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Mossy fibres form synapses with identified pyramidal basket cells in the CA3 region of the guinea-pig hippocampus: a combined Golgi-electron microscope study

  • Published:
Journal of Neurocytology

Summary

Mossy fibres, i.e. the axons of dentate granule cells, terminate with characteristic giant boutons on large spines or excrescences of the pyramidal cells in regio inferior of the hippocampus. In addition to pyramidal cells there are several types of non-pyramidal neuron which extend their dendrites into the termination zone of mossy fibres. By using the combined Golgi-electron microscope technique mossy fibre terminals were found, which established asymmetric synaptic contacts with both spines of pyramidal cells and smooth dendrites of identified (Golgi-stained) pyramidal basket cells in the CA3 region of the guinea-pig hippocampus. The observed synaptic connection with pyramidal basket cells suggests an involvement of the mossy fibre system in feed-forward inhibition of the hippocampal pyramidal neurons.

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References

  • Alger, B. E. &Nicoll, R. A. (1982) Feed-forward dendritic inhibition in rat hippocampal pyramidal cells studied in vitro.Journal of Physiology 328, 105–23.

    PubMed  Google Scholar 

  • Amaral, D. G. (1978) A Golgi study of cell types in the hilar region of the hippocampus in the rat.Journal of Comparative Neurology 182, 851–914.

    PubMed  Google Scholar 

  • Amaral, D. G. (1979) Synaptic extensions from the mossy fibers of the fascia dentata.Anatomy and Embryology 155, 241–51.

    PubMed  Google Scholar 

  • Amaral, D. G. &Dent, J. A. (1981) Development of the mossy fibers of the dentate gyrus. I. A light and electron microscopic study of the mossy fibers and their expansions.Journal of Comparative Neurology 195, 51–86.

    PubMed  Google Scholar 

  • Andersen, P. (1975) Organization of hippocampal neurons and their interconnections. InThe Hippocampus (edited byIsaacson, R. L. &Pribram, K. H.), pp. 159–64. New York: Plenum Press.

    Google Scholar 

  • Andersen, P. (1979) Factors influencing functional connectivity during hippocampal development.Progress in Brain Research 51, 139–47.

    PubMed  Google Scholar 

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

    Google Scholar 

  • Andersen, P., Eccles, J. C. &Løyning, Y. (1964a) Location of postsynaptic inhibitory synapses of hippocampal pyramids.Journal of Neurophysiology 27, 592–607.

    Google Scholar 

  • Andersen, P., Eccles, J. C. &Løyning, Y. (1964b) Pathway of postsynaptic inhibition in the hippocampus.Journal of Neurophysiology 27, 608–19.

    PubMed  Google Scholar 

  • Blackstad, T. W. &Kjaerheim, A. (1961) Special axo-dendritic synapses in the hippocampal cortex: electron and light microscopic studies on the layer of mossy fibers.Journal of Comparative Neurology 117, 113–59.

    Google Scholar 

  • Buzsáki, G. &Eidelberg, E. (1981) Commissural projection to the dentate gyrus of the rat — evidence for feed-forward inhibition.Brain Research 230, 346–50.

    PubMed  Google Scholar 

  • Buzsákl, G. &Eidelberg, E. (1982) Direct afferent excitation and long-term potentiation of hippocampal interneurons.Journal of Neurophysiology 48, 597–607.

    PubMed  Google Scholar 

  • Cajal, S. R. Y. (1911)Histologie du Système Nerveux de l'Homme et des Vertébrés. Tome II. Paris: Maloine.

    Google Scholar 

  • Douglas, R. M., McNaughton, B. L. &Goddard, G. V. (1983) Commissural inhibition and facilitation of granule cell discharge in fascia dentata.Journal of Comparative Neurology 219, 285–94.

    PubMed  Google Scholar 

  • Fairén, A., Peters, A. &Saldanha, J. (1977) A new procedure for examining Golgi impregnated neurons by light and electron microscopy.Journal of Neurocytology 6, 311–37.

