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Non-pyramidal neurons in the guinea pig hippocampus

A combined Golgi-electron microscope study

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Summary

Morphological characteristics of non-pyramidal neurons in the guinea pig hippocampus (regions CA1 and CA3) were analyzed by a correlated light and electron microscopic approach. Following Golgi impregnation, the cells were first studied under the light microscope and classified according to the location of their cell bodies and the distribution of their dendrites in the different hippocampal layers. Next, the Golgi impregnated non-pyramidal neurons were gold-toned and deimpregnated, allowing an electron microscopic analysis of the identified structures.

With regard to cell body location and dendritic pattern, non-pyramidal cells are a rather heterogeneous group of neurons. Their perikarya were found in all hippocampal layers and their dendrites had a less regular orientation when compared to pyramidal neurons and granule cells. Two basic types, i.e., “vertical” and “horizontal” non-pyramidal neurons are described. Many cells were of an intermediate type with dendrites extending in all directions. Non-pyramidal cell dendrites were mostly devoid of spines but exhibited numerous varicosities. Non-pyramidal cell axons could sometimes be seen extending towards the pyramidall cell layer.

A surprising uniformity was observed when the impregnated, identified non-pyramidal neurons were studied in the electron microscope. Their perikarya exhibited a well-developed endoplasmic reticulum and indented nuclei. Both the cell bodies and the varicose dendrites were densely covered with synaptic boutons which mainly formed asymmetric synaptic contacts. Only occasionally were symmetric synaptic contacts observed. Non-pyramidal cell dendrites extending into the stratum lucidum of CA3 were found to be contacted by the giant boutons of mossy fiber axons. In addition to synaptic contacts, the dendrites of gold-toned non-pyramidal neurons formed gap junctions with neigh-boring dendrites.

The results are discussed in relation to recent immunocytochemical studies which have shown non-pyramidal neurons in the hippocampus to contain gamma-aminobutyric acid and/or various neuropeptides.

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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, Woodward DJ (1977) A hippocampal interneuron observed in the inferior region. Brain Res 124:225–236

    Google Scholar 

  • Andersen P, Eccles, JC, Løyning Y (1964a) Location of postsynaptic inhibitory synapses of hippocampal pyramids. J Neurophysiol 27:592–607

    Google Scholar 

  • Andersen P, Eccles JC, Løyning Y (1964b) Pathway of postsynaptic inhibiton in the hippocampus. J Neurophysiol 27:608–619

    Google Scholar 

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

    Google Scholar 

  • Benardo LS, Prince DA (1982) Cholinergic excitation of mammalian hippocampal pyramidal cells. Brain Res 249:315–331

    Google Scholar 

  • Blackstad TW (1963) Ultrastructural studies on the hippocampal region. In: Bargmann W, Schadé JP (eds) the rhinencephalon and related structures. Progr Brain Res 3:122–148

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

    Google Scholar 

  • Braak H (1974) On the structure of the human archicortex. I. The cornu ammonis. A Golgi and pigmentarchitectonic study. Cell Tissue Res 152:349–383

    Google Scholar 

  • Buzsáki G (1984) Feed-forward inhibition in the hippocampal formation. Prog Neurobiol 22:131–153

    Google Scholar 

  • Buzsáki G, Eidelberg E (1982) Direct afferent excitation and long-term potentiation of hippocampal interneurons. J Neurophysiol 48:597–607

    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 

  • Cole AE, Nicoll RA (1984) The pharmacology of cholinergic excitatory responses in hippocampal pyramidal cells. Brain Res 305:283–290

    Google Scholar 

  • Cotman CW, Nadler JV (1978) Reactive synaptogenesis in the hippocampus. In: Cotman CW (ed) Neuronal plasticity, Raven Press, New York, pp 227–271

    Google Scholar 

  • Dodd J, Kelly JS (1978) Is somatostatin an excitatory transmitter in the hippocampus? Nature 273:674–675

