Skip to main content
Log in

Immunocytochemical study of GABAergic neurons containing the calcium-binding protein parvalbumin in the rat hippocampus

  • Regular Papers
  • Published:
Experimental Brain Research Aims and scope Submit manuscript

Summary

The structural features of PV-immunoreactive (PV-I) neurons, a particular subpopulation of GABAergic neurons, in the hippocampus were studied by immunocytochemistry. The PV-I cell bodies were concentrated within the stratum pyramidale (SP) and stratum oriens (SO) in the hippocampus. PV-I puncta were frequent in SP, while they were rarely seen in other layers. The dendritic arborization of PV-I neurons resembled that of some of the nonpyramidal cells observed after Golgi-impregnation. The most commonly observed PV-I neurons had their perikarya located in SP with dendrites extending into SO and the stratum radiatum (SR). Most of the dendrites in SR had typical beaded or varicose segments. The dendrites extending into SO had few beaded parts. There were many bipolar and multipolar neurons with smooth dendrites in SO, but only a small number of such multipolar neurons in SR. An electron microscopic analysis revealed that PV-I products were located to perikarya, dendrites, myelinated axons and synaptic boutons. The perikarya of PV-I neurons exhibited several ultrastructural features of nonpyramidal cells, e.g., abundant cisternae of endoplasmic reticulum, mitochondria and other perikaryal organelles, an infolded nuclear envelope and intranuclear inclusions. They received many asymmetric synapses with round presynaptic vesicles. There were numerous PV-I boutons, presumably axonal endings, covering the pyramidal cell bodies. The PV-I boutons also contacted the axon initial segments and proximal dendrites of the pyramidal cells. In addition PV-I terminals were found on somata and dendrites of both PV-I or PV-negative nonpyramidal cells. The results suggest that PV-containing neurons include basket and axo-axonic 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

  • Bendayan M, Zollinger M (1983) Ultrastructural localization of antigenic sites on osmium-fixed tissues applying the protein A-gold technique. J Histochem Cytochem 31: 101–109

    Google Scholar 

  • Celio MR (1986) Parvalbumin in most γ-aminobutyric acidcontaining neurons of the rat cerebral cortex. Science 231: 995–997

    Google Scholar 

  • Celio MR, Heizmann CW (1981) Calcium-binding protein parvalbumin as a neuronal marker. Nature 293: 300–302

    Google Scholar 

  • Fairén A, Valverde F (1980) A specialized type of neuron in the visual cortex of cat: a Golgi and electron microscope study of chandelier cells. J Comp Neurol 194: 761–779

    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 

  • Heizmann CW (1984) Parvalbumin, an intracellular calciumbinding protein; distribution, properties and possible roles in mammalian cells. Experientia 40: 910–921

    Google Scholar 

  • Heizmann CW, Celio MR (1987) Immunolocalization of parvalbumin. Methods Enzymol 139: 552–570

    Google Scholar 

  • Hendry SHC, Jones EG (1985) Morphology of synapses formed by cholecystokinin-immunoreactive axon terminals in regio superior of rat hippocampus. Neuroscience 16: 57–68

    Google Scholar 

  • Hökfelt T, Holets VR, Staines W, Meister B, Melander T, Schalling M, Schultzberg M, Freedman J, Björklund H, Olson L, Lindh B, Elfvin L-G, Lundberg JM, Lindgren JA, Samuelsson B, Pernow B, Terenius L, Post C, Everitt B, Goldstein M (1986) Coexistence of neuronal messengers — an overview. In: Hökfelt T, Fuxe K, Pernow B (eds) Progress in brain research, Vol 68. Elsevier Science Publishers, Amsterdam, pp 33–70

    Google Scholar 

  • Jones EG, Hendry SHC (1986) Co-localization of GABA and neuropeptides in neocortical neurons. Trends Neurosci 9: 71–76

    Google Scholar 

  • Kägi U, Berchtold MW, Heizmann CW (1987) Ca2+-binding parvalbumin in rat testis. J Biol Chem 262: 7314–7320

    Google Scholar 

  • Katsumaru H, Kosaka T, Heizmann CW, Hama K (1988) Gap junctions on GABAergic neurons containing the calciumbinding protein parvalbumin in the rat hippocampus (CA1 region). Exp Brain Res 72: 363–370

    Google Scholar 

  • Kawaguchi Y, Hama K (1987) Two subtypes of non-pyramidal cells in rat hippocampal formation identified by intracellular recording and HRP injection. Brain Res 411: 190–195

    Google Scholar 

  • 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

    Google Scholar 

  • Kisvárday ZF, Martin KAC, Whitteridge D, Somogyi P (1985) Synaptic connections of intracellularly filled clutch cells: a type of small basket cell in the visual cortex of the cat. J Comp Neurol 241: 111–137

    Google Scholar 

  • Kosaka T (1980) The axon initial segment as a synaptic site: ultrastructure and synaptology of the initial segment of the pyramidal cell in the rat hippocampus (CA3 region). J Neurocytol 9: 861–882

