Anatomy and Embryology

, Volume 177, Issue 1, pp 1–14 | Cite as

Fine structure and synaptic connections of identified neurons in the rat fascia dentata

  • Klaus Lübbers
  • Michael Frotscher
Review Article

Summary

A survey is given of the synaptic connections of identified neurons in the rat fascia dentata based on our own Golgi/electron microscopic and light and electron microscopic immunocytochemical findings as well as on results obtained from the literature. The report largely deals with the dominating cell type in the region, the dentate granule cell. Of the various types of hilar cells, the GA-BAergic neurons, particularly the inhibitory basket cells, are taken into account. Differences in fine structure between granule cells and basket cells as well as mutual synaptic connections between these two types of dentate neurons are elaborated. This survey may provide a basis for further neurophysiological and pharmacological studies on these cells.

Key words

Fascia dentata Granule cell Basket cell Golgi/electron microscopy Glutamate decarboxylase immunocytochemistry 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Alonso A, Köhler C (1982) Evidence for separate projections of hippocampal pyramidal and non-pyramidal neurons to different parts of the septum in the rat brain. Neurosci Lett 31:209–214Google Scholar
  2. Amaral DG (1978) A Golgi study of cell types in the hilar region of the hippocampus in the rat. J Comp Neurol 182:851–914Google Scholar
  3. Amaral DG (1979) Synaptic extensions from the mossy fibers of the fascia dentata. Anat Embryol 155:241–251Google Scholar
  4. Amaral DG, Cowan WM (1980) Subcortical efferents to the hippocampal formation in the monkey. J Comp Neurol 189:573–591Google Scholar
  5. Amaral DG, Dent JA (1981) Development of the mossy fibers of the dentate gyrus: I. A light and electron microscopic study of the mossy fibers and their expansions. J Comp Neurol 195:51–86Google Scholar
  6. andersen P, Bliss TVP, Skrede KK (1971) Lamellar organisation of hippocampal excitatory pathways. Exp Brain Res 13:222–238Google Scholar
  7. Berger TW, Semple-Rowland S, Bassett JL (1981) Hippocampal polymorph neurons are the cells of origin for ipsilateral association and commissural afferents to the dentate gyrus. Brain Res 215:329–336Google Scholar
  8. Blackstad TW (1956) Commissural connections of the hippocampal region in the rat, with special reference to their mode of termination. J Comp Neurol 105:417–537Google Scholar
  9. Blackstad TW (1963) Ultrastructural studies on the hippocampal region. Progr Brain Res 3:122–148Google Scholar
  10. Blackstad TW (1965) Mapping of experimental axon degeneration by electron microscopy of Golgi preparations. Z Zellforsch 67:819–834Google Scholar
  11. Blackstad TW (1967) Cortical grey matter. A correlation of light and electron microscopic data. In: Hyden H (ed) The neuron, Elsevier, AmsterdamGoogle Scholar
  12. Blackstad TW, Kjaerheim A (1961) Special axo-dendritic synapses in the hippocampal cortex: electron and light microscopic studies on the layer of mossy fibers. J Comp Neurol 117:113–159Google Scholar
  13. Blackstad TW, Brink K, Hem J, Jeune B (1970) Distribution of the hippocampal mossy fibers in the rat. An experimental study with silver impregnation methods. J Comp Neurol 138:433–450Google Scholar
  14. Cajal SR y (1911) Histologie du Système Nerveux de l'Homme, et des Vertébrés, vol II. A Maloine, ParisGoogle Scholar
  15. Chronister RB, DeFrance J (1979) Organization of projection neurons of the hippocampus. Exp Neurol 66:509–523Google Scholar
  16. Dent JA, Galvin NJ, Standield BB, Cowan WM (1983) The mode of termination of the hypothalamic projection to the dentate gyrus — an EM autoradiographic study. Brain Res 258:1–10Google Scholar
