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Diffuse perineuronal nets and modified pyramidal cells immunoreactive for glutamate and the GABAA receptor α1 subunit form a unique entity in rat cerebral cortex
Abstract
Perineuronal nets (PNs) consisting of polyanionic chondroitin sulfate proteoglycans (CSPG) and other extracellular matrix components create an exceptional microenvironment around certain types of neurons. In rat neocortex, three types of PNs can be distinguished after staining with Wisteria floribunda agglutinin (WFA) by their different morphological structure: lattice-like PNs associated with subpopulations of nonpyramidal neurons, weakly labeled PNs showing a pyramidal morphology, and diffuse PNs that possess a thick, strongly labeled matrix sheath located mainly in layer VIb above the white matter. The type of neuron surrounded by diffuse nets has not been described so far. This study is focused on the cytochemical and morphological characteristics of neurons associated with diffusely contoured PNs in rat parietal cortex using immunocytochemical staining, intracellular injection, and retrograde tracing methods. Cells surrounded by diffuse PNs were glutamate-immunoreactive in contrast to nonpyramidal, net-associated neurons that showed immunoreactivity for GABA, the calcium-binding protein parvalbumin and the potassium channel subunit Kv3.1b. Both groups of PN-ensheathed cells were mostly immunoreactive for the GABA(A) receptor alpha1 subunit. Lucifer Yellow-injected neurons surrounded by diffuse PNs displayed the morphological properties of modified pyramidal cells with intracortical main axons. Many neurons with diffuse PNs were retrogradely labeled over a long distance after Fluoro-Gold tracer injection in the parietal cortex, but remained unlabeled after intrathalamic injection. We conclude that neurons associated with diffuse PNs are a subpopulation of glutamatergic modified pyramidal cells that could act as excitatory long-range intracortically projecting neurons.
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“PNNs surround inhibitory fast spiking parvalbumin-positive GABAergic interneurons12–14, but are also associated with further subpopulations, for example excitatory pyramidal neurons in the cerebral cortex15,16.”
From Elimination of the four extracellular matrix molecules tenascin-C, tenascin-R, brevican and neurocan alters the ratio of excitatory and inhibitory synapses (2019) · cites this paper as [16]
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“Other cell types, including putative excitatory neurons also contain PNNs but they are less numerous compared to GABAergic-PNN expressing cells (Wegner et al., 2003).”
From The Perineuronal ‘Safety’ Net? Perineuronal Net Abnormalities in Neurological Disorders (2018) · cites this paper as Wegner et al., 2003
Citations
Cites
The rat brain in stereotaxic coordinates
Palkovits, M. (1983) · Neuropeptides · doi:10.1016/0143-4179(83)90049-5 · Cited by 28,959
The Rat Brain in Stereotaxic Coordinates
Paxinos, G., & Watson, C. (1983) · Elsevier eBooks · doi:10.1016/c2009-0-63235-9 · Cited by 28,585
Macdonald, R. L., & Olsen, R. W. (1994) · Annual Review of Neuroscience · doi:10.1146/annurev.ne.17.030194.003033 · Cited by 1,975
Reactivation of Ocular Dominance Plasticity in the Adult Visual Cortex
Pizzorusso, T., Medini, P., Berardi, N., Chierzi, S., Fawcett, J. W., & Maffei, L. (2002) · Science · doi:10.1126/science.1072699 · Cited by 1,679
