The DOI matches its Crossref record; 74 of the 74 references it cites were found in a registry or an index.
Perineuronal nets provide a polyanionic, glia‐associated form of microenvironment around certain neurons in many parts of the rat brain
Abstract
The nature and function of previously described perineuronal nets are still obscure. In the present study their polyanionic components were demonstrated in the rat brain using colloidal iron hydroxide (CIH) staining. In subcortical regions, such as the red nucleus, cerebellar, and vestibular nuclei, most neurons were ensheathed by CIH‐binding material. In the cerebral cortex perineuronal nets were seen around numerous nonpyramidal neurons. Biotinylated hyaluronectin revealed that hyaluronan occurs in perineuronal nets. Two plant lectins [ Wisteria floribunda agglutinin (WFA) and Vicia villosa agglutinin (VVA)] with affinity for N‐acetylgalactosamine visualized perineuronal nets similar to those rich in anionic components. Glutamic acid decarboxylase (GAD)‐immunoreactive synaptic boutons were shown to occupy numerous meshes of perineuronal VVA‐positive nets. Electron microscopically, VVA binding sites were scattered throughout perisynaptic profiles, but accumulated at membranes and in the extra‐cellular space except not in synaptic clefts. To investigate the spatial relationship between glial cell processes and perineuronal nets, two astrocytic markers (S100‐protein and glutamine synthetase) were visualized at the light and electron microscopic level. Two methods to detect microglia by the use of Griffonia simplicifolia agglutinin (GSA I‐B 4 ) and the monoclonal antibody, OX‐42, were also applied. Labelled structures forming perineuronal nets were observed with both astrocytic, but not with microglial, markers. It is concluded that perineuronal nets are composed of a specialized type of glia‐associated extracellular matrix rich in polyanionic groups and N‐acetylgalactosamine. The net‐like appearance is due to perisynaptic arrangement of the astrocytic processes and these extracellular components. Similar to the ensheathment of nodes of Ranvier, perineuronal nets may provide a special ion buffering capacity required around various, perhaps highly active, types of neurons. © 1993 Wiley‐Liss, Inc.
Overview
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
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?
In the citing paper
“Sulphate groups attached to these GAGs in concert with the negatively charged hyaluronic acid generate a highly polyanionic microenvironment around PN-ensheathed neurons.20, 21”
From Aggrecan, link protein and tenascin-R are essential components of the perineuronal net to protect neurons against iron-induced oxidative stress (2014) · cites this paper as [20]
In the citing paper
“the polyanionic components might also interact with ions of potential pathophysiological relevance such as iron ions involved in generating oxidative stress.20, 22, 26, 27”
From Aggrecan, link protein and tenascin-R are essential components of the perineuronal net to protect neurons against iron-induced oxidative stress (2014) · cites this paper as [20]
In the citing paper
“Astrocytes extend their processes into PNNs localized near the synapse (Brückner et al., 1993; Blümcke et al., 1995), suggesting a tetrapartite synaptic organization involving ECM, pre/post synaptic sites and astrocytes (Dityatev and Rusakov, 2011; Smith et al., 2015) whose synergistic functions remain unexplored.”
From The Perineuronal ‘Safety’ Net? Perineuronal Net Abnormalities in Neurological Disorders (2018) · cites this paper as Brückner et al., 1993
In the citing paper
“First, PNNs carry a high degree of negative charge and may function as cation sinks (Bruckner et al, 1993).”
From Reduced Labeling of Parvalbumin Neurons and Perineuronal Nets in the Dorsolateral Prefrontal Cortex of Subjects with Schizophrenia (2016) · cites this paper as Bruckner et al, 1993
In the citing paper
“As part of the extracellular matrix (ECM), perineuronal nets (PNs) are polyanionic, chondroitin sulfate proteoglycan (CSPG)-rich coatings of certain neurons, known to be affected in various neural diseases.”
From Damaged Neocortical Perineuronal Nets Due to Experimental Focal Cerebral Ischemia in Mice, Rats and Sheep (2017) · cites this paper as Brückner et al., 1993
In the citing paper
“They are composed of chondroitin sulfate proteoglycans (CSPGs) and their glycosaminoglycans, hyaluronic acid and tenascins, produced by various neural cell types (Brückner et al., 1993).”
