Quantitative analysis of neurons and glial cells in the rat somatosensory cortex, with special reference to GABAergic neurons and parvalbumin-containing neurons

Ren, J.Q.; Aika, Y.; Heizmann, C.W.; Kosaka, T.

doi:10.1007/bf00230378

Cited by 148Neuroscience and Neuropharmacology ResearchNeuroinflammation and Neurodegeneration MechanismsNeural dynamics and brain function

Quantitative analysis of neurons and glial cells in the rat somatosensory cortex, with special reference to GABAergic neurons and parvalbumin-containing neurons

Ren, J.Q., Aika, Y., Heizmann, C.W., Kosaka, T.·1992·Experimental Brain Research

DOI 10.1007/bf00230378

Open this paper in CoChat — free account

Abstract

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-microns-thick sections, 1.5 microns 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 beta-LIR glial cells (astrocytes); and (5) S-100 beta-negative glial cells (oligodendrocytes and microglia). The densities of total cells, glial cells, and neurons in the rat somatosensory cortex were 85.4 +/- 10(3)/mm3, 30.5 x 10(3)/mm3, and 54.9 x 10(3)/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 x 10(3); the number of neurons and glial cells were 110.2 x 10(3) and 61.4 x 10(3), respectively. There were 27.7 x 10(3) GABA-LIR neurons and 15.0 x 10(3) and 12.7 x 10(3) 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.

Integrity signals

Registry

Crossref · 10.1007/bf00230378

Cites

38 of 38 references verified0 citation errors · 0 not checkable

Statistics

Recomputing p-values needs the paper’s full text.

Claims the paper makes

This paper’s full text isn’t openly available, so its claims and self-check weren’t run. The registry and citation checks still apply.

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Approximately 10% of all NeuN+ neurons in cortex are PV+.
“In agreement with the literature24–26, ~10% of all NeuN+ neurons in cortex were PV+ (Fig. 1b, c)”
From Perineuronal nets decrease membrane capacitance of peritumoral fast spiking interneurons in a model of epilepsy (2018) · cites this paper as [24]