  17. Fairén A, Peters A, Saldanha J (1977) A new procedure for examining Golgi impregnated neurons by light and electron microscopy. J Neurocytol 6:311–337Google Scholar
  18. Fibiger HC (1982) The organization and some projections of cholinergic neurons of the mammalian forebrain. Brain Res Rev 4:327–388Google Scholar
  19. Frotscher M (1983) Dendritic plasticity in response to deafferentation. In: Seifert W (ed) Neurobiology of the hippocampus. Academic Press, LondonGoogle Scholar
  20. Frotscher M (1985) 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 14:245–259Google Scholar
  21. Frotscher M, Leranth C (1985) Cholinergic innervation of the rat hippocampus as revealed by choline acetyltransferase immunocytochemistry: a combined light and electron microscopic study. J Comp Neurol 239:237–246Google Scholar
  22. Frotscher M, Leranth C (1986) The cholinergic innervation of the rat fascia dentata: identification of target structures on granule cells by combining choline acetyltransferase immunocytochemistry and Golgi impregnation. J Comp Neurol 243:58–70Google Scholar
  23. 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. J Comp Neurol 215:299–311Google Scholar
  24. Frotscher M, Zimmer J (1983b) Commissural fibers terminate on non-pyramidal neurons in the guinea pig hippocampus — a combined Golgi/EM degeneration study. Brain Res 265:289–293Google Scholar
  25. 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. Exp Brain Res 30:549–560Google Scholar
  26. Frotscher M, Rinne U, Hassler R, Wagner A (1981) Termination of cortical afferents on identified neurons in the caudate nucleus of the cat: A combined Golgi/EM degeneration study. Exp Brain Res 41:329–337Google Scholar
  27. Frotscher M, Leranth Cs, Lübbers K, Oertel WH (1984) Commissural afferents innervate glutamate decarboxylase immunoreactive non-pyramidal neurons in the guinea pig hippocampus. Neurosci Lett 46:137–143Google Scholar
  28. Gaarskjaer FB (1978) Organization of the mossy fiber system of the rat studied in extended hippocampi. II. Experimental analysis of fiber distribution with silver impregnation methods. J Comp Neurol 178:73–88Google Scholar
  29. Golgi C (1884) Sulla fina anatomia degli organi centrali del sistema nervoso. Hoepli U, MilanoGoogle Scholar
  30. Groenewegen HJ, Steinbusch HWM (1984) Serotonergic and nonserotonergic projections from the interpeduncular nucleus to the ventral hippocampus in the rat. Neurosci Lett 51:19–24Google Scholar
  31. Hamlyn LH (1962) The fine structure of the mossy fiber endings in the hippocampus of the rabbit. J Anat 96:112–120Google Scholar
  32. Hayes L, Totterdell S (1985) A light and electron microscopic study of nonpyramidal hippocampal cells that project ot the medial nucleus accumbens. Neurosci Lett Suppl 22:S507Google Scholar
  33. Ibata Y (1968) Electron microscopy of the hippocampal formation of the rabbit. J Hirnforsch 10:451–469Google Scholar
  34. Köhler C, Steinbusch H (1982) Identification of serotonin containing neurons of the midbrain raphe projecting to the entorhinal area and the hippocampal formation: a combined immunohistochemical and fluorescent retrograde tracing study in the rat brain. Neuroscience 7:951–975Google Scholar
  35. Koelliker A von (1896) Handbuch der Gewebelehre des Menschen. 2. Bd.: Nervensystem des Menschen und der Thiere, 6. Aufl. Engelmann, LeipzigGoogle Scholar
  36. Kosaka T, Hama K, Wu J-Y (1984) GABAergic synaptic boutons in the granule cell layer of rat dentate gyrus. Brain Res 293:353–359Google Scholar
  37. Laatsch RH, Cowan WM (1966) Electron microscopic studies of the dentate gyrus of the rat. I. Normal structure with special reference to synaptic organization. J Comp Neurol 128:359–396Google Scholar