    Google Scholar 

  • Dodd J, Kelly JS (1981) The actions of cholecystokinin and related peptides on pyramidal neurones of the mammalian hippocampus. Brain Res 205:337–350

    Google Scholar 

  • Dodd J, Kelly JS, Said SI (1979) Excitation of CA1 neurones of the rat hippocampus by the octacosapeptide, vasoactive intestinal polypeptide (VIP). Br J Pharmacol 66:125P

  • Dodd J, Dingledine R, Kelly JS (1981) The excitatory action of acetylcholine on hippocampal neurons of the gunea-pig and rat maintained in vitro. Brain Res 207:109–127

    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 

  • Frotscher M (1983) Dendritic plasticity in response to partial deafferentation. In: Seifert W (ed) Neurobiology of the hippocampus, Academic Press London-New York, pp 65–80

    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, Léránth Cs (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, 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, 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, Léránth 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 

  • Gall C (1984) The distribution of cholecystokinin-like immunore-activity in the hippocampal formation of the guinea pig: localization in the mossy fibers. Brain Res 306:73–83

    Google Scholar 

  • Golgi C (1886) Sulla fina anatomia degli organi centrali del sistema nervoso. U. Hoepli, Milano

    Google Scholar 

  • Greenwood RS, Godar SE, Reaves TA, Hayward JN (1981) Cholecystokinin in hippocampal pathways. J Comp Neurol 203:335–350

    Google Scholar 

  • Handelmann GE, Meyer DK, Beinfeld MC, Oertel WH (1981) CCK-containing terminals in the hippocampus are derived from intrinsic neurons: an immunohistochemical and radioimmunological study. Brain Res 224:180–184

    Google Scholar 

  • Harris KM, Marshall PE, Landis DMD (1985) Ultrastructural study of cholecystokinin-immunoreactive cells and processes in area CA1 of the rat hippocampus. J Comp Neurol 233:147–158

    Google Scholar 

  • Hayes L, Totterdell S (1985) A light and electron microscopic study of non-pyramidal hippocampal cells that project to the medial nucleus accumbens. Neurosci Lett Suppl 22:S507

  • Köhler C (1982) Distribution and morphology of vasoactive intestinal polypeptide-like immunoreactive neurons in regio superior of the rat hippocampal formation. Neurosci Lett 33:265–270

    Google Scholar 

  • Köhler C, Chan-Palay V (1982) Somatostatin-like immunoreactive neurons in the hippocampus: an immunocytochemical study in the rat. Neurosci Lett 34:259–264

    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 (1985) Gap junctions between non-pyramidal cell dendrites in the rat hippocampus (CA1 and CA3 regions): a combined Golgi/electron microscopy study. J Comp Neurol 231:150–161

    Google Scholar 

  • Kosaka T, Kosaka K, Tateishi K, Hamaoka Y, Yanaihara N, Wu JY, Hama K (1985) GABAergic neurons containing CCK-8-like and/or VIP-like immunoreactivities in the rat hippocampus and dentate gyrus. J Comp Neurol 239:420–430

    Google Scholar 

  • Léránth Cs, Frotscher M (1983) Comissural afferents to the rat hippocampus terminate on vasoactive intestinal polypeptide-like immunoreactive non-pyramidal neurons. Brain Res 276:357–361

    Google Scholar 

  • Léránth Cs, Frotscher M, Tömböl T, Palkovits M (1984) Ultrastructure and synaptic connections of vasoactive intestinal polypeptide-like immunoreactive non-pyramial neurons and axon terminals in the rat hippocampus. Neuroscience 12:531–542

    Google Scholar 

  • Lorén I, Emson PC, Fabrenkrug J, Björklund A, Alumets J, Hakanson R, Sundler F (1979) Distribution of vasoactive intestinal polypeptide in the rat and mouse brain. Neuroscience 4:1953–1976

    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 

  • Lugaro E (1893) Contributo alla fina anatomia del grande piede del hippocampo. Arch Sci Med 18:113–142