GABAergic cell subtypes and their synaptic connections in rat frontal cortex
Kawaguchi, Y. (1997) · Cerebral Cortex · doi:10.1093/cercor/7.6.476 · Cited by 1,416
Fritschy, J., & Mohler, H. (1995) · Journal of Comparative Neurology · doi:10.1002/cne.903590111 · Cited by 1,244
Organizing principles for a diversity of GABAergic interneurons and synapses in the neocortex
Gupta, A., Wang, Y., & Markram, H. (2000) · Science · doi:10.1126/science.287.5451.273 · Cited by 1,036
Peters, A., & Vaughan, D. W. (1981) · Springer eBooks · doi:10.1007/978-1-4684-3929-8_1 · Cited by 900
Molecular and Physiological Diversity of Cortical Nonpyramidal Cells
Cauli, B., Audinat, E., Lambolez, B., Angulo, M. C., Ropert, N., Tsuzuki, K., Hestrin, S., & Rossier, J. (1997) · Journal of Neuroscience · doi:10.1523/jneurosci.17-10-03894.1997 · Cited by 738
Kawaguchi, Y. (1995) · The Journal of Neuroscience · doi:10.1523/jneurosci.15-04-02638.1995 · Cited by 533
Perineuronal nets: past and present
Celio, M. R., Spreafico, R., De Biasi, S., & Vitellaro-Zuccarello, L. (1998) · Trends in Neurosciences · doi:10.1016/s0166-2236(98)01298-3 · Cited by 497
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
Interlaminar Connections in the Neocortex
Thomson, A. M. (2002) · Cerebral Cortex · doi:10.1093/cercor/13.1.5 · Cited by 468
Wisteria floribunda agglutinin-labelled nets surround parvalbumin-containing neurons
Härtig, W., Brauer, K., & Brückner, G. (1992) · NeuroReport · doi:10.1097/00001756-199210000-00012 · Cited by 440
Self-citationMonoclonal antibodies directed against the calcium binding protein parvalbumin
Celio, M. R., Baier, W. K., Schärer, L., de Viragh, P. A., & Gerday, C. (1988) · Cell Calcium · doi:10.1016/0143-4160(88)90027-9 · Cited by 423
Oertel, W., Schmechel, D. E., Tappaz, M., & Kopin, I. J. (1981) · Neuroscience · doi:10.1016/0306-4522(81)90113-5 · Cited by 419
Perineuronal nets — a specialized form of extracellular matrix in the adult nervous system
Celio, M. R., & Blümcke, I. (1994) · Brain Research Reviews · doi:10.1016/0165-0173(94)90006-x · Cited by 386
Kawaguchi, Y., & Kubota, Y. (1996) · The Journal of Neuroscience · doi:10.1523/jneurosci.16-08-02701.1996 · Cited by 380
DeFelipe, J. (1993) · Cerebral Cortex · doi:10.1093/cercor/3.4.273 · Cited by 365
Brückner, G., Brauer, K., Härtig, W., Wolff, J. R., Rickmann, M. J., Derouiche, A., Delpech, B., Girard, N., Oertel, W. H., & Reichenbach, A. (1993) · Glia · doi:10.1002/glia.440080306 · Cited by 358
Self-citationFast-spike Interneurons and Feedforward Inhibition in Awake Sensory Neocortex
Swadlow, H. A. (2002) · Cerebral Cortex · doi:10.1093/cercor/13.1.25 · Cited by 354
Aggrecan Glycoforms Contribute to the Molecular Heterogeneity of Perineuronal Nets
Matthews, R. T., Kelly, G. M., Zerillo, C. A., Gray, G., Tiemeyer, M., & Hockfield, S. (2002) · The Journal of Neuroscience · doi:10.1523/jneurosci.22-17-07536.2002 · Cited by 341
Härtig, W., Derouiche, A., Welt, K., Brauer, K., Grosche, J., Mäder, M., Reichenbach, A., & Brückner, G. (1999) · Brain Research · doi:10.1016/s0006-8993(99)01784-9 · Cited by 339
Self-citationKawaguchi, Y., & Kubota, Y. (1998) · Neuroscience · doi:10.1016/s0306-4522(97)00685-4 · Cited by 296
Zhang, Z., & Deschênes, M. (1997) · Journal of Neuroscience · doi:10.1523/jneurosci.17-16-06365.1997 · Cited by 279
Monoclonal antibodies directed against the calcium binding protein Calbindin D-28k