The Rat Brain in Stereotaxic Coordinates
Paxinos, G., & Watson, C. (1983) · Elsevier eBooks · doi:10.1016/c2009-0-63235-9 · Cited by 28,585 · see citing works
Use of avidin-biotin-peroxidase complex (ABC) in immunoperoxidase techniques: a comparison between ABC and unlabeled antibody (PAP) procedures.
Hsu, S. M., Raine, L., & Fanger, H. (1981) · Journal of Histochemistry & Cytochemistry · doi:10.1177/29.4.6166661 · Cited by 14,248 · see citing works
The unbiased estimation of number and sizes of arbitrary particles using the disector
Sterio, D. C. (1984) · Journal of Microscopy · doi:10.1111/j.1365-2818.1984.tb02501.x · Cited by 2,533 · see citing works
Calbindin D-28k and parvalbumin in the rat nervous system
Celio, M. R. (1990) · Neuroscience · doi:10.1016/0306-4522(90)90091-h · Cited by 2,086 · see citing works
The rat brain in stereotaxic coordinates (2nd edn)
Herman, J. P., & Watson, S. J. (1987) · Trends in Neurosciences · doi:10.1016/0166-2236(87)90017-8 · Cited by 1,751 · see citing works
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.
Gundersen, H. J. G. (1986) · PubMed · Cited by 1,659 · see citing works
Notes on the estimation of the numerical density of arbitrary profiles: the edge effect
Gundersen, H. J. G. (1977) · Journal of Microscopy · doi:10.1111/j.1365-2818.1977.tb00062.x · Cited by 1,265 · see citing works
THE BASIC UNIFORMITY IN STRUCTURE OF THE NEOCORTEX
Röckel, A., Hiorns, R. W., & Powell, T. P. S. (1980) · Brain · doi:10.1093/brain/103.2.221 · Cited by 902 · see citing works
Numbers and proportions of GABA-immunoreactive neurons in different areas of monkey cerebral cortex
Hendry, S., Schwark, H. D., Jones, E. G., & Yan, J. (1987) · Journal of Neuroscience · doi:10.1523/jneurosci.07-05-01503.1987 · Cited by 601 · see citing works
GABAergic neurons containing the Ca2+-binding protein parvalbumin in the rat hippocampus and dentate gyrus
Kosaka, T., Katsumaru, H., Hama, K., Wu, J.-Y., & Heizmann, C. W. (1987) · Brain Research · doi:10.1016/0006-8993(87)90575-0 · Cited by 536 · see citing works
Self-citation
The impact of recent stereological advances on quantitative studies of the nervous system
Brændgaard, H., & Gundersen, H. J. G. (1986) · Journal of Neuroscience Methods · doi:10.1016/0165-0270(86)90112-3 · Cited by 505 · see citing works
Intracellular calcium-binding proteins: more sites than insights
Heizmann, C. W., & Hunzlker, W. (1991) · Trends in Biochemical Sciences · doi:10.1016/0968-0004(91)90041-s · Cited by 454 · see citing works
Self-citation
Investigation of glial cells in semithin sections. I. Identification of glial cells in the brain of young rats
Ling, E., Paterson, J. A., Privat, A., Mori, S., & Leblond, C. P. (1973) · The Journal of Comparative Neurology · doi:10.1002/cne.901490104 · Cited by 402 · see citing works
Total number of neurons and glial cells in human brain nuclei estimated by the disector and the fractionator
Pakkenberg, B., & Gundersen, H. J. G. (1988) · Journal of Microscopy · doi:10.1111/j.1365-2818.1988.tb04582.x · Cited by 347 · see citing works
Calcium‐binding proteins as markers for subpopulations of GABAergic neurons in monkey striate cortex
van Brederode, J. F. M., Mulligan, K. A., & Hendrickson, A. E. (1990) · The Journal of Comparative Neurology · doi:10.1002/cne.902980102 · Cited by 284 · see citing works
Quantitative distribution of GABA-immunoreactive neurons in the visual cortex (area 17) of the cat
Gabbott, P. L. A., & Somogyi, P. (1986) · Experimental Brain Research · doi:10.1007/bf00239522 · Cited by 269 · see citing works
Immunocytochemical study of GABAergic neurons containing the calcium-binding protein parvalbumin in the rat hippocampus
Katsumaru, H., Kosaka, T., Heizmann, C. W., & Hama, K. (1988) · Experimental Brain Research · doi:10.1007/bf00250256 · Cited by 249 · see citing works
Self-citation
Use of high concentrations of glutaraldehyde for immunocytochemistry of transmitter-synthesizing enzymes in the central nervous system
Kosaka, T., Nagatsu, I., Wu, J., & Hama, K. (1986) · Neuroscience · doi:10.1016/0306-4522(86)90112-0 · Cited by 232 · see citing works
Self-citation
GABAergic neurons containing somatostatin-like immunoreactivity in the rat hippocampus and dentate gyrus
Kosaka, T., Wu, J., & Benoit, R. (1988) · Experimental Brain Research · doi:10.1007/bf00247498 · Cited by 218 · see citing works
Self-citation
Co-localization of GABA and neuropeptides in neocortical neurons
Jones, E. G., & Hendry, S. H. C. (1986) · Trends in Neurosciences · doi:10.1016/0166-2236(86)90026-3 · Cited by 204 · see citing works
GABA immunoreactive neurons in rat visual cortex
Meinecke, D. L., & Peters, A. (1987) · The Journal of Comparative Neurology · doi:10.1002/cne.902610305 · Cited by 196 · see citing works
Distribution of the calcium-binding proteins parvalbumin and calbindin-D28k in the sensorimotor cortex of the rat.
van Brederode, J. V., Helliesen, M., & Hendrickson, A. (1991) · Neuroscience · doi:10.1016/0306-4522(91)90258-p · Cited by 184 · see citing works
Propolypeptide of von Willebrand Factor Circulates in Blood and Is Identical to von Willebrand Antigen II
Fay, P. J., Kawai, Y., Wagner, D. D., Ginsburg, D., Bonthron, D. T., Ohlsson‐Wilhelm, B. M., Chavin, S. I., Abraham, G. N., Handin, R. I., Orkin, S. H., et al. (1986) · Science · doi:10.1126/science.3486471 · Cited by 160 · see citing works
Selective staining of a population of parvalbumin-containing GABAergic neurons in the rat cerebral cortex by lectins with specific affinity for terminal N-acetylgalactosamine
Kosaka, T., & Heizmann, C. W. (1989) · Brain Research · doi:10.1016/0006-8993(89)90048-6 · Cited by 153 · see citing works
Self-citation
Monoclonal antibodies demonstrating GABA-like immunoreactivity
Matute, C., & Streit, P. (1986) · Histochemistry and Cell Biology · doi:10.1007/bf00493380 · Cited by 148 · see citing works
Calcium binding proteins and neuropeptides as molecular markers of GABAergic interneurons in the cat visual cortex
Demeulemeester, H. G., Arckens, L., Vandesande, F., Orban, G. A., Heizmann, C. W., & Pochet, R. (1991) · Experimental Brain Research · doi:10.1007/bf00230966 · Cited by 144 · see citing works
Self-citation
Ca2+-binding parvalbumin in rat testis. Characterization, localization, and expression during development.
Kägi, U., Berchtold, M. W., & Heizmann, C. W. (1987) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)48238-5 · Cited by 141 · see citing works
Self-citation
The number of neurons in the different laminae of the binocular and monocular regions of area 17 in the cat
Beaulieu, C., & Colonnier, M. (1983) · The Journal of Comparative Neurology · doi:10.1002/cne.902170308 · Cited by 124 · see citing works
An efficient method for estimating the total number of neurons in rat brain cortex
Korbo, L., Pakkenberg, B., Ladefoged, O., Gundersen, H. J. G., Arlien-Søborg, P., & Pakkenberg, H. (1990) · Journal of Neuroscience Methods · doi:10.1016/0165-0270(90)90153-7 · Cited by 108 · see citing works
Glutamic acid decarboxylase immunoreactivity in layer IV of barrel cortex of rat and mouse
Lin, C., Lu, S., & Schmechel, D. E. (1985) · Journal of Neuroscience · doi:10.1523/jneurosci.05-07-01934.1985 · Cited by 87 · see citing works
An aspect of the organizational principle of the γ-aminobutyric acidergic system in the cerebral cortex
Kosaka, T., Heizmann, C. W., Tateishi, K., Hamaoka, Y., & Hama, K. (1987) · Brain Research · doi:10.1016/0006-8993(87)90732-3 · Cited by 84 · see citing works
Self-citation
Monoclonal antibody HNK-1 selectively stains a subpopulation of GABAergic neurons containing the calcium-binding protein parvalbumin in the rat cerebral cortex
Kosaka, T., Isogai, K., Barnstable, C. J., & Heizmann, C. W. (1990) · Experimental Brain Research · doi:10.1007/bf00228797 · Cited by 79 · see citing works
Self-citation
A simple and rapid section embedding technique for sequential light and electron microscopic examination of individually stained central neurons
Wilson, C. J., & Groves, P. M. (1979) · Journal of Neuroscience Methods · doi:10.1016/0165-0270(79)90027-x · Cited by 62 · see citing works
Distribution of glutamic acid decarboxylase-immunoreactive structures in the barrel region of mouse somatosensory cortex
Keller, A., & White, E. L. (1986) · Neuroscience Letters · doi:10.1016/0304-3940(86)90026-1 · Cited by 54 · see citing works
γ-Aminobutyric acid (GABA) immunoreactivity in mouse and rat first somatosensory (SI) cortex: description and comparison
Chmielowska, J., Stewart, M. G., & Bourne, R. C. (1988) · Brain Research · doi:10.1016/0006-8993(88)91472-2 · Cited by 36 · see citing works
GABAergic neurons in the barrel cortex of the mouse: An analysis using neuronal archetypes
Cobas, A., Welker, E., Fairén, A., Kraftsik, R., & der Loos, H. V. (1987) · Journal of Neurocytology · doi:10.1007/bf01611990 · Cited by 36 · see citing works
Textbook of neuroanatomy
Elliott, H. C. (1963) · Lippincott eBooks · Cited by 24 · see citing works
[Nervous system-specific proteins].
Isobe, T., Ichimura, T., & Okuyama, T. (1990) · PubMed · Cited by 6 · see citing works

