Summary
The calcium-binding protein parvalbumin is considered to be involved in the control of intracellular ion homeostasis of highly active inhibitory neurons. A review of the light and electron microscopical features as well as the identified synaptic connections of these neurons is presented. Parvalbumin-containing neurons are mostly located within or in the vicinity of the granule or pyramidal cell layer. They form a subgroup of GABAergic neurons that has a target specificity for the cell body region. Their fine structural characteristics are identical to those known for hippocampal inhibitory neurons. Parvalbumin-containing neurons are involved in several inhibitory pathways: feed-back inhibition, feed-forward inhibition and disinhibition. The functional implications of our own as well as published data are discussed. Special consideration is given to the possible physiological role of parvalbumin in these neurons.
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References
Andersen P, Bliss TVP, Skrede KK (1971) Lamellar organization of hippocampal excitatory pathways. Exp Brain Res 13:222–238
Bakst I, Morrison JH, Amaral DG (1985) The distribution of somatostatin-like immunoreactivity in the monkey hippocampal formation. J Comp Neurol 236:423–442
Berchtold MW, Celio MR, Heizmann CW (1984) Parvalbumin in non-muscle tissue of the rat. Quantitation and immunohistochemical localisation. J Biol Chem 259:5189–5196
Braun K, Scheich H, Schachner M, Heizmann CW (1985a) Distribution of parvalbumin, cytochrome oxydase activity and 14c-2-deoxyglucose uptake in the brain of the zebra finch. Part 1: Auditory and vocal motor system. Cell Tissue Res 240:101–115
Braun K, Scheich H, Schachner M, Heizmann CW (1985b) Distribution of parvalbumin, cytochrome oxydase activity and 14c-2-deoxyglucose uptake in the brain of the zebra finch. Part 2: Visual system. Cell Tissue Res 240:117–127
Buzsáki G (1984) Feed-forward inhibition in the hippocampal formation. Prog Neurobiol 22:131–151
Cajal SR y (1911) Histologie du système nerveux de l’homme et des vertébrés, vol 2. Maloine, Paris
Celio MR (1986) Parvalbumin in most gamma-aminobutyric acidcontaining neurons in the rat cerebral cortex. Science 9231:995–997
Celio MR, Heizmann CW (1981) Calcium-binding protein parvalbumin as a neuronal marker. Nature 293:300–302
Celio MR, Keller GA, Bloom FE (1986) Immunoelectronmicroscopy of neuronal antigens on ultrathin frozen sections. J Histochem Cytochem 34:491–500
Celio MR, Baier W, Schärer PA, DeViragh PA, Gerday C (1988) Monoclonal antibodies directed against the calcium-binding protein parvalbumin. Cell Calcium 9:81–86
DeFelipe J, Hendry SHC, Jones EG, Schmechel D (1989) Variability of the terminations of GABAergic chandelier cell axons in the monkey sensory-motor cortex. J Comp Neurol 321:364–384
Desphande JK, Siesjö BK, Wieloch T (1987) Calcium accumulation and neuronal damage in the rat hippocampus following cerebral ischemia. J Cereb Blood Flow Metab 7:89–95
Freund TF (1989) GABAergic septohippocampal neurons contain parvalbumin. Brain Res 478:375–381
Freund TF, Antal M (1988) GABA-containing neurons in the septum control inhibitory interneurons in the hippocampus. Nature 336:170–173
Frotscher M (1985) Mossy fibers from 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
Frotscher M (1989) Mossy fiber synapses on glutamate decarboxylase-immunoreactive neurons: evidence for feed-forward inhibition in the CA3 region of the hippocampus. Exp Brain Res 75:441–445
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