Celio, M. R., Baier, W. K., Schärer, L., Gregersen, H.-J., de Viragh, P. A., & Norman, A. W. (1990) · Cell Calcium · doi:10.1016/0143-4160(90)90014-l · Cited by 273
Hockfield, S., Kalb, R. G., Zaremba, S., & Fryer, H. (1990) · Cold Spring Harbor Symposia on Quantitative Biology · doi:10.1101/sqb.1990.055.01.049 · Cited by 271
Schwaller, B., Buchwald, P., Blümcke, I., Celio, M. R., & Hunziker, W. H. (1993) · Cell Calcium · doi:10.1016/0143-4160(93)90089-o · Cited by 255
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
Klausberger, T., Roberts, J. D. B., & Somogyi, P. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-07-02513.2002 · Cited by 234
Structure and Pharmacology of Vertebrate GABAA Receptor Subtypes
Whiting, P. J., McKernan, R. M., & Wafford, K. A. (1995) · International review of neurobiology · doi:10.1016/s0074-7742(08)60525-5 · Cited by 211
Hendry, S., Jones, E. G., Hockfield, S. J., & McKay, R. D. G. (1988) · Journal of Neuroscience · doi:10.1523/jneurosci.08-02-00518.1988 · Cited by 205
Brückner, G., Hausen, D., Härtig, W., Drlicek, M., Arendt, T., & Brauer, K. (1999) · Neuroscience · doi:10.1016/s0306-4522(99)00071-8 · Cited by 196
Self-citationLander, C., Kind, P., Maleski, M., & Hockfield, S. (1997) · The Journal of Neuroscience · doi:10.1523/jneurosci.17-06-01928.1997 · Cited by 195
Morphology of Golgi‐Cox‐impregnated barrel neurons in rat SmI cortex
Simons, D. J., & Woolsey, T. A. (1984) · Journal of Comparative Neurology · doi:10.1002/cne.902300111 · Cited by 175
Gall, C. M. (1988) · Journal of Neuroscience · doi:10.1523/jneurosci.08-06-01852.1988 · Cited by 157
Kosaka, T., & Heizmann, C. W. (1989) · Brain Research · doi:10.1016/0006-8993(89)90048-6 · Cited by 153
Ha¨rtig, W., Brauer, K., Bigl, V., & Bru¨ckner, G. (1994) · Brain Research · doi:10.1016/0006-8993(94)91452-4 · Cited by 147
Self-citationBrückner, G., Seeger, G., Brauer, K., Härtig, W., Kacza, J., & Bigl, V. (1994) · Brain Research · doi:10.1016/s0006-8993(09)90012-9 · Cited by 132
Self-citationDistinct Firing Patterns of Neuronal Subtypes in Cortical Synchronized Activities
Kawaguchi, Y. (2001) · Journal of Neuroscience · doi:10.1523/jneurosci.21-18-07261.2001 · Cited by 123
Extracellular matrix organization in various regions of rat brain grey matter
Brückner, G., Härtig, W., Kacza, J., Seeger, J., Welt, K., & Brauer, K. (1996) · Journal of Neurocytology · doi:10.1007/bf02284806 · Cited by 109
Self-citationKöppe, G., Brückner, G., Härtig, W., Delpech, B., & Bigl, V. (1997) · The Histochemical Journal · doi:10.1023/a:1026408716522 · Cited by 100
Self-citationMorris, N. P., & Henderson, Z. (2000) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2000.00970.x · Cited by 98
Naegele, J. R., & Katz, L. C. (1990) · Journal of Neuroscience · doi:10.1523/jneurosci.10-02-00540.1990 · Cited by 88
Naegele, J. R., Arimatsu, Y., Schwartz, P. M., & Barnstable, C. J. (1988) · Journal of Neuroscience · doi:10.1523/jneurosci.08-01-00079.1988 · Cited by 88
The LectinVicia VillosaLabels a Distinct Subset of GABAergic Cells in Macaque Visual Cortex
Mulligan, K. A., van Brederode, J. F. M., & Hendrickson, A. E. (1989) · Visual Neuroscience · doi:10.1017/s0952523800004338 · Cited by 82
Morino-Wannier, P., Fujita, S. C., & Jones, E. G. (1992) · Experimental Brain Research · doi:10.1007/bf02259117 · Cited by 81
Kosaka, T., Isogai, K., Barnstable, C. J., & Heizmann, C. W. (1990) · Experimental Brain Research · doi:10.1007/bf00228797 · Cited by 79