Flagged first, then by citations

Sorted by citations

Interneurons of the neocortical inhibitory system
Markram, H., Toledo-Rodriguez, M., Wang, Y., Gupta, A., Silberberg, G., & Wu, C. (2004) · Nature Reviews Neuroscience · doi:10.1038/nrn1519 · Cited by 2,954 · see citing works
Driving fast-spiking cells induces gamma rhythm and controls sensory responses
Cardin, J. A., Carlén, M., Meletis, K., Knoblich, U., Zhang, F., Deisseroth, K., Tsai, L.-H., & Moore, C. I. (2009) · Nature · doi:10.1038/nature08002 · Cited by 2,603 · see citing works
CORTICAL PLASTICITY: From Synapses to Maps
Buonomano, D. V., & Merzenich, M. M. (1998) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.21.1.149 · Cited by 2,083 · see citing works
Microstructure of the neocortex: comparative aspects
DeFelipe, J., Alonso-Nanclares, L., & Arellano, J. I. (2002) · Journal of Neurocytology · doi:10.1023/a:1024130211265 · Cited by 686 · see citing works
Types of neurons, synaptic connections and chemical characteristics of cells immunoreactive for calbindin-D28K, parvalbumin and calretinin in the neocortex
DeFelipe, J. (1997) · Journal of Chemical Neuroanatomy · doi:10.1016/s0891-0618(97)10013-8 · Cited by 550 · see citing works
Three distinct families of GABAergic neurons in rat visual cortex
Gonchar, Y. (1997) · Cerebral Cortex · doi:10.1093/cercor/7.4.347 · Cited by 481 · see citing works
Cellular distribution of the calcium-binding proteins parvalbumin, calbindin, and calretinin in the neocortex of mammals: phylogenetic and developmental patterns
Hof, P. R., Glezer, I. I., Condé, F., Flagg, R. A., Rubin, M. B., Nimchinsky, E. A., & Weisenhorn, D. M. V. (1999) · Journal of Chemical Neuroanatomy · doi:10.1016/s0891-0618(98)00065-9 · Cited by 411 · see citing works
Calcium Dynamics of Cortical Astrocytic Networks In Vivo
Hirase, H., Qian, L., Barthó, P., & Buzsáki, G. (2004) · PLoS Biology · doi:10.1371/journal.pbio.0020096 · Cited by 401 · see citing works
Cell Densities in the Mouse Brain: A Systematic Review
Keller, D., Erö, C., & Markram, H. (2018) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2018.00083 · Cited by 380 · see citing works
Anatomical, Physiological, Molecular and Circuit Properties of Nest Basket Cells in the Developing Somatosensory Cortex
Wang, Y. (2002) · Cerebral Cortex · doi:10.1093/cercor/12.4.395 · Cited by 371 · see citing works
Layer V Neurons in Mouse Cortex Projecting to Different Targets Have Distinct Physiological Properties
Hattox, A. M., & Nelson, S. B. (2007) · Journal of Neurophysiology · doi:10.1152/jn.00397.2007 · Cited by 344 · see citing works
Diverse Types of Interneurons Generate Thalamus-Evoked Feedforward Inhibition in the Mouse Barrel Cortex
Porter, J. T., Johnson, C. K., & Agmon, A. (2001) · Journal of Neuroscience · doi:10.1523/jneurosci.21-08-02699.2001 · Cited by 344 · see citing works
Excitatory neuronal connectivity in the barrel cortex
Feldmeyer, D. (2012) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2012.00024 · Cited by 298 · see citing works
Stress-induced activation of nitric oxide-producing neurons in the rat brain
Krukoff, T. L., & Khalili, P. (1997) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19970127)377:4 · Cited by 167 · see citing works
Connectomic comparison of mouse and human cortex
Loomba, S., Straehle, J., Gangadharan, V., Heike, N., Khalifa, A., Motta, A., Ju, N., Sievers, M., Gempt, J., Meyer, H. S., et al. (2022) · Science · doi:10.1126/science.abo0924 · Cited by 242 · see citing works
Geometric and functional organization of cortical circuits
Shepherd, G. M., Stepanyants, A., Bureau, I., Chklovskii, D. B., & Svoboda, K. (2005) · Nature Neuroscience · doi:10.1038/nn1447 · Cited by 257 · see citing works
Inhibitory interneurons in a cortical column form hot zones of inhibition in layers 2 and 5A
Meyer, H. S., Schwarz, D., Wimmer, V. C., Schmitt, A. C., Kerr, J. N. D., Sakmann, B., & Helmstaedter, M. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1113648108 · Cited by 254 · see citing works
Major defects in neocortical GABAergic inhibitory circuits in mice lacking the fragile X mental retardation protein
Selby, L., Zhang, C., & Sun, Q.-Q. (2007) · Neuroscience Letters · doi:10.1016/j.neulet.2006.11.062 · Cited by 245 · see citing works
K+Channel Expression Distinguishes Subpopulations of Parvalbumin- and Somatostatin-Containing Neocortical Interneurons
Chow, A., Erişir, A., Farb, C. R., Nadal, M. S., Ozaita, A., Lau, D., Welker, E., & Rudy, B. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-21-09332.1999 · Cited by 238 · see citing works
Ischemia-induced neurogenesis of neocortical layer 1 progenitor cells
Ohira, K., Furuta, T., Hioki, H., Nakamura, K., Kuramoto, E., Tanaka, Y. H., Funatsu, N., Shimizu, K., Oishi, T., Hayashi, M., et al. (2009) · Nature Neuroscience · doi:10.1038/nn.2473 · Cited by 236 · see citing works
Laminar and Columnar Organization of Ascending Excitatory Projections to Layer 2/3 Pyramidal Neurons in Rat Barrel Cortex
Shepherd, G. M. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.1173-05.2005 · Cited by 236 · see citing works
The spatial dimensions of electrically coupled networks of interneurons in the neocortex
Amitai, Y., Gibson, J. R., Beierlein, M., Patrick, S. L., Ho, A. M., Connors, B. W., & Golomb, D. (2002) · The Journal of Neuroscience · doi:10.1523/jneurosci.22-10-04142.2002 · Cited by 235 · see citing works
Effects of diazepam, baclofen and thiopental on the silent period evoked by transcranial magnetic stimulation in humans
Inghilleri, M., Berardelli, A., Marchetti, P., & Manfredi, M. (1996) · Experimental Brain Research · doi:10.1007/bf00229631 · Cited by 217 · see citing works
Perineuronal nets decrease membrane capacitance of peritumoral fast spiking interneurons in a model of epilepsy
Tewari, B. P., Chaunsali, L., Campbell, S. L., Patel, D. C., Goode, A. E., & Sontheimer, H. (2018) · Nature Communications · doi:10.1038/s41467-018-07113-0 · Cited by 208 · see citing works
Hyperexcitability in a Model of Cortical Maldevelopment
Jacobs, K. M., Gutnick, M. J., & Prince, D. A. (1996) · Cerebral Cortex · doi:10.1093/cercor/6.3.514 · Cited by 207 · see citing works
Local circuit neurons in the medial prefrontal cortex (areas 24a,b,c, 25 and 32) in the monkey: I. Cell morphology and morphometrics
Gabbott, P. L. A., & Bacon, S. J. (1996) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19960122)364:4 · Cited by 165 · see citing works
The neocortical microcircuit as a tabula rasa
Kalisman, N., Silberberg, G., & Markram, H. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0407088102 · Cited by 201 · see citing works
Cortical and Clonal Contribution of Tbr2 Expressing Progenitors in the Developing Mouse Brain