    Google Scholar 

  • Kosaka T, Hataguchi Y, Hama K, Nagatsu I, Wu J-Y (1985a) Coexistence of immunoreactivities for glutamate decarboxylase and tyrosine hydroxylase in some neurons in the periglomerular region of the rat main olfactory bulb: possible coexistence of gamma-aminobutyric acid (GABA) and dopamine. Brain Res 343: 166–171

    Google Scholar 

  • Kosaka T, Katsumaru H, Hama K, Wu J-Y, Heizmann CW (1987) GABAergic neurons containing the Ca2+-binding protein parvalbumin in the rat hippocampus and dentate gyrus. Brain Res 419: 119–130

    Google Scholar 

  • Kosaka T, Kosaka K, Tateishi K, Hamaoka Y, Yanaihara N, Wu J-Y, Hama K (1985b) 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 

  • Kosaka T, Nagatsu I, Wu J-Y, Hama K (1986) Use of high concentrations of glutaraldehyde for immmunocytochemistry of transmitter-synthesizing enzymes in the central nervous system. Neuroscience 18: 975–990

    Google Scholar 

  • Kosaka T, Wu J-Y, Benoit R (1988) GABAergic neurons containing somatostatin-like immunoreactivity in the rat hippocampus and dentate gyrus, Exp Brain Res 71: 388–398

    Google Scholar 

  • Lane BP, Europa DL (1965) Differential staining of ultrathin sections of Epon-embedded tissues for light microscopy. J Histochem Cytochem 13: 579–582

    CAS  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. J Psychol Neurol 46: 113–177

    Google Scholar 

  • Lundberg JM, Hökfelt T (1983) Coexistence of peptides and classical neurotransmitters. Trends Neurosci 6: 325–333

    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 

  • Oertel WH, Schmechel DE, Tappaz ML, Kopin IJ (1981a) Production of a specific antiserum to rat brain glutamic acid decarboxylase by injection of an antigen-antibody complex. Neuroscience 6: 2689–2700

    Google Scholar 

  • Oertel WH, Schmechel DE, Mugnaini E, Tappaz ML, Kopin IJ (1981b) Immunocytochemical localization of glutamate decarboxylase in rat cerebellum with a new antiserum. Neuroscience 6: 2715–2735

    Google Scholar 

  • Ottersen OP, Storm-Mathisen J (1984) Glutamate and GABAcontaining neurons in the mouse and rat brain, as demonstrated with a new immunocytochemical technique. J Comp Neurol 229: 374–392

    Google Scholar 

  • Peters A, Proskauer CC, Ribak CE (1982) Chandelier cells in rat visual cortex. J Comp Neurol 206: 397–416

    Google Scholar 

  • Ramón Y, Cajal S (1968) The structure of Ammon's Horn, translated by Kraft LM. Charles Thomas, Springfield IL, 78 pp

    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 47: 227–232

    Google Scholar 

  • Schwartzkroin PA, Knowles WD (1983) Local interactions in the hippocampus. Trends Neurosci 6: 88–92

    Google Scholar 

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

    Google Scholar 

  • Somogyi P (1977) A specific ‘axo-axonic’ interneuron in the visual cortex of the rat. Brain Res 136: 345–350

    Google Scholar 

  • Somogyi P, Freund TF, Hodgson AJ, Somogyi J, Beroukas D, Chubb IW (1985a) Identified axo-axonic cells are immunoreactive for GABA in the hippocampus and visual cortex of the cat. Brain Res 332: 143–149

    Google Scholar 

  • Somogyi P, Hodgson AJ, Chubb IW, Penke B, Erdei A (1985b) Antisera to γ-aminobutyric acid. II. Immunocytochemical application to the central nervous system. J Histochem Cytochem 33: 240–248

    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 somatostatinor cholecystokinin-immunoreactive material. J Neurosci 4: 2590–2603

    Google Scholar 

  • Somogyi P, Kisvárday ZF, Martin KAC, Whitteridge D (1983a) Synaptic connections of morphologically identified and physiologically characterized large basket cells in the striate cortex of cat. Neuroscience 10: 261–294

    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 

  • Sternberger LA (1979) Immunocytochemistry (2nd edn). Wiley, New York

    Google Scholar 

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

    Google Scholar 

  • Tömböl T, Babosa M, Hajdú F, Somogyi G (1979) Interneurons: an electron microscopic study of the cat's hippocampal formation. II. Acta Morphol Acad Sci Hung 27: 297–313

    Google Scholar 

  • Totterdell S, Smith AD (1986) Cholecystokinin-immunoreactive boutons in synaptic contact with hippocampal pyramidal neurons that project to the nucleus accumbens. Neuroscience 19: 181–192

    Google Scholar 

  • Wilson CJ, Groves PM (1979) A simple and rapid section embedding technique for sequential light and electron microscopic examination of individually stained central neurons. J Neurosci Meth 1: 383–391

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Katsumaru, H., Kosaka, T., Heizmann, C.W. et al. Immunocytochemical study of GABAergic neurons containing the calcium-binding protein parvalbumin in the rat hippocampus. Exp Brain Res 72, 347–362 (1988). https://doi.org/10.1007/BF00250256

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00250256

Key words

Navigation