Nakagawa, F., Schulte, B. A., Wu, J. Y., & Spicer, S. S. (1986) · Journal of Neurocytology · doi:10.1007/bf01611440 · Cited by 67
Härtig, W., Singer, A., Grosche, J., Brauer, K., Ottersen, O. P., & Brückner, G. (2001) · Brain Research · doi:10.1016/s0006-8993(01)02211-9 · Cited by 62
Self-citationIn vivo and in vitro labelling of perineuronal nets in rat brain
Brückner, G., Bringmann, A., Köppe, G., Härtig, W., & Brauer, K. (1996) · Brain Research · doi:10.1016/0006-8993(96)00152-7 · Cited by 62
Self-citationPyramidal cells ensheathed by perineuronal nets in human motor and somatosensory cortex
Hausen, D., Brückner, G., Drlicek, M., Härtig, W., Brauer, K., & Bigl, V. (1996) · NeuroReport · doi:10.1097/00001756-199607290-00006 · Cited by 59
Self-citationFreeing the Brain from the Perineuronal Net
Fox, K. D., & Caterson, B. (2002) · Science · doi:10.1126/science.1079224 · Cited by 57
Ericson, A., Blomqvist, A. G., Craig, A. D., Ottersen, O. P., & Broman, J. (1995) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.1995.tb01066.x · Cited by 57
Neuronal composition and morphology in layer IV of two vibrissal barrel subfields of rat cortex
Elston, G. N., Pow, D. V., & Calford, M. B. (1997) · Cerebral Cortex · doi:10.1093/cercor/7.5.422 · Cited by 56
Relationship between astrocytic processes and “perineuronal nets” in rat neocortex.
Blümcke, I., Eggli, P., & Celio, M. R. (1995) · Glia · doi:10.1002/glia.440150205 · Cited by 53
Okamoto, M., Mori, S., Ichimura, M., & Endô, H. (1994) · Neuroscience Letters · doi:10.1016/0304-3940(94)90660-2 · Cited by 52
Structural and cytochemical features of perineuronal glial nets in the rat brain
Brauer, K., Brückner, G., Leibnitz, L., & Werner, L. (1984) · Acta Histochemica · doi:10.1016/s0065-1281(84)80026-4 · Cited by 51
Self-citationSchüppel, K., Brauer, K., Härtig, W., Grosche, J., Earley, B., Leonard, B. E., & Brückner, G. (2002) · Brain Research · doi:10.1016/s0006-8993(02)03569-2 · Cited by 47
Self-citationDistribution of cat‐301 immunoreactivity in the frontal and parietal lobes of the macaque monkey
McGuire, P. K., Hockfield, S. J., & Goldman, P. S. (1989) · The Journal of Comparative Neurology · doi:10.1002/cne.902880207 · Cited by 45
Yang, H.-W., Appenteng, K., & Batten, T. F. C. (1997) · Experimental Brain Research · doi:10.1007/pl00005627 · Cited by 44
Hobohm, C., Härtig, W., Brauer, K., & Brückner, G. (1998) · Journal of Chemical Neuroanatomy · doi:10.1016/s0891-0618(98)00044-1 · Cited by 41
Self-citationEffects of ion channel activity on development of dorsal root ganglion neurons
Fields, R. D. (1998) · Journal of Neurobiology · doi:10.1002/(sici)1097-4695(199810)37:1 · Cited by 40
Dupuy, S. T., & Houser, C. R. (1997) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19971222)389:3 · Cited by 38
Derouiche, A., Härtig, W., Brauer, K., & Brückner, G. (1996) · PubMed · Cited by 35
Self-citationNeuropeptide Y System of the Female Monkey Hypothalamus: Retrograde Tracing and Immunostaining
Thind, K. K., Boggan, J. E., & Goldsmith, P. C. (2008) · Neuroendocrinology · doi:10.1159/000126371 · Cited by 26
Pascual, M., Acsády, L., Rocamora, N., Freund, T. F., & Soriano, E. (1999) · Neuroscience · doi:10.1016/s0306-4522(98)00391-1 · Cited by 23
Ojima, H., Sakai, M., & Ohyama, J. (1998) · Brain Research · doi:10.1016/s0006-8993(97)01564-3 · Cited by 19
Proteoglycans in Perineuronal Nets.