Vasistha, N. A., García-Moreno, F., Arora, S., Cheung, A. F. P., Arnold, S. J., Robertson, E. J., & Molnár, Z. (2015) · Cerebral Cortex · doi:10.1093/cercor/bhu125 · Cited by 177 · see citing works
“Further, among neurons, ∼25% is constituted by GABAergic interneurons with excitatory cells making the majority of cells (Ren et al. 1992).”
Background
Microglia and astrocytes in the adult rat brain: comparative immunocytochemical analysis demonstrates the efficacy of lipocortin 1 immunoreactivity
Savchenko, V. L., McKanna, J. A., Nikonenko, I., & Skibo, G. G. (2000) · Neuroscience · doi:10.1016/s0306-4522(99)00538-2 · Cited by 168 · see citing works
Experience-dependent development of perineuronal nets and chondroitin sulfate proteoglycan receptors in mouse visual cortex
Ye, Q., & Miao, Q.-L. (2013) · Matrix Biology · doi:10.1016/j.matbio.2013.04.001 · Cited by 146 · see citing works
Mapping functional connectivity in barrel-related columns reveals layer- and cell type-specific microcircuits
Schubert, D., Kötter, R., & Staiger, J. F. (2007) · Brain Structure and Function · doi:10.1007/s00429-007-0147-z · Cited by 147 · see citing works
Brain-derived neurotrophic factor mediates activity-dependent dendritic growth in nonpyramidal neocortical interneurons in developing organotypic cultures
Jin, X., Hu, H., Mathers, P. H., & Agmon, A. (2003) · The Journal of Neuroscience · doi:10.1523/jneurosci.23-13-05662.2003 · Cited by 137 · see citing works
Refined protocols of tamoxifen injection for inducible DNA recombination in mouse astroglia
Jahn, H. M., Kasakow, C. V., Helfer, A. G., Michely, J. A., Verkhratsky, A., Maurer, H. H., Scheller, A., & Kirchhoff, F. (2018) · Scientific Reports · doi:10.1038/s41598-018-24085-9 · Cited by 126 · see citing works
Connectivity of GABAergic Calretinin-immunoreactive Neurons in Rat Primary Visual Cortex
Gonchar, Y. (1999) · Cerebral Cortex · doi:10.1093/cercor/9.7.683 · Cited by 117 · see citing works
Comparative density of CCK- and PV-GABA cells within the cortex and hippocampus
Whissell, P. D., Cajanding, J. D., Fogel, N., & Kim, J. C. (2015) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2015.00124 · Cited by 118 · see citing works
Laminar fate of cortical GABAergic interneurons is dependent on both birthdate and phenotype
Rymar, V. V., & Sadikot, A. F. (2007) · The Journal of Comparative Neurology · doi:10.1002/cne.21250 · Cited by 116 · see citing works
Parvalbumin‐containing neurons, perineuronal nets and experience‐dependent plasticity in murine barrel cortex
Nowicka, D., Soulsby, S., Skangiel‐Kramska, J., & Glazewski, S. (2009) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2009.06996.x · Cited by 110 · see citing works
Stereotypy in neocortical microcircuits
Silberberg, G., Gupta, A., & Markram, H. (2002) · Trends in Neurosciences · doi:10.1016/s0166-2236(02)02151-3 · Cited by 117 · see citing works
Quantitative analysis of GABA-like-immunoreactive and parvalbumin-containing neurons in the CA1 region of the rat hippocampus using a stereological method, the disector
Aika, Y., Ren, J., Kosaka, K., & Kosaka, T. (1994) · Experimental Brain Research · doi:10.1007/bf00239593 · Cited by 115 · see citing works
Self-citation
A study of SMI 32‐stained pyramidal cells, parvalbumin‐immunoreactive chandelier cells, and presumptive thalamocortical axons in the human temproal neocortex
del Rı́o, M. R., & DeFelipe, J. (1994) · The Journal of Comparative Neurology · doi:10.1002/cne.903420307 · Cited by 108 · see citing works
Overexpression of p27Kip1, Probability of Cell Cycle Exit, and Laminar Destination of Neocortical Neurons
Tarui, T., Takahashi, T., Nowakowski, R. S., Hayes, N. L., Bhide, P. G., & Caviness, V. S. (2005) · Cerebral Cortex · doi:10.1093/cercor/bhi017 · Cited by 106 · see citing works
Brief Bursts Self-Inhibit and Correlate the Pyramidal Network
Berger, T. K., Silberberg, G., Perin, R., & Markram, H. (2010) · PLoS Biology · doi:10.1371/journal.pbio.1000473 · Cited by 108 · see citing works
Combinations of AMPA Receptor Subunit Expression in Individual Cortical Neurons Correlate with Expression of Specific Calcium-Binding Proteins
Kondo, M., Sumino, R., & Okado, H. (1997) · Journal of Neuroscience · doi:10.1523/jneurosci.17-05-01570.1997 · Cited by 104 · see citing works
Bone marrow: a possible alternative source of cells in the adult nervous system
Mezey, É., & Chandross, K. J. (2000) · European Journal of Pharmacology · doi:10.1016/s0014-2999(00)00561-6 · Cited by 100 · see citing works
Excitatory and inhibitory neurons express c-Fos in barrel-related columns after exploration of a novel environment
Staiger, J. F., Masanneck, C., Bisler, S., Schleicher, A., Zuschratter, W., & Zilles, K. (2002) · Neuroscience · doi:10.1016/s0306-4522(01)00501-2 · Cited by 96 · see citing works
Inter- and Intralaminar Subcircuits of Excitatory and Inhibitory Neurons in Layer 6a of the Rat Barrel Cortex
Kumar, P. A., & Ohana, O. (2008) · Journal of Neurophysiology · doi:10.1152/jn.90684.2008 · Cited by 90 · see citing works
Computational Modeling of Distinct Neocortical Oscillations Driven by Cell-Type Selective Optogenetic Drive: Separable Resonant Circuits Controlled by Low-Threshold Spiking and Fast-Spiking Interneurons
Vierling-Claassen, D., Cardin, J. A., Moore, C. I., & Jones, S. R. (2010) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2010.00198 · Cited by 86 · see citing works
Critical Time Window of Neuronal Cholesterol Synthesis during Neurite Outgrowth
Fünfschilling, U., Jockusch, W. J., Sivakumar, N., Möbius, W., Corthals, K., Li, S., Quintes, S., Kim, Y., Schaap, I. A. T., Rhee, J., et al. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.1352-11.2012 · Cited by 90 · see citing works
mRNA expression of AMPA receptors and AMPA receptor binding proteins in the cerebral cortex of elderly schizophrenics
Dracheva, S. M., McGurk, S. R., & Haroutunian, V. H. (2005) · Journal of Neuroscience Research · doi:10.1002/jnr.20423 · Cited by 84 · see citing works
Minimum neuron density for synchronized bursts in a rat cortical culture on multi-electrode arrays
Ito, D., Tamate, H., Nagayama, M., Uchida, T., Kudoh, S. N., & Gohara, K. (2010) · Neuroscience · doi:10.1016/j.neuroscience.2010.08.038 · Cited by 80 · see citing works
Cortical Orofacial Motor Representation in Old World Monkeys, Great Apes, and Humans
Sherwood, C. C., Holloway, R. L., ERWIN, J. M., Schleicher, A., Zilles, K., & Hof, P. R. (2003) · Brain Behavior and Evolution · doi:10.1159/000075672 · Cited by 79 · see citing works
Impact of Altered Cholinergic Tones on the Neurovascular Coupling Response to Whisker Stimulation
