Quantitative analysis of neurons and glial cells in the rat somatosensory cortex, with special reference to GABAergic neurons and parvalbumin-containing neurons (original) (raw)
Summary
The number of neuronal and glial cells in the rat somatosensory cortex (barrel area) has been estimated by a stereological method, the disector, using pairs of toluidine blue-stained, plastic-embedded 0.5-_μ_m-thick sections, 1.5 _μ_m distant from each other. Chemical properties of those disector-counted cells were further analyzed by postembedding immunocytochemical methods on adjacent semithin sections. Thus we were able to analyze quantitatively number, distribution, and proportion of five cell types: (1) gamma-aminobutyric acid-(GABA)-negative neurons; (2) GABA-like immunoreactive (GABA-LIR) neurons; (3) a specific calcium-binding protein parvalbumin-immunoreactive (PV-IR) neurons, a subpopulation of GABA-LIR neurons; (4) S-100_β_-LIR glial cells (astrocytes); and (5) S-100_β_-negative glial cells (oligodendrocytes and microglia). The densities of total cells, glial cells, and neurons in the rat somatosensory cortex were 85.4 × 103/mm3, 30.5 × 103/mm3, and 54.9 × 103/mm3, respectively. Of all neurons 25% and 14% were GABA-LIR and PV-IR, respectively; all PV-IR neurons are GABA-LIR, and thus about 54% of GABA-LIR neurons are PV-positive. The number of total cells under a unit surface area of 1 mm2 through the thickness of the somatosensory cortex was 171.6 × 103; the number of neurons and glial cells were 110.2 × 103 and 61.4 × 103, respectively. There were 27.7 × 103 GABA-LIR neurons and 15.0 × 103 and 12.7 × 103 PV-IR neurons and PV-negative GABA-LIR neurons, respectively. The laminar distribution of each group of cells shows prominent differences, indicating that the cellular composition was different from layer to layer. The density of GABA-LIR neurons was highest in layer IV. The numerical density of PV-IR neurons was 2–4 times higher in layer IV than in layers II/III, V, and VI, whereas that of PV-negative GABA-LIR neurons was almost constant throughout the layers.
Access this article
Subscribe and save
- Starting from 10 chapters or articles per month
- Access and download chapters and articles from more than 300k books and 2,500 journals
- Cancel anytime View plans
Buy Now
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
- Beaulieu C, Colonníer M (1983) The number of neurons in the different laminae of the binocular and monocular regions of area 17 in the cat. J Comp Neurol 217: 337–344
Google Scholar - Brændgaard H, Gundersen HJG (1986) The impact of recent stereological advances on quantitative studies of the nervous system. J Neurosci Methods 18: 39–78
Google Scholar - Celio MR (1986) GABA neurons contain the calcium binding protein parvalbumin. Science 232: 995–997
Google Scholar - Celio MR (1990) Calbindin D-28k and parvalbumin in the rat nervous system. Neuroscience 35: 375–475
Google Scholar - Chmielowska J, Stewart MG, Bourne RC (1988) _γ_-Aminobutyric acid (GABA) immunoreactivity in mouse and rat first somatosensory (SI) cortex: description and comparison. Brain Res 439: 155–168
Google Scholar - Cobas A, Welker E, Fairén A, Kraftsik R, Van der Loos H (1987) GABAergic neurons in the barrel cortex of the mouse: an analysis using neuronal archetypes. J Neurocytol 16: 843–871
Google Scholar - Demeulemeester H, Arckens L, Vandesande F, Orban GA, Heizmann CW, Pochet R (1991) Calcium binding proteins and neuropeptides as molecular markers of GABAergic interneurons in the cat visual cortex. Exp Brain Res 84: 538–544
Google Scholar - Elliot HC (1969) Textbook of neuroanatomy, 2nd ed. Lippincott, Philadelphia
Google Scholar - Fairén A, DeFelipe J, Regidor J (1984) Nonpyramidal neurons: general account. In: Peters A, Jones EG (eds) Cerebral cortex, vol 1, Plenum Press, New York, pp 29–245
Google Scholar - Gabbott PLA, Somogyi P (1986) Quantitative distribution of GABA-immunoreactive neurons in the visual cortex (area 17) of cat. Exp Brain Res 61: 323–331
Google Scholar - Gundersen HJG (1977) Notes on the estimation of the numerical density of arbitrary profiles: the edge effect. J Microsc 111: 219–223
Google Scholar - Gundersen HJG (1986) Stereology of arbitrary particles: a review of unbiased number and size estimators and the presentation of some new ones. In memory of William R. Thompson. J Microsc 143: 3–45
Google Scholar - Heizmann CW, Hunziker W (1991) Intracellular calcium-binding proteins: more sites than insights. Trends Biochem Sci 16: 98–103
Google Scholar - Hendry SHC, Schwark HD, Jones EG, Yan J (1987) Numbers and proportions of GABA-immunoreactive neurons in different areas of monkey cerebral cortex. J Neurosci 7: 1503–1519
Google Scholar - Hsu S-M, Raine L, Fanger H (1981) Use of avidin-biotin-peroxidase complex (ABC) in immunoperoxidase techniques. J Histochem Cytochem 29: 577–580
