C., Steward, O. Polysynaptic activation of the dentate gyrus of the hippocampal formation: An olfactory input via the lateral entorhinal cortex. Exp. Brain Res. 33, 523–534 (1978). https://doi.org/10.1007/BF00235572

Download citation

Key words

  • Lateral olfactory tract
  • Evoked potentials
  • Dentate gyrus
  • Lateral entorhinal cortex