Lecrux, C., Sandoe, C. H., Neupane, S., Kropf, P., Toussay, X., Tong, X., Lacalle‐Aurioles, M., Shmuel, A., & Hamel, É. (2017) · Journal of Neuroscience · doi:10.1523/jneurosci.1784-16.2016 · Cited by 75 · see citing works
Thalamocortical specificity and the synthesis of sensory cortical receptive fields
Alonso, J.-M., & Swadlow, H. A. (2005) · Journal of Neurophysiology · doi:10.1152/jn.01281.2004 · Cited by 73 · see citing works
Postnatal Development of GABA Neurons in the Rat Somatosensory Barrel Cortex: A Quantitative Study
Micheva, K. D., & Beaulieu, C. (1995) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.1995.tb00338.x · Cited by 70 · see citing works
Neocortical calretinin neurons in primates: increase in proportion and microcircuitry structure
aja, D. D. ⁄., Hladnik, A., Bičanić, I., BakoviÄ‡, M., & Petanjek, Z. (2014) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2014.00103 · Cited by 69 · see citing works
Metabotropic Glutamate Receptor Type 5-Dependent Long-Term Potentiation of Excitatory Synapses on Fast-Spiking GABAergic Neurons in Mouse Visual Cortex
Sarihi, A., Jiang, B., Komaki‬, A., Sohya, K., Yanagawa, Y., & Tsumoto, T. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.4928-07.2008 · Cited by 68 · see citing works
Effects of neonatal freeze lesions on expression of parvalbumin in rat neocortex
Rosen, G. D. (1998) · Cerebral Cortex · doi:10.1093/cercor/8.8.753 · Cited by 69 · see citing works
Untitled work
Fashena, D. (1999) · doi:10.1002/(sici)1096-9861(19990412)406:3
A claim in search of evidence: reply to Manger’s thermogenesis hypothesis of cetacean brain structure
Marino, L., Butti, C., Connor, R. C., Fordyce, R. E., Herman, L. M., Hof, P. R., Lefebvre, L., Lusseau, D., McCowan, B., Nimchinsky, E. A., et al. (2008) · Biological reviews/Biological reviews of the Cambridge Philosophical Society · doi:10.1111/j.1469-185x.2008.00049.x · Cited by 65 · see citing works
Total Number and Ratio of GABAergic Neuron Types in the Mouse Lateral and Basal Amygdala
Vereczki, V., Müller, K., Krizsán, É., Máté, Z., Fekete, Z., Rovira-Esteban, L., Veres, J. M., Erdélyi, F., & Hájos, N. (2021) · Journal of Neuroscience · doi:10.1523/jneurosci.2700-20.2021 · Cited by 60 · see citing works
GABA-immunopositive neurons in rat neocortex with contralateral projections to S-I
Gonchar, Y., Johnson, P. B., & Weinberg, R. J. (1995) · Brain Research · doi:10.1016/0006-8993(95)00746-d · Cited by 59 · see citing works
Reduction of GABAA receptor binding of [3H]muscimol in the barrel field of mice after peripheral denervation: transient and long-lasting effects
Skangiel-Kramska, J., Glazewski, S., Jabłońska, B., Siucińska, E., & Kossut, M. M. (1994) · Experimental Brain Research · doi:10.1007/bf00227277 · Cited by 59 · see citing works
Preliminary clinical observations on a new trigeminal reflex
Lazzaro, V. D., Restuccia, D., Nardone, R., Tartaglione, T., Quartarone, A., Tonali, P., & Rothwell, J. C. (1996) · Neurology · doi:10.1212/wnl.46.2.479 · Cited by 56 · see citing works
Local circuits targeting parvalbumin-containing interneurons in layer IV of rat barrel cortex
Staiger, J. F., Zuschratter, W., Luhmann, H. J., & Schubert, D. (2009) · Brain Structure and Function · doi:10.1007/s00429-009-0225-5 · Cited by 55 · see citing works
Dense Neuron Clustering Explains Connectivity Statistics in Cortical Microcircuits
Klinshov, V. V., Teramae, J.-N., Nekorkin, V. I., & Fukai, T. (2014) · PLoS ONE · doi:10.1371/journal.pone.0094292 · Cited by 52 · see citing works
Distribution of microglia and astrocytes in different regions of the normal adult rat brain
Savchenko, V. L., Nikonenko, I., Skibo, G. G., & McKanna, J. A. (1997) · Neurophysiology · doi:10.1007/bf02463354 · Cited by 51 · see citing works
Characterization of thalamocortical responses of regular-spiking and fast-spiking neurons of the mouse auditory cortex in vitro and in silico
Schiff, M. L., & Reyes, A. D. (2012) · Journal of Neurophysiology · doi:10.1152/jn.00208.2011 · Cited by 48 · see citing works
Characterization and Distribution of Reelin-Positive Interneuron Subtypes in the Rat Barrel Cortex
Pohlkamp, T., Dávid, C., Cauli, B., Gallopin, T., Bouché, E., Karagiannis, A., May, P., Herz, J., Frotscher, M., Staiger, J. F., et al. (2013) · Cerebral Cortex · doi:10.1093/cercor/bht161 · Cited by 47 · see citing works
Evaluation of in vitro neuronal platforms as surrogates for in vivo whole brain systems
Belle, A. M., Enright, H. A., Sales, A. P., Kulp, K. S., Osburn, J. J., Kuhn, E. A., Fischer, N. O., & Wheeler, E. K. (2018) · Scientific Reports · doi:10.1038/s41598-018-28950-5 · Cited by 45 · see citing works
Secretagogin is Expressed by Developing Neocortical GABAergic Neurons in Humans but not Mice and Increases Neurite Arbor Size and Complexity
Raju, C. S., Spatazza, J., Stanco, A., Larimer, P., Sorrells, S. F., Kelley, K. W., Nicholas, C. R., Paredes, M. F., Lui, J. H., Hasenstaub, A. R., et al. (2017) · Cerebral Cortex · doi:10.1093/cercor/bhx101 · Cited by 44 · see citing works
Long‐lasting dysregulation of gene expression in corticostriatal circuits after repeated cocaine treatment in adult rats: effects on zif 268 and homer 1a
Ünal, Ç. T., Beverley, J. A., Willuhn, I., & Steiner, H. (2009) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2009.06691.x · Cited by 43 · see citing works
GABA immunoreactivity in mouse barrel field after aversive and appetitive classical conditioning training involving facial vibrissae
Siucińska, E., Kossut, M. M., & Stewart, M. G. (1999) · Brain Research · doi:10.1016/s0006-8993(99)01881-8 · Cited by 43 · see citing works
The use of the optical disector to estimate the number of neurons, glial and endothelial cells in the spinal cord of the mouse — with a comparative note on the rat spinal cord
Bjugn, R. (1993) · Brain Research · doi:10.1016/0006-8993(93)90744-8 · Cited by 40 · see citing works
The onset of parvalbumin‐expression in interneurons of the rat parietal cortex depends upon extrinsic factor(s)
Weisenhorn, D. M. V., Celio, M. R., & Rickmann, M. (1998) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.1998.00120.x · Cited by 39 · see citing works
A quantitative analysis of parvalbumin neurons in rabbit auditory neocortex
McMullen, N. T., Smelser, C. B., & de Venecia, R. K. (1994) · The Journal of Comparative Neurology · doi:10.1002/cne.903490402 · Cited by 38 · see citing works
Prolonged deficits in parvalbumin neuron stimulation-evoked network activity despite recovery of dendritic structure and excitability in the somatosensory cortex following global ischemia in mice.
Xie, Y., Chen, S., Wu, Y., & Murphy, T. H. (2014) · The Journal of Neuroscience · doi:10.1523/jneurosci.1775-14.2014 · Cited by 35 · see citing works