Matsui, F., Nishizuka, M., & Oohira, A. (1999) · ACTA HISTOCHEMICA ET CYTOCHEMICA · doi:10.1267/ahc.32.141 · Cited by 19
Ojima, H. (1993) · Journal of Chemical Neuroanatomy · doi:10.1016/0891-0618(93)90035-3 · Cited by 9
Campos‐Ortega, J. A., & Hartenstein, V. (1997) · Springer eBooks · doi:10.1007/978-3-662-22489-2_11 · Cited by 7
Postnatal development of perineuronal nets in wild-type mice and in a mutant deficient in tenascin-R
Br�ckner, G., Grosche, J., Schmidt, S., H�rtig, W., Margolis, R. U., Delpech, B., Seidenbecher, C. I., Czaniera, R., & Schachner, M. (2000) · The Journal of Comparative Neurology · doi:10.1002/1096-9861(20001225)428:4
Self-citationHagihara (1999) · doi:10.1002/(sici)1096-9861(19990726)410:2
Research works printed but not linked: 3
- Benke, 1991, Ubiquitous presence of GABAA-receptors containing the α1-subunit in rat brain demonstrated by immunoprecipitation and immunohistochemistry, Mol. Neuropharmacol., 1, 103
- Golgi, 1893, Intorno all'origine del quarto nervo cerebrale e una questione isto-fisiologica che a questo argomento si collega, Rend. R. Accad. Lincei (21 maggio), 2, 443
- Härtig, 1999, Cortical neurons immunoreactive for the potassium channel Kv3.1b subunit are predominantly surrounded by perineuronal nets presumed as a buffering system for cations, Brain Res., 842, 15, 10.1016/S0006-8993(99)01784-9 · DOI · Paper page
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Casting a Wide Net: Role of Perineuronal Nets in Neural Plasticity
Sorg, B. A., Berretta, S., Blacktop, J. M., Fawcett, J. W., Kitagawa, H., Kwok, J. C. F., & Miquel, M. (2016) · The Journal of Neuroscience · doi:10.1523/jneurosci.2351-16.2016 · Cited by 454
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Metadata
- Authors
- Wegner, F., Härtig, W., Bringmann, A., Grosche, J., Wohlfarth, K., Zuschratter, W., & Brückner, G.
- Affiliations
- Leipzig University (DE)
- Leibniz Institute for Neurobiology (DE)
- Corresponding author
- Brückner, Gert
- Venue
- Experimental Neurology
- Publisher
- Elsevier BV
- Published
- 2003-12
- Volume
- 184
- Issue
- 2
- Pages
- 705-714
- ISSN
- 0014-4886 (ISSN-L)
- OpenAlex
- W2025692046
- Cited by
- 107
- References
- 74
- Citations by year
- 2026: 2 · 2025: 6 · 2024: 1 · 2023: 2 · 2022: 10 · 2021: 8 · 2020: 3 · 2019: 5 · 2018: 8 · 2017: 8 · 2016: 6 · 2015: 4 · 2014: 6 · 2013: 3 · 2012: 3
- FWCI
- 1.62
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Experimental Neurology (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Deutsche Forschungsgemeinschaft
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Proteoglycans and glycosaminoglycans research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Keywords
- glutamate immunoreactivity, GABA-A receptor alpha1 subunit, chondroitin sulfate proteoglycans, extracellular matrix, parietal cortex, glutamatergic neurons, retrograde tracing, parvalbumin, Wisteria floribunda agglutinin
- MeSH terms
- Animals, Cerebral Cortex, Extracellular Matrix, Female, Fluorescent Dyes, Immunohistochemistry, Isoquinolines, Male, Organ Culture Techniques, Chondroitin Sulfate Proteoglycans, Receptors, GABA-A, Stilbamidines, Rats, Wistar, Pyramidal Cells, Microscopy, Confocal, Glutamic Acid, Rats
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