Frotscher M, Leranth C (1988) Catecholaminergic innervation of pyramidal and GABAergic nonpyramidal neurons in the rat hippocampus. Double label immunostaining with antibodies against tyrosine hydroxylase and glutamate decarboxylase. Histochemistry 88:313–319
Frotscher M, Zimmer J (1983) Commissural fibers terminate on nonpyramidal neurons in the guinea-pig hippocampus — a combined Golgi/EM degeneration study. Brain Res 265:289–293
Frotscher M, Leranth C, Lübbers K, Oertel WH (1984) Commissural afferents innervate glutamate decarboxylase immunoreactive nonpyramidal neurons in the guinea-pig hippocampus. Neurosci Lett 46:137–143
Frotscher M, Nitsch R, Leranth C (1989) Cholinergic innervation of identified neurons in the hippocampus: electron microscopic double labeling studies. In: Chan-Palay V, Köhler C (eds) The hippocampus: new vistas. Alan R Liss, New York, pp 85–96
Germroth P, Schwerdtfeger WK, Buhl EH (1989) Identified GABAergic neurons in the entorhinal cortex project to the hippocampus. Eur J Neurosci [Suppl 2]:272
Heizmann CW (1984) Parvalbumin, an intracellular calcium-binding protein: Distribution, properties and possible role in mammalian cells. Experientia 40:910–921
Johansen FF, Zimmer J, Diemer NH (1987) Early loss of somatostatin neurons in the dentate hilus after cerebral ischemia in the rat precedes CA1 pyramidal cell loss. Acta Neuropathol (Berl) 73:110–114
Johansen FF, Tonder N, Baimbridge K, Zimmer J, Diemer NH (1989) Reversible loss of parvalbumin immunoreactivity in the postischemic rat hippocampus. Europ J Neurosci [Suppl 2]:149
Katsumaru H, Kosaka T, Heizmann CW, Hama K (1988) Immunocytochemical study of GABAergic neurons containing the calcium-binding protein parvalbumin in the rat hippocampus. Exp Brain Res 72:347–362
Kawaguchi Y, Hama K (1987) Fast-spiking non-pyramidal cells in the hippocampal CA3 region, dentate gyrus and subiculum of rats. Brain Res 425:351–355
Kawaguchi Y, Katsumaru H, Kosaka T, Heizmann CW, Hama K (1987) Fast-spiking cells in rat hippocampus (CA1 region) contain the calcium-binding protein parvalbumin. Brain Res 416:369–374
Köhler C, Chan-Palay V (1982) Somatostatin-like immunoreactivity in the hippocampus: an immunocytochemical study in the rat. Neurosci Lett 34:259–264
Kosaka T, Hama K, Wu JY (1984) GABAergic synaptic boutons in the granule cell layer of rat dentate gyrus. Brain Res 293:353–359
Kosaka T, Katsumaru H, Hama K, Wu JY, Heizmann CW (1987) GABAergic neurons containing the Ca2+-binding protein parvalbumin in the rat hippocampus and dentate gyrus. Brain Res 419:119–130
Kosaka T, Wu JY, Benoit R (1988) GABAergic neurons containing somatostatin-like immunoreactivity in the rat hippocampus and dentate gyrus. Exp Brain Res 71:388–398
Leranth C, Frotscher M (1987) Cholinergic innervation of hippocampal GAD- and somatostatin-immunoreactive commissural neurons. J Comp Neurol 261:33–47
Leranth C, Malcom AJ, Frotscher M (1989) Afferent and efferent synaptic connections of somatostatin-immunoreactive neurons in the rat fascia dentata. J Comp Neurol, in press
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 (Lpz) 46:113–177
Lübbers K, Frotscher M (1987) Fine structure and synaptic connections of identified neurons in the rat fascia dentata. Anat Embryol 177:1–14
Lübbers K, Wolff JR, Frotscher M (1985) Neurogenesis of GABAergic neurons in the rat dentate gyrus: a combined autoradiographic and immunocytochemical study. Neurosci Lett 62:317–322
Milner TA, Bacon CE (1989) Ultrastructural localization of somatostatin-like immunoreactivity in the rat dentate gyrus. Soc Neurosci Abstr 15:401
Misgeld U, Frotscher M (1986) Postsynaptic GABAergic inhibition of nonpyramidal neurons in the guinea-pig hippocampus. Neuroscience 19:193–206