  38. Laurberg S (1979) Commissural and intrinsic connections of the rat hippocampus. J Comp Neurol 184:685–708Google Scholar
  39. Leranth Cs, Frotscher M (1983) Commissural afferents to the rat hippocampus terminate on vasoactive intestinal polypeptide-like immunoreactive non-pyramidal neurons. An EM immunocytochemical degeneration study. Brain Res 276:357–361Google Scholar
  40. Leranth C, Frotscher M (1986) Synaptic connections of cholecystokinin-immunoreactive neurons and terminals in the rat fascia dentata: a combined light and electron microscopic study. J Comp Neurol 254:51–64Google Scholar
  41. Leranth C, Frotscher M (1987) Cholinergic innervations of hippocampal GAD- and somatostatin-immunoreactive commissural neurons. J Comp Neurol 261:33–47Google Scholar
  42. Lewis PR, Shute CCD (1967) The cholinergic limbic system: Projections to hippocampal formation, medial cortex, nuclei of the ascending cholinergic reticular system and the subfornical organ and supraoptic crest. Brain 90:521–540Google Scholar
  43. Lindsay RD, Scheibel AB (1981) Quantitative analysis of the dendritic branching pattern of granule cells from adult rat dentate gyrus. Exp Neurol 73:286–297Google Scholar
  44. Lorente de Nó R (1934) Studies on the structure of the cerebral cortex. II. Continuation of the study of the ammonic system. J Psychol Neurol 46:113–177Google Scholar
  45. Lübbers K, Wolff JR, Frotscher M (1985) Neurogenesis of GA-BAergic neurons in the rat dentate gyrus: a combined autoradiographic and immunocytochemical study. Neurosci Lett 62:317–322Google Scholar
  46. Lugaro E (1983) Contributo alla fina anatomia del grande piede del hippocampo. Arch Sci Med 18:113–142Google Scholar
  47. Matthews DA, Cotman C, Lynch G (1976) An electron microscopic study of lesion-induced synaptogenesis in the dentate gyrus of the adult rat. I. Magnitude and time course of degeneration. Brain Res 115:1–21Google Scholar
  48. McGeer PL, McGeer EG, Peng JH (1984) Choline acetyltransferase: Purification and immunohistochemical localization. Life Sci 34:2319–2338Google Scholar
  49. Mesulam M-M, Mufson EJ, Wainer BH, Levey AI (1983) Central cholinergic pathways in the rat: An overview based on an alternative nomenclature (Ch1-Ch6). Neuroscience 10:1185–1201Google Scholar
  50. Misgeld U, Frotscher M (1986) Postsynaptic-GABAergic inhibition of non-pyramidal neurons in the guinea-pig hippocampus. Neuroscience 19:193–206Google Scholar
  51. Nauta WJH (1950) Über die sogenannte Degeneration im Zentralnervensystem und ihre Darstellung durch Silberimprägnation. Arch Neurol Psychiatr 66:353–376Google Scholar
  52. Oertel WH, Schmechel DE, Mugnaini E, Tappaz ML, Kopin IJ (1982) Immunocytochemical localization of glutamate decarboxylase in the rat cerebellum with a new antiserum. Neuroscience 6:2715–2735Google Scholar
  53. Peters A, Palay SL, Webster H (1970) The fine structure of the nervous system. Harper and Row, New YorkGoogle Scholar
  54. Ribak CE, Anderson L (1980) Ultrastructure of the pyramidal basket cells in the dentate gyrus of the rat. J Comp Neurol 192:903–916Google Scholar
  55. Ribak CE, Seress L (1983) Five types of basket cell in the hippocampal dentate gyrus: a combined Golgi and electron microscopic study. J Neurocytol 12:577–597Google Scholar
  56. Ribak CE, Vaughn JE, Saito K (1978) Immunocytochemical localization of glutamic acid decarboxylase in neuronal somata following colchicine inhibition of axonal transport. Brain Res 140:315–332Google Scholar
  57. Ribak CE, Seress L, Amaral DG (1985a) The development, ultrastructure and synaptic connections of the mossy cells of the dentate gyrus. J Neurocytol 14:835–857Google Scholar