From Damaged Neocortical Perineuronal Nets Due to Experimental Focal Cerebral Ischemia in Mice, Rats and Sheep (2017) · cites this paper as Brückner et al., 1993
In the citing paper
“More recent evidence indicates that WFA-labeled PNNs are associated with more heterogeneous neuronal phenotypes than previously thought, including several subgroups of interneurons, a small subset of cortico-cortical pyramidal cells, spinal cord motor neurons and cerebellum Purkinje cells (Ajmo et al., 2008; Brauer et al., 1995; Bruckner et al., 1993; Gati and Lendvai, 2013; Hartig et al., 1995;”
From Losing the sugar coating: Potential impact of perineuronal net abnormalities on interneurons in schizophrenia (2015) · cites this paper as Bruckner et al., 1993
In the citing paper
“PNNs have been implicated in ion homeostasis around highly active neurons”
From Perineuronal nets and schizophrenia: The importance of neuronal coatings (2014) · cites this paper as Bruckner et al., 1993
In the citing paper
“They can thus potentially act as a buffering system for physiologically relevant ions such as calcium, potassium, and sodium around highly active types of neurons”
From Perineuronal nets and schizophrenia: The importance of neuronal coatings (2014) · cites this paper as Bruckner et al., 1993
In the citing paper
“The PNN is a unique ECM structure that is most prominently displayed around GABAergic interneurons, with parvalbumin expressing cells having the highest level of colocalization (Brückner et al., 1993;Celio and Chiquet-Ehrismann, 1993;Morris and Henderson, 2000).”
From The hyaluronan and proteoglycan link proteins: Organizers of the brain extracellular matrix and key molecules for neuronal function and plasticity (2015) · cites this paper as Brückner et al., 1993
In the citing paper
“Perineuronal nets are extracellular matrix structures which surround synapses of highly active neuronal subtypes and are associated with microglia [156].”
From Apolipoprotein E4, inhibitory network dysfunction, and Alzheimer’s disease (2019) · cites this paper as [156]
Citations
Cites
Handbook of Chemical Neuroanatomy
Stern, C. D. (1986) · Neurochemistry International · doi:10.1016/0197-0186(86)90021-5 · Cited by 4,160
Fine structural localization of glutamine synthetase in astrocytes of rat brain
Norenberg, M. D., & Martinez-Hernandez, A. (1979) · Brain Research · doi:10.1016/0006-8993(79)90071-4 · Cited by 1,349
Parvalbumin in Most γ-Aminobutyric Acid-Containing Neurons of the Rat Cerebral Cortex
Celio, M. R. (1986) · Science · doi:10.1126/science.3945815 · Cited by 740
A simple, non-chromatographic procedure to purify immunoglobulins from serum and ascites fluid
McKinney, M. M., & Parkinson, A. (1987) · Journal of Immunological Methods · doi:10.1016/0022-1759(87)90324-3 · Cited by 618
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-citationOertel, W., Schmechel, D. E., Tappaz, M., & Kopin, I. J. (1981) · Neuroscience · doi:10.1016/0306-4522(81)90113-5 · Cited by 419
Self-citationStreit, W. J. (1990) · Journal of Histochemistry & Cytochemistry · doi:10.1177/38.11.2212623 · Cited by 372
Expression of tenascin in the developing and adult cerebellar cortex
Bartsch, S., Bartsch, U., Dörries, U., Faissner, A., Weller, A., Ekblom, P., & Schachner, M. (1992) · Journal of Neuroscience · doi:10.1523/jneurosci.12-03-00736.1992 · Cited by 271
GABA Neurons in the Cerebral Cortex
Houser, C. R., Vaughn, J. E., Hendry, S. H. C., Jones, E. G., & Peters, A. (1984) · Cerebral cortex · doi:10.1007/978-1-4615-6610-6_3 · Cited by 261
Organization of radial glial cells during the development of the rat dentate gyrus
Rickmann, M., Amaral, D. G., & Cowan, W. M. (1987) · The Journal of Comparative Neurology · doi:10.1002/cne.902640403 · Cited by 243
Self-citation
Research works printed but not linked: 13
- Delpech B., 1989, The Biology of Hyaluronan. CIBA Foundation Symposion, 143
- Faissner A., 1989, Dynamics and Plasticity in Neuronal Systems. Proc. 17th Göttingen Neurobiology Conference, 1
- Golgi C., 1891, La réseau diffus des centres du système nerveux, Arch. Ital. Biol., 15, 314
- Graumann W., 1958, Weitere Untersuchungen zur Spezifität der histochemischen Polysaccharid‐Eisenreaktion, Acta Histochem., 6, 1
- Hockfield S., 1989, Neuroimmune Networks, 57
- Kettenmann H., 1988, In: Glial Cell Receptors, 95
- Kimelberg H. K., 1988, Glial Cell Receptors
- McGeer P. L., 1986, In: Neurohistochemistry: Modern Methods and Applications P. Panula, 355
- Raff M. C., 1990, In: Differentiation and Functions of Glial Cells, 17
- Ramon y Cajal S., 1906, Studien über die Hirnrinde des Menschen
- Schweizer M. Müller C. M. andStreit J. W.(1991)Perisynaptic lectin‐binding sites in cat visual cortex: an electron microscopical investigation. In: Synapse‐Transmission‐Moduluation. Proc. 19th Göttingen Neurobiology Conference. Elsner N. and eds. Thieme Stuttgart p.226.