    PubMed  Google Scholar 

  • Frotscher, M., Hámori, J. &Wenzel, J. (1977) Transneuronal effects of entorhinal lesions in the early postnatal period on synaptogenesis in the hippocampus of the rat.Experimental Brain Research 30, 549–60.

    Google Scholar 

  • Frotscher, M., Léránth, Cs., Lübbers, K. &Oertel, W. H. (1984) Commissural afferents innervate glutamate decarboxylase immunoreactive non-pyramidal neurons in the guinea pig hippocampus.Neuroscience Letters 46, 137–43.

    PubMed  Google Scholar 

  • Frotscher, M., Misgeld, U. &Nitsch, C. (1981a) Ultrastructure of mossy fiber endings in in vitro hippocampal slices.Experimental Brain Research 41, 247–55.

    Google Scholar 

  • Frotscher, M., Rinne, U., Hassler, R. &Wagner, A. (1981b) Termination of cortical afferents on identified neurons in the caudate nucleus of the cat: A combined Golgi/EM degeneration study.Experimental Brain Research 41, 329–37.

    Google Scholar 

  • Frotscher, M. &Zimmer, J. (1983a) Lesion-induced mossy fibers to the molecular layer of the rat fascia dentata: identification of postsynaptic granule cells by the Golgi/EM technique.Journal of Comparative Neurology 215, 299–311.

    PubMed  Google Scholar 

  • Frotscher, M. &Zimmer, J. (1983b) Commissural fibers terminate on non-pyramidal neurons in the guinea pig hippocampus — a combined Golgi/EM degeneration study.Brain Research 265, 289–93.

    PubMed  Google Scholar 

  • Golgi, C. (1886)Sulla Fina Anatomia degli Organi Centrali del Sistema Nervoso. Milano: U. Hoepli.

    Google Scholar 

  • Hamlyn, L. H. (1962) The fine structure of the mossy fiber endings in the hippocampus of the rabbit.Journal of Anatomy 97, 112–20.

    Google Scholar 

  • Ibata, Y. (1968) Electron microscopy of the hippocampal formation of the rabbit.Journal für Hirnforschung 10, 451–69.

    Google Scholar 

  • Köhler, C. (1982) Distribution and morphology of vasoactive intestinal polypeptide-like immunoreactive neurons in regio superior of the rat hippocampal formation.Neuroscience Letters 33, 265–70.

    PubMed  Google Scholar 

  • Laatsch, R. H. &Cowan, W. M. (1966) Electron microscopic studies of the dentate gyrus. I. Normal structure.Journal of Comparative Neurology 128, 359–96.

    PubMed  Google Scholar 

  • Laurberg, S. &Zimmer, J. (1981) Lesion-induced sprouting of hippocampal mossy fiber collaterals to the fascia dentata in developing and adult rats.Journal of Comparative Neurology 200, 433–59.

    PubMed  Google Scholar 

  • Léránth, Cs. &Frotscher, M. (1983) Commissural afferents to the rat hippocampus terminate on vasoactive intestinal polypeptide-like immunoreactive non-pyramidal neurons.Brain Research 276, 357–61.

    PubMed  Google Scholar 

  • Léránth, Cs., Frotscher, M., Tömböl, T. &Palkovits, M. (1984) Ultrastructure and synaptic connections of vasoactive intestinal polypeptide-like immunoreactive non-pyramidal neurons and axon terminals in the rat hippocampus.Neuroscience 12, 531–42.

    PubMed  Google Scholar 

  • Lorén, I., Emson, P. C., Fahrenkrug, J., Björklund, A., Alumets, J., Hakanson, R. &Sundler, F. (1979) Distribution of vasoactive intestinal polypeptide in the rat and mouse brain.Neuroscience 4, 1953–76.