Distribution Patterns of Three Molecularly Defined Classes of GABAergic Neurons Across Columnar Compartments in Mouse Barrel Cortex
Almási, Z., Dávid, C., Witte, M., & Staiger, J. F. (2019) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2019.00045 · Cited by 37 · see citing works
Brain‐derived neurotrophic factor acutely depresses excitatory synaptic transmission to GABAergic neurons in visual cortical slices
Jiang, B., Kitamura, A., Yasuda, H., Sohya, K., Maruyama, A., Yanagawa, Y., Obata, K., & Tsumoto, T. (2004) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2004.03523.x · Cited by 37 · see citing works
Intracellularly labeled pyramidal neurons in the cortical areas projecting to the spinal cord
Cho, R.-H., Segawa, S., Mizuno, A., & Kaneko, T. (2004) · Neuroscience Research · doi:10.1016/j.neures.2004.08.006 · Cited by 37 · see citing works
Optogenetic induction of orbitostriatal long-term potentiation in the dorsomedial striatum elicits a persistent reduction of alcohol-seeking behavior in rats
Cheng, Y., Xie, X., Lu, J., Gangal, H., Wang, W., Melo, S., Wang, X., Jerger, J., Woodson, K., Garr, E., et al. (2021) · Neuropharmacology · doi:10.1016/j.neuropharm.2021.108560 · Cited by 30 · see citing works
Vertical Bias in Dendritic Trees of Non-pyramidal Neocortical Neurons Expressing GAD67-GFP In Vitro
Jin, X., Mathers, P. H., Szabó, G., Katarova, Z., & Agmon, A. (2001) · Cerebral Cortex · doi:10.1093/cercor/11.7.666 · Cited by 31 · see citing works
Interneurons containing somatostatin are affected by learning-induced cortical plasticity
Cybulska-Kłosowicz, A., Posluszny, A., Nowak, K., Siucińska, E., Kossut, M. M., & Liguz‐Lecznar, M. (2013) · Neuroscience · doi:10.1016/j.neuroscience.2013.09.020 · Cited by 30 · see citing works
Brain is modulated by neuronal plasticity during postnatal development
Kourosh‐Arami, M., Hosseini, N., & Komaki‬, A. (2021) · The Journal of Physiological Sciences · doi:10.1186/s12576-021-00819-9 · Cited by 30 · see citing works
The distribution, number, and certain neurochemical identities of infracortical white matter neurons in a lar gibbon ( Hylobates lar ) brain
Swiegers, J., Bhagwandin, A., Sherwood, C. C., Bertelsen, M. F., Maseko, B. C., Hemingway, J., Rockland, K. S., Molnár, Z., & Manger, P. R. (2018) · The Journal of Comparative Neurology · doi:10.1002/cne.24545 · Cited by 31 · see citing works
Gap Junctions Interconnect Different Subtypes of Parvalbumin-Positive Interneurons in Barrels and Septa with Connectivity Unique to Each Subtype
Shigematsu, N., Nishi, A., & Fukuda, T. (2018) · Cerebral Cortex · doi:10.1093/cercor/bhy038 · Cited by 29 · see citing works
Regional density of glial cells in the rat corpus callosum
Reyes‐Haro, D., Mora-Loyola, E., Soria-Ortiz, B., & García‐Colunga, J. (2013) · Biological Research · doi:10.4067/s0716-97602013000100004 · Cited by 26 · see citing works
Intracellularly labeled pyramidal neurons in the cortical areas projecting to the spinal cord
Cho, R.-H., Segawa, S., Okamoto, K., Mizuno, A., & Kaneko, T. (2004) · Neuroscience Research · doi:10.1016/j.neures.2004.08.007 · Cited by 27 · see citing works
Neuronal Avalanches Across the Rat Somatosensory Barrel Cortex and the Effect of Single Whisker Stimulation
Mariani, B., Nicoletti, G., Bisio, M., Maschietto, M., Oboe, R., Leparulo, A., Suweis, S. S., & Vassanelli, S. (2021) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2021.709677 · Cited by 25 · see citing works
Functional properties and short‐term dynamics of unidirectional and reciprocal synaptic connections between layer 2/3 pyramidal cells and fast‐spiking interneurons in juvenile rat prefrontal cortex
Zaitsev, A. V., & Lewis, D. A. (2013) · European Journal of Neuroscience · doi:10.1111/ejn.12294 · Cited by 23 · see citing works
SIMULATING VERTICAL AND HORIZONTAL INHIBITION WITH SHORT-TERM DYNAMICS IN A MULTI-COLUMN MULTI-LAYER MODEL OF NEOCORTEX
Strack, B., Jacobs, K. M., & Cios, K. J. (2014) · International Journal of Neural Systems · doi:10.1142/s0129065714400024 · Cited by 22 · see citing works
Dysregulation of gene induction in corticostriatal circuits after repeated methylphenidate treatment in adolescent rats: differential effects on zif 268 and homer 1a
Cotterly, L. M., Beverley, J. A., Yano, M., & Steiner, H. (2007) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2007.05570.x · Cited by 22 · see citing works
Long nanoneedle-electrode devices for extracellular and intracellular recording in vivo
Kubota, Y., Yamagiwa, S., Sawahata, H., Idogawa, S., Tsuruhara, S., Numano, R., Koida, K., Ishida, M., & Kawano, T. (2017) · Sensors and Actuators B Chemical · doi:10.1016/j.snb.2017.11.152 · Cited by 21 · see citing works
Aspects of the organization of neurons and dendritic bundles in primary somatosensory cortex of the rat
Skoglund, T. S., Pascher, R., & Berthold, C. (2004) · Neuroscience Research · doi:10.1016/j.neures.2004.06.017 · Cited by 21 · see citing works
Pharmacological Tools to Study the Role of Astrocytes in Neural Network Functions
Peña‐Ortega, F., Rivera‐Angulo, A., & Lorea-Hernández, J. J. (2016) · Advances in experimental medicine and biology · doi:10.1007/978-3-319-40764-7_3 · Cited by 21 · see citing works
Contact-associated Neurite Outgrowth and Branching of Immature Cortical Interneurons
Sang, Q. (2003) · Cerebral Cortex · doi:10.1093/cercor/13.6.677 · Cited by 20 · see citing works
Short-term sensory learning does not alter parvalbumin neurons in the barrel cortex of adult mice: A double-labeling study
Siucińska, E., & Kossut, M. M. (2006) · Neuroscience · doi:10.1016/j.neuroscience.2005.11.053 · Cited by 19 · see citing works
Calcium-Binding Protein Phenotype Defines Metabolically Distinct Groups of Neurons in Barrel Cortex of Behaving Hamsters
Maier, D. L., & McCasland, J. S. (1997) · Experimental Neurology · doi:10.1006/exnr.1997.6426 · Cited by 19 · see citing works
A comparison of the distribution of GABA-ergic neurons in cortices representing different sensory modalities
Clemo, H. R., Keniston, L., & Meredith, M. A. (2003) · Journal of Chemical Neuroanatomy · doi:10.1016/s0891-0618(03)00039-5 · Cited by 18 · see citing works
Correlation of the apparent diffusion coefficient and the creatine level in early ischemic stroke: A comparison of different patterns by magnetic resonance
Rumpel, H., Khoo, J. B. K., Chang, H. M., Lim, W. E. H., Chen, C., Wong, M. C., & Tan, K. P. (2001) · Journal of Magnetic Resonance Imaging · doi:10.1002/jmri.1048 · Cited by 18 · see citing works
Inducing gene expression in barrel cortex - focus on immediate early genes
Filipkowski, R. K. (2000) · Acta Neurobiologiae Experimentalis · doi:10.55782/ane-2000-1360 · Cited by 16 · see citing works