- Szentagothai J., 1975, In: Golgi Centennial Symposium, 1
- Wolff J. R., 1970, Proc. 6th Intern. Congr. Neuropathology, 327
Cited by
Sorted by citations
Items 301–357 of 357
Component-specific reduction in perineuronal nets in senescence-accelerated mouse strains
Ueno, H., Takahashi, Y., Murakami, S., Wani, K., Miyazaki, T., Matsumoto, Y., Okamoto, M., & Ishihara, T. (2023) · IBRO Neuroscience Reports · doi:10.1016/j.ibneur.2023.01.002 · Cited by 5
Regulation of CNS Plasticity Through the Extracellular Matrix
Warren, P. M., Dickens, S., Gigout, S., Fawcett, J. W., & Kwok, J. C. F. (2018) · Oxford University Press eBooks · doi:10.1093/oxfordhb/9780190635374.013.11 · Cited by 5
Midbrain extracellular matrix and microglia are associated with cognition in aging mice
Gray, D. T., Gutierrez, A., Jami‐Alahmadi, Y., Pandey, V., Pan, L., Zhang, Y., Wohlschlegel, J. A., McDevitt, R. A., & Biase, L. M. D. (2025) · Nature Communications · doi:10.1038/s41467-025-66434-z · Cited by 6
da Silva, N. R., Gobbo, D., Gomes, F. V., Scheller, A., Kirchhoff, F., Bel, E. D., & Guimarães, F. S. (2025) · Brain Research · doi:10.1016/j.brainres.2025.149772 · Cited by 4
Costa, C., Tortosa, R., Vidal, E., Padilla, D., Torres, J. M., Ferrer, I., Pumarola, M. B., & Bassols, A. (2008) · The Veterinary Journal · doi:10.1016/j.tvjl.2008.07.019 · Cited by 4
Schob, S., Puchta, J., Winter, K., Michalski, D., Mages, B., Martens, H., Emmer, A., Hoffmann, K., Gaunitz, F., Meinicke, A., et al. (2021) · Journal of Chemical Neuroanatomy · doi:10.1016/j.jchemneu.2021.102036 · Cited by 4
Self-citationBrevican, a Conditional Proteoglycan from Rat Brain
Seidenbecher, C. I., Richter, K., & Gundelfinger, E. D. (1997) · Springer eBooks · doi:10.1007/978-1-4615-5405-9_148 · Cited by 4
Malone, C. L., Li, J., Luebke, E. M., Carreras-Simons, L., Treis, W. W., Hammond, E. R., Monari, P. K., & Marler, C. A. (2025) · Biology of Sex Differences · doi:10.1186/s13293-025-00741-4 · Cited by 4
Post-Stroke Recovery in Relation to Parvalbumin-Positive Interneurons and Perineuronal Nets
Kuhl, L. M., Jeffers, M. S., Hristozov, N., Karthikeyan, S., McDonald, M. W., Hufnagel, A., Carter, A., Dancause, N., & Corbett, D. (2025) · Neurorehabilitation and neural repair · doi:10.1177/15459683241309567 · Cited by 4
Gáti, G., & Lendvai, D. (2013) · Orvosi Hetilap · doi:10.1556/oh.2013.29646 · Cited by 3
Perineuronal Nets in the Superior Olivary Complex
Morawski, M., & Sonntag, M. (2018) · Oxford University Press eBooks · doi:10.1093/oxfordhb/9780190849061.013.12 · Cited by 3
Bausch, S. B. (1998) · Brain Research Protocols · doi:10.1016/s1385-299x(98)00011-7 · Cited by 3
Huang, Y.-F., Liu, C., Liu, Z., Zhuang, X., Chen, J.-H., Zhang, Z.-N., Shen, C., & Hu, Y. (2026) · Brain · doi:10.1093/brain/awag058 · Cited by 3
Distribution of perineuronal nets in the adult rat neocortex
Budhu, K., Gomes, H., Borukhov, Y., Chu, P., & Brumberg, J. C. (2025) · Somatosensory & Motor Research · doi:10.1080/08990220.2025.2476945 · Cited by 2
Molecular and Extracellular Cues in Motor Neuron Specification and Differentiation
Swetenburg, R. L., Stice, S. L., & Karumbaiah, L. (2017) · Elsevier eBooks · doi:10.1016/b978-0-12-802257-3.00001-8 · Cited by 3
Sayed, R. (2009) · Assiut Veterinary Medical Journal/Maǧallaẗ Asyūṭ al-ṭibiyyaẗ al-baytariyyaẗ · doi:10.21608/avmj.2009.166994 · Cited by 2
Beneyto, M., Rueda, J., Merchