Skip to main content
Log in

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

  • Review Article
  • Published:
Anatomy and Embryology Aims and scope Submit manuscript

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.

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • 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 31:209–214

    Google Scholar 

  • Amaral DG (1978) A Golgi study of cell types in the hilar region of the hippocampus in the rat. J Comp Neurol 182:851–914

    Google Scholar 

  • Amaral DG (1979) Synaptic extensions from the mossy fibers of the fascia dentata. Anat Embryol 155:241–251

    Google Scholar 

  • Amaral DG, Cowan WM (1980) Subcortical efferents to the hippocampal formation in the monkey. J Comp Neurol 189:573–591

    Google Scholar 

  • 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 195:51–86

    Google Scholar 

  • andersen P, Bliss TVP, Skrede KK (1971) Lamellar organisation of hippocampal excitatory pathways. Exp Brain Res 13:222–238

    Google Scholar 

  • 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 215:329–336

    Google Scholar 

  • Blackstad TW (1956) Commissural connections of the hippocampal region in the rat, with special reference to their mode of termination. J Comp Neurol 105:417–537

    Google Scholar 

  • Blackstad TW (1963) Ultrastructural studies on the hippocampal region. Progr Brain Res 3:122–148

    Google Scholar 

  • Blackstad TW (1965) Mapping of experimental axon degeneration by electron microscopy of Golgi preparations. Z Zellforsch 67:819–834

    Google Scholar 

  • Blackstad TW (1967) Cortical grey matter. A correlation of light and electron microscopic data. In: Hyden H (ed) The neuron, Elsevier, Amsterdam

    Google Scholar 

  • 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 117:113–159

    Google Scholar 

  • 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 138:433–450

    Google Scholar 

  • Cajal SR y (1911) Histologie du Système Nerveux de l'Homme, et des Vertébrés, vol II. A Maloine, Paris

    Google Scholar 

  • Chronister RB, DeFrance J (1979) Organization of projection neurons of the hippocampus. Exp Neurol 66:509–523

    Google Scholar 

  • 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 258:1–10

    Google Scholar 

  • Fairén A, Peters A, Saldanha J (1977) A new procedure for examining Golgi impregnated neurons by light and electron microscopy. J Neurocytol 6:311–337

    Google Scholar 

  • Fibiger HC (1982) The organization and some projections of cholinergic neurons of the mammalian forebrain. Brain Res Rev 4:327–388

    Google Scholar 

  • Frotscher M (1983) Dendritic plasticity in response to deafferentation. In: Seifert W (ed) Neurobiology of the hippocampus. Academic Press, London

    Google Scholar 

  • 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 14:245–259

    Google Scholar 

  • 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 239:237–246

    Google Scholar 

  • 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 243:58–70

    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. J Comp Neurol 215:299–311

    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 Res 265:289–293

    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. Exp Brain Res 30:549–560

    Google Scholar 

  • 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 41:329–337

    Google Scholar 

  • 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 46:137–143

    Google Scholar 

  • 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 178:73–88

    Google Scholar 

  • Golgi C (1884) Sulla fina anatomia degli organi centrali del sistema nervoso. Hoepli U, Milano

    Google Scholar 

  • Groenewegen HJ, Steinbusch HWM (1984) Serotonergic and nonserotonergic projections from the interpeduncular nucleus to the ventral hippocampus in the rat. Neurosci Lett 51:19–24

    Google Scholar 

  • Hamlyn LH (1962) The fine structure of the mossy fiber endings in the hippocampus of the rabbit. J Anat 96:112–120

    Google Scholar 

  • 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:S507

    Google Scholar 

  • Ibata Y (1968) Electron microscopy of the hippocampal formation of the rabbit. J Hirnforsch 10:451–469

    Google Scholar 

  • 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 7:951–975

    Google Scholar 

  • Koelliker A von (1896) Handbuch der Gewebelehre des Menschen. 2. Bd.: Nervensystem des Menschen und der Thiere, 6. Aufl. Engelmann, Leipzig

    Google Scholar 

  • Kosaka T, Hama K, Wu J-Y (1984) GABAergic synaptic boutons in the granule cell layer of rat dentate gyrus. Brain Res 293:353–359

    Google Scholar 

  • 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 128:359–396

    Google Scholar 

  • Laurberg S (1979) Commissural and intrinsic connections of the rat hippocampus. J Comp Neurol 184:685–708

    Google Scholar 

  • 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 276:357–361

    Google Scholar 

  • 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 254:51–64

    Google Scholar 

  • Leranth C, Frotscher M (1987) Cholinergic innervations of hippocampal GAD- and somatostatin-immunoreactive commissural neurons. J Comp Neurol 261:33–47

    Google Scholar 

  • 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 90:521–540

    Google Scholar 

  • Lindsay RD, Scheibel AB (1981) Quantitative analysis of the dendritic branching pattern of granule cells from adult rat dentate gyrus. Exp Neurol 73:286–297