Mugnaini E, Dahl AL (1983) Zinc-aldehyde fixation for light microscopic immunocytochemistry for nervous tissue. J Histochem Cytochem 31:1435–1438
Nitsch R, Klauer G (1989) Cryostat sections for coexistence studies and pre-embedding electron microscopic immunocytochemistry of central and peripheral nervous system tissue. Histochemistry 92:459–465
Nitsch C, Goping G, Klatzo I (1989a) Preservation of GABAergic perikarya and boutons after transient ischemia in the gerbil hippocampal CA1 field. Brain Res 495:243–252
Nitsch C, Scotti AL, Sommacal A, Kalt G (1989b) GABAergic hippocampal neurons resistant to ischemia induced delayed neuronal death contain the calcium-binding protein parvalbumin. Neurosci Lett 105:263–268
Novikoff AB, Novikoff PM, Quintana M, Davis C (1972) Diffusion artifacts in 3,3′-diaminobenzidine cytochemistry. J Histochem Cytochem 20:745–749
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
Ribak CE, Anderson L (1980) Ultrastructure of the pyramidal basket cells in the dentate gyrus of the rat. J Comp Neurol 192:903–916
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
Ribak CE, Vaughn JE, Barber RP (1981) Immunocytochemical localization of GABAergic neurons at the electron microscopic level. Histochem J 13:555–582
Ribak CE, Seress L, Peterson GM, Seroogy KB, Falloon JH, Schmued LC (1986) A GABAergic inhibitory component within the hippocampal commissural pathway. Neurosci 6:3492–3498
Scharfman HI, Schwartzkroin PA (1989) Protection of hilar cells from prolonged stimulation by intracellular calcium chelation. Science 246:257–260
Schlander M, Frotscher M (1986) Nonpyramidal neurons in the guinea-pig hippocampus: A combined Golgi-electron microscope study. Anat Embryol 174:35–47
Schlander M, Hoyer S, Frotscher M (1988) Glutamate decarboxylase immunoreactive neurons in the aging rat hippocampus are more resistant to ischemia than CA1 pyramidal cells. Neurosci Lett 91:241–246
Schwartzkroin PA, Kunkel DD (1985) Morphology of identified interneurons in the CA1 region of guinea pig hippocampus. J Comp Neurol 232:205–218
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
Seress L, Ribak CE (1985) A combined Golgi-electron microscopic study of nonpyramidal neurons in the CA1 area of the hippocampus. J Neurocytol 14:717–730
Sloviter RS (1987) Decreased hippocampal inhibition and a selective loss of interneurons in experimental epilepsy. Science 235:73–76
Sloviter RS (1989) Calcium-binding protein (Calbindin-D28k) and parvalbumin immunocytochemistry: Localization in the rat hippocampus with specific reference to the selective vulnerability of hippocampal neurons to seizure activity. J Comp Neurol 280:183–196
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 4:2590–2603
Soriano E, Nitsch R, Frotscher M (1990) Axo-axonic chandelier cells in the rat fascia dentata: Golgi-EM and immunocytochemical studies. J Comp Neurol 293:1–25
Storm-Mathisen J, Ottersen OP (1984) Neurotransmitters in the hippocampal formation. In: Reinoso Suárez, Ajmone-Marsan C (eds) Cortical integration. Raven Press, New York, pp 105–130
Zipp F, Nitsch R, Soriano E, Frotscher M (1989) Entorhinal fibers form synaptic contacts on parvalbumin-immunoreactive neurons in the rat fascia dentata. Brain Res 495:161–166
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Nitsch, R., Soriano, E. & Frotscher, M. The parvalbumin-containing nonpyramidal neurons in the rat hippocampus. Anat Embryol 181, 413–425 (1990). https://doi.org/10.1007/BF02433788
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DOI: https://doi.org/10.1007/BF02433788