  58. Ribak CE, Seress L, Seroogy KB, Peterson GM, Oertel WH (1985b) The hippocampal commissural pathway contains a GABAergic inhibitory component. Anat Rec 211:160AGoogle Scholar
  59. Sala L (1891) Zur feineren Anatomie des großen Seepferdefußes. Z Wiss Zool 52:18–45Google Scholar
  60. Schaffer K (1892) Beitrag zur Histologie der Ammonshornformation. Arch Mikrosk Anat 39:611–632Google Scholar
  61. Schmechel DE, Vickrey BG, Fitzpatrick D, Elde RP (1984) GABAergic neurons of mammalian cerebral cortex: widespread subclass defined by somatostatin content. Neurosci Lett 17:227–232Google Scholar
  62. Segal M (1979) A potent inhibitory monosynaptic hypothalamo-hippocampal connection. Brain Res 162:137–141Google Scholar
  63. Segal M, Landis S (1974) Afferents to the hippocampus studied with the method of retrograde transport of horseradish-peroxidase. Exp Neurol 78:1–15Google Scholar
  64. Seress L, Pokorny J (1981) Structure of the granular layer of the rat dentate gyrus. A light microscopic and Golgi study. J Anat 133 (1981) 181–195Google Scholar
  65. Seress L, Ribak CE (1983) GABA-ergic cells in the dentate gyrus appear to be local circuit and projection neurons. Exp Brain Res 50:173–182Google Scholar
  66. Seress L, Ribak CE (1984) Direct commissural connections to the basket cells of the hippocampal dentate gyrus: anatomical evidence for feed-forward inhibition. J Neurocytol 13:215–225Google Scholar
  67. Seress L, Ribak CE (1985) A substantial number of asymmetric axosomatic synapses is a characteristic of the granule cells of the hippocampal dentate gyrus. Neurosci Lett 56:21–26Google Scholar
  68. Steinbusch H (1981) Distribution of serotonin immunoreactivity in the central nervous system of the rat — cell bodies and terminals. Neuroscience 6:557–618Google Scholar
  69. Steward O, Scoville SA (1976) Cells of origin of entorhinal cortical afferents to the hippocampus and fascia dentata of the rat. J Comp Neurol 169:347–370Google Scholar
  70. Storm-Mathisen J, Ottersen OP (1984) Neurotransmitters in the hippocampal formation. In: Reinoso-Suarez F, Ajmone-Marsan C (eds) Cortical integration, Raven Press, New YorkGoogle Scholar
  71. Swanson LW, Wyss JM, Cowan WM (1978) An autoradiographic study of the organization of intrahippocampal association pathways in the rat. J Comp Neurol 181:681–716Google Scholar
  72. Swanson LW, Sawchenko PE, Cowan WM (1981) Evidence for collateral projections by neurons in ammons horn, the dentate gyrus, and the subiculum — a multiple retrograde labeling study in the rat. J Neurosci 1:548–559Google Scholar
  73. Voneida TJ, Vardaris RM, Fish SE, Reinheld CT (1981) The origin of the hippocampal commissure in the rat. Anat Rec 201:91–103Google Scholar
  74. Wainer BH, Levey AI, Mufson EJ, Mesulam M-M (1984) Cholinergic systems in mammalian brain identified with antibodies against choline acetyltransferase. Neurochem Int 6:163–182Google Scholar
  75. West JR, Nornes HO, Barnes CL, Bronfenbrenner M (1979) The cells of origin of the commissural afferents to the area dentata in the mouse. Brain Res 160:203–215Google Scholar
  76. Wyss JM, Swanson LW, Cowan WM (1979a) Evidence for input to the molecular layer and the stratuin granulosum of the dentate gyrus from the supramammillary region of the hypothalamus. Anat Embryol 156:165–176Google Scholar
  77. Wyss JM, Swanson LW, Cowan WM (1979b) A study of subcortical afferents to the hippocampal formation in the rat. Neuroscience 4:463–476Google Scholar

Copyright information

© Springer-Verlag 1987

Authors and Affiliations

  • Klaus Lübbers
    • 1
  • Michael Frotscher
    • 1
  1. 1.Institute of AnatomyJohann Wolfgang Goethe UniversityFrankfurt/MainGermany

Personalised recommendations