    Google Scholar 

  • 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 46:113–177

    Google Scholar 

  • 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 62:317–322

    Google Scholar 

  • Lugaro E (1983) Contributo alla fina anatomia del grande piede del hippocampo. Arch Sci Med 18:113–142

    Google Scholar 

  • 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 115:1–21

    Google Scholar 

  • McGeer PL, McGeer EG, Peng JH (1984) Choline acetyltransferase: Purification and immunohistochemical localization. Life Sci 34:2319–2338

    Google Scholar 

  • 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 10:1185–1201

    Google Scholar 

  • Misgeld U, Frotscher M (1986) Postsynaptic-GABAergic inhibition of non-pyramidal neurons in the guinea-pig hippocampus. Neuroscience 19:193–206

    Google Scholar 

  • Nauta WJH (1950) Über die sogenannte Degeneration im Zentralnervensystem und ihre Darstellung durch Silberimprägnation. Arch Neurol Psychiatr 66:353–376

    Google Scholar 

  • 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 6:2715–2735

    Google Scholar 

  • Peters A, Palay SL, Webster H (1970) The fine structure of the nervous system. Harper and Row, New York

    Google Scholar 

  • Ribak CE, Anderson L (1980) Ultrastructure of the pyramidal basket cells in the dentate gyrus of the rat. J Comp Neurol 192:903–916

    Google Scholar 

  • Ribak CE, Seress L (1983) Five types of basket cell in the hippocampal dentate gyrus: a combined Golgi and electron microscopic study. J Neurocytol 12:577–597

    Google Scholar 

  • Ribak CE, Vaughn JE, Saito K (1978) Immunocytochemical localization of glutamic acid decarboxylase in neuronal somata following colchicine inhibition of axonal transport. Brain Res 140:315–332

    Google Scholar 

  • Ribak CE, Seress L, Amaral DG (1985a) The development, ultrastructure and synaptic connections of the mossy cells of the dentate gyrus. J Neurocytol 14:835–857

    Google Scholar 

  • Ribak CE, Seress L, Seroogy KB, Peterson GM, Oertel WH (1985b) The hippocampal commissural pathway contains a GABAergic inhibitory component. Anat Rec 211:160A

    Google Scholar 

  • Sala L (1891) Zur feineren Anatomie des großen Seepferdefußes. Z Wiss Zool 52:18–45

    Google Scholar 

  • Schaffer K (1892) Beitrag zur Histologie der Ammonshornformation. Arch Mikrosk Anat 39:611–632

    Google Scholar 

  • Schmechel DE, Vickrey BG, Fitzpatrick D, Elde RP (1984) GABAergic neurons of mammalian cerebral cortex: widespread subclass defined by somatostatin content. Neurosci Lett 17:227–232

    Google Scholar 

  • Segal M (1979) A potent inhibitory monosynaptic hypothalamo-hippocampal connection. Brain Res 162:137–141

    Google Scholar 

  • Segal M, Landis S (1974) Afferents to the hippocampus studied with the method of retrograde transport of horseradish-peroxidase. Exp Neurol 78:1–15

    Google Scholar 

  • 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) 181–195

    Google Scholar 

  • Seress L, Ribak CE (1983) GABA-ergic cells in the dentate gyrus appear to be local circuit and projection neurons. Exp Brain Res 50:173–182

    Google Scholar 

  • 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 13:215–225

    Google Scholar 

  • 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 56:21–26

    Google Scholar 

  • Steinbusch H (1981) Distribution of serotonin immunoreactivity in the central nervous system of the rat — cell bodies and terminals. Neuroscience 6:557–618

    Google Scholar 

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

    Google Scholar 

  • Storm-Mathisen J, Ottersen OP (1984) Neurotransmitters in the hippocampal formation. In: Reinoso-Suarez F, Ajmone-Marsan C (eds) Cortical integration, Raven Press, New York

    Google Scholar 

  • Swanson LW, Wyss JM, Cowan WM (1978) An autoradiographic study of the organization of intrahippocampal association pathways in the rat. J Comp Neurol 181:681–716

    Google Scholar 

  • 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 1:548–559

    Google Scholar 

  • Voneida TJ, Vardaris RM, Fish SE, Reinheld CT (1981) The origin of the hippocampal commissure in the rat. Anat Rec 201:91–103

    Google Scholar 

  • Wainer BH, Levey AI, Mufson EJ, Mesulam M-M (1984) Cholinergic systems in mammalian brain identified with antibodies against choline acetyltransferase. Neurochem Int 6:163–182

    Google Scholar 

  • 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 160:203–215

    Google Scholar 

  • 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 156:165–176

    Google Scholar 

  • Wyss JM, Swanson LW, Cowan WM (1979b) A study of subcortical afferents to the hippocampal formation in the rat. Neuroscience 4:463–476

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Lübbers, K., Frotscher, M. Fine structure and synaptic connections of identified neurons in the rat fascia dentata. Anat Embryol 177, 1–14 (1987). https://doi.org/10.1007/BF00325285

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00325285

Key words

Navigation