Stereological Analysis of GABAergic Neurons and Calcium Binding Protein Parvalbumin-containing Neurons in the Rat Somatosensory Cortex
Ren, J. (1991) · QIR (Kyushu University Institutional Repository) (Kyushu University) · doi:10.15017/7393583
Self-citation
Quantitative analysis of GABA-like-immunoreactive and parvalbumin-containing neurons in the CA1 region of the rat hippocampus using a stereological method, the disector
Aika, Y., Ren, J., Kosaka, K., & Kosaka, T. (1994) · Experimental Brain Research · doi:10.1007/bf00239593 · Cited by 115 · see citing works
Self-citation
Numerical data on neocortical neurons in adult rat, with special reference to the GABA population
Beaulieu, C. (1993) · Brain Research · doi:10.1016/0006-8993(93)90884-p · Cited by 301 · see citing works
A quantitative analysis of parvalbumin neurons in rabbit auditory neocortex
McMullen, N. T., Smelser, C. B., & de Venecia, R. K. (1994) · The Journal of Comparative Neurology · doi:10.1002/cne.903490402 · Cited by 38 · see citing works
γ-Aminobutyric acid (GABA) immunoreactivity in mouse and rat first somatosensory (SI) cortex: description and comparison
Chmielowska, J., Stewart, M. G., & Bourne, R. C. (1988) · Brain Research · doi:10.1016/0006-8993(88)91472-2 · Cited by 36 · see citing works

Authors: Ren, J. Q., Aika, Y., Heizmann, C. W., & Kosaka, T.
Affiliations: Kyushu University (JP)
University of Zurich (CH)
Venue: Experimental Brain Research
Publisher: Springer Science and Business Media LLC
Published: 1992-12
Volume: 92
Issue: 1
Pages: 1-14
ISSN: 0014-4819 (ISSN-L)
1432-1106
DOI: 10.1007/bf00230378
OpenAlex: W2086657106
Cited by: 148
References: 38
Citations by year: 2026: 3 · 2025: 1 · 2024: 4 · 2022: 3 · 2021: 6 · 2020: 2 · 2019: 6 · 2018: 8 · 2017: 4 · 2016: 4 · 2015: 3 · 2014: 8 · 2013: 6 · 2012: 3
FWCI: 0.95
Type: journal article
Language: en
Open access: closed
Licence: www.springer.com/tdm (tdm)
Locations: Experimental Brain Research (publishedVersion)
PubMed (publishedVersion)
Topics: Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
Keywords: somatosensory cortex, barrel cortex, GABAergic neurons, parvalbumin neurons, S100β, astrocytes, oligodendrocytes, microglia, neuronal density, glial density, laminar distribution, cell types, rat brain, stereology, immunocytochemistry
MeSH terms: Animals, gamma-Aminobutyric Acid, Immunohistochemistry, Male, Neuroglia, Neurons, Oxazines, Parvalbumins, Somatosensory Cortex, Tolonium Chloride, Plastic Embedding, Rats, Wistar, Benzoxazines, Rats

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review

Quantitative analysis of neurons and glial cells in the rat somatosensory cortex, with special reference to GABAergic neurons and parvalbumin-containing neurons

Abstract

Integrity signals

Claims the paper makes

Claims other papers make about this one

Cites

Cited by

Related

Record

About these checks