    Google Scholar 

  • Misgeld U, Frotscher M (1985) Postsynaptic GABAergic inhibition of identified non-pyramidal neurons in the guinea pig hippocampus (submitted)

  • Morrison JH, Benoit R, Magistretti PJ, Ling N, Bloom FE (1982) Immunohistochemical distribution of prosomatostatin-related peptides in hippocampus. Neurosci Lett 34:137–142

    Google Scholar 

  • Nunzi MG, Gorio A, Milan F, Freund TF, Somogyi P, Smith AD (1985) Cholecystokinin-immunoreactive cells form symmetrical synaptic contacts with pyramidal and nonpyramidal neurons in the hippocampus. J Comp Neurol 237:485–505

    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, 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, Vaughn JE, Barber RP (1981) Immunocytochemical localization of GABAergic neurons at the electron microscopical level. J Histochem 13:555–582

    Google Scholar 

  • Ribak CE, Seress L, Amaral DG (1985) The development, ultrastructure and synaptic connections of the mossy cells of the dentate gyrus. J Neurocytol (in press)

  • Roberts GW, Woodhams PL, Polak JM, Crow TJ (1984) Distribution of neuropeptides in the limbic system of the rat: the hippocampus. Neuroscience 11:35–77

    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 

  • Schwartzkroin PA, Kunkel D (1985) Morphology of identified interneurons in the CA1 regions of guinea pig hippocampus. J Comp Neurol 232:205–218

    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 

  • Somogyi P, Smith AD, Nunzi MG, Gorio A, Takagi H, Wu JY (1983a) Glutamate decarboxylase immunoreactivity in the hippocampus of the cat: distribution of immunoreactive synaptic terminals with special reference to the axon initial segment of pyramidal neurons. J Neurosci 3:1450–1468

    Google Scholar 

  • Somogyi P, Nunzi MG, Gorio A, Smith AD (1983b) A new type of specific interneuron in the monkey hippocampus forming synapses exclusively with the axon initial segments of pyramidal cells. Brain Res 259:137–142

    Google Scholar 

  • Somogyi P, Hodgson AJ, Smith AD, Nunzi MG, Gorio A, Wu JY (1984) Different populations of GABAergic neurons in the visual cortex and hippocampus of cat contain somatostatin or cholecystokinin-immunoreactive material. J Neurosci 4:2590

    Google Scholar 

  • Spencer WA, Kandel ER (1961) Hippocampal neuron responses to selective activation of recurrent collaterals of hippocampofugal axons. Exp Neurol 4:149–161

    Google Scholar 

  • Stephan H (1975) Allocortex. Handbuch der mikroskopischen Anatomie des Menschen. Vol. IV/9. Springer, Berlin-Heidelberg-New York

    Google Scholar 

  • Storm-Mathisen J, Ottersen OP (1984) Neurotransmitters in the hippocampal formation. In: Reinoso-Suárez F, Ajmone-Marsan C (eds) Cortical integration. Raven Press, New York, pp 105–130

    Google Scholar 

  • Storm-Mathisen J, Leknes AK, Bore AT, Vaaland JL, Edminson P, Haug FMS, Ottersen OP (1983) First visualization of glutamate and GABA in neurones by immunocytochemistry. Nature 301:517–520

    Google Scholar 

  • Tömböl T, Somogyi G, Hajdu F (1978) Golgi study on cat hippocampal formation. Anat Embryol 153:331–350

    Google Scholar 

  • Zimmer J, Laurberg S, Sunde N (1983) Neuroanatomical aspects of normal and transplanted hippocampal tissue. In: Seifert W (ed) Neurobiology of the hippocampus. Academic Press, London New York, pp 39–64

    Google Scholar 

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In partial fulfilment of the requirements for the degree of Dr. med. at the Johann Wolfgang Goethe University, Frankfurt/Main

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Schlander, M., Frotscher, M. Non-pyramidal neurons in the guinea pig hippocampus. Anat Embryol 174, 35–47 (1986). https://doi.org/10.1007/BF00318334

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