    PubMed  Google Scholar 

  • Lorente De Nó, R. (1934) Studies on the structure of the cerebral cortex. II. Continuation of the study of the Ammonic system.Journal für Psychologie und Neurologie 46, 113–77.

    Google Scholar 

  • McNaughton, B. L., Douglas, R. M. &Goddard, G. V. (1978) Synaptic enhancement in fascia dentata. Cooperativity among coactive afferents.Brain Research 157, 277–93.

    PubMed  Google Scholar 

  • Misgeld, U. &Klee, M. R. (1984) Long-term potentiation and inhibition in CA3 neurons.Experimental Brain Research Suppl.9, 325–39.

    Google Scholar 

  • Misgeld, U., Klee, M. R., Sarvey, J. M. &Zeise, M. L. (1981) Role of inhibition in heterosynaptic postactivation potentiation of CA3 neurons in vitro. InCellular Analogues and Neural Plasticity (edited byFehér, O. andJoó, F.), pp. 155–64. Budapest: Akadémiai Kiadó.

    Google Scholar 

  • Ribak, C. E. &Anderson, L. (1980) Ultrastructure of the pyramidal basket cells in the dentate gyrus of the rat.Journal of Comparative Neurology 192, 903–16.

    Google Scholar 

  • Ribak, C. E. &Seress, L. (1983) Five types of basket cell in the hippocampal dentate gyrus: a combined Golgi and electron microscopic study.Journal of Neurocytology 12, 577–97.

    PubMed  Google Scholar 

  • Ribak, C. E., Vaughn, J. E. &Barber, R. P. (1981) Immunocytochemical localization of GABAergic neurons at the electron microscopical level.Histochemical Journal 13, 555–82.

    PubMed  Google Scholar 

  • Ribak, C. E., Vaughn, J. E. &Saito, K. (1978) Immunocytochemical localization of glutamic acid decarboxylase in neuronal somata following colchicine inhibition of axonal transport.Brain Research 140, 315–32.

    PubMed  Google Scholar 

  • Seress, L. &Ribak, C. E. (1984) Direct commissural connections to the basket cells of the hippocampal dentate gyrus: anatomical evidence for feed-forward inhibition.Journal of Neurocytology 13, 215–25.

    Google Scholar 

  • Sims, K. B., Hoffmann, D. L., Said, S. I. &Zimmermann, E. A. (1980) Vasoactive intestinal polypeptide (VIP) in mouse and rat brain: an immunocytochemical study.Brain Research 186, 165–83.

    PubMed  Google Scholar 

  • Somogyi, P., Smith, A. D., Nunzi, M. G., Gorio, A., Takagi, H. &Wu, J. Y. (1983) Glutamate decarboxylase immunoreactivity in the hippocampus of the cat: distribution of immunoreactive synaptic terminals with specific reference to the axon initial segment of pyramidal neurons.Journal of Neuroscience 3, 1450–68.

    PubMed  Google Scholar 

  • Spencer, W. A. &Kandel, E. R. (1961) Hippocampal neuron responses to selective activation of recurrent collaterals of hippocampofugal axons.Experimental Neurology 4, 149–61.

    Google Scholar 

  • Storm-Mathisen, J., Leknes, A. K., Bore, A. T., Vaaland, J. L., Edminson, P., Haug, F. M. S. &Ottersen, O. P. (1983) First visualization of glutamate and GABA in neurones by immunocytochemistry.Nature 301, 517–20.

    PubMed  Google Scholar 

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  1. Institute of Anatomy, Johann Wolfgang Goethe University, Theodor-Stern-Kai 7, D-6000, Frankfurt/Main 70, FRG

    Michael Frotscher

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  1. Michael Frotscher
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Frotscher, M. Mossy fibres form synapses with identified pyramidal basket cells in the CA3 region of the guinea-pig hippocampus: a combined Golgi-electron microscope study. J Neurocytol 14, 245–259 (1985). https://doi.org/10.1007/BF01258450

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  • DOI: https://doi.org/10.1007/BF01258450

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