CAS PubMed Google Scholar - Isobe T, Ichimura T, Okuyama T (1990) Nervous system-specific proteins (in Japanese). Tanpakushitsu Kakusan Koso 35: 597–611
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 the rat testis: characterization, localization, and expression during development. J Biol Chem 262: 7314–7320
Google Scholar - 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
Google Scholar - Keller A, White EL (1986) Distribution of glutamic acid decarboxylase immunoreactive structures in the barrel region of mouse somatosensory cortex. Neurosci Lett 66: 245–250
Google Scholar - Korbo L, Pakkenberg B, Ladefoged O, Gundersen HJG, Arlien-Søborg P, Pakkenberg H (1990) An efficient method for estimating the total number of neurons in rat brain cortex. J Neurosci Methods 31: 93–100
Google Scholar - Kosaka T, Heizmann CW (1989) Selective staining of a population of parvalbumin-containing GABAergic neurons in the rat cerebral cortex by lectins with specific affinity for terminal N-acetylgalactosamine. Brain Res 483: 158–163
Google Scholar - Kosaka T, Nagatsu I, Wu J-Y, Hama K (1986) Use of high concentrations of glutaraldehyde for immunocytochemistry of transmitter-synthesizing enzymes in the central nervous system. Neuroscience 18: 975–990
Google Scholar - Kosaka T, Heizmann CW, Tateishi K, Hamaoka Y, Hama K (1987a)An aspect of the organizational principle of the _γ_-aminobutyric acidergic system in the cerebral cortex. Brain Res 409: 403–408
Google Scholar - Kosaka T, Katsumaru H, Hama K, Wu J-Y, Heizmann CW (1987b) GABAergic neurons containing the Ca2+-binding protein parvalbumin in the rat hippocampus and dentate gyrus. Brain Res 419: 119–130
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 - Kosaka T, Heizmann CW, Barnstable CJ (1989) Monoclonal antibody VC1. 1 selectively stains a population of GABAergic neurons containing the calcium-binding protein parvalbumin in the rat cerebral cortex. Exp Brain Res 78: 43–50
Google Scholar - Kosaka T, Isogai K, Barnstable CJ, Heizmann CW (1990) Monoclonal antibody HNK-1 selectively stains a subpopulation of GABAergic neurons containing the calcium-binding protein parvalbumin in the rat cerebral cortex. Exp Brain Res 82: 566–574
Google Scholar - Kosaka T, Heizmann CW, Fujita SC (1992) Monoclonal antibody 473 selectively stains a population of GABAergic neurons containing the calcium-binding protein parvalbumin in the rat cerebral cortex. Exp Brain Res 89: 109–114
Google Scholar - Lin C-S, Lu SM, Schmechel DE (1985) Glutamic acid decarboxylase immunoreactivity in layer IV of barrel cortex of rat and mouse. J Neurosci 5: 1934–1939
Google Scholar - Ling EA, Paterson JA, Privat A, Mori S, Leblond CP (1973)Investigation of glial cells in semithin sections. I. Identification of glial cells in the brain of young rats. J. Comp Neurol 149: 43–72
Google Scholar - Matute C, Streit P (1986) Monoclonal antibodies demonstrating GABA-like immunoreactivity. Histochemistry 86: 147–157
Google Scholar - Meinecke DL, Peters A (1987) GABA immunoreactive neurons in rat visual cortex. J Comp Neurol 261: 388–404
Google Scholar - Pakkenberg B, Gundersen HJG (1988) Total number of neurons and glial cells in human brain nuclei estimated by the disector and the fractionator. J Microsc 150: 1–20
PubMed Google Scholar - Paxinos G, Watson C (1986) The rat brain in stereotaxic coordinates, 2nd edn. Academic Press, Sydney
Google Scholar - Rockel AJ, Hiorns RW, Powell TPS (1980) The basic uniformity in structure of the neocortex. Brain 103: 221–244
Google Scholar - Sterio DC (1984) The unbiased estimation of number and sizes of arbitrary particles using the disector. J Microsc 134: 127–136
PubMed Google Scholar - Van Brederode JFM, Mulligan KA, Hendrickson AE (1990) Calcium-binding proteins as markers for subpopulations of GABAergic neurons in monkey striate cortex. J Comp Neurol 298: 1–22
Google Scholar - Van Brederode JFM, Helliesen MK, Hendrickson AE (1991) Distribution of the calcium-binding proteins parvalbumin and calbindin-D28k in the sensorimotor cortex of the rat. Neuroscience 44: 157–171
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 Methods 1: 383–391
Google Scholar
Author information
Authors and Affiliations
- Department of Anatomy and Neurobiology, Faculty of Medicine, Kyushu University, Higashi-ku, 812, Fukuoka, Japan
J. Q. Ren, Y. Aika & T. Kosaka - Department of Pediatrics, Division of Clinical Chemistry, University of Zürich, Steinwiesstr. 75, CH-8032, Zürich, Switzerland
C. W. Heizmann
Authors
- J. Q. Ren
- Y. Aika
- C. W. Heizmann
- T. Kosaka
Rights and permissions
About this article
Cite this article
Ren, J.Q., Aika, Y., Heizmann, C.W. et al. Quantitative analysis of neurons and glial cells in the rat somatosensory cortex, with special reference to GABAergic neurons and parvalbumin-containing neurons.Exp Brain Res 92, 1–14 (1992). https://doi.org/10.1007/BF00230378
- Received: 03 September 1991
- Accepted: 29 May 1992
- Issue date: December 1992
- DOI: https://doi.org/10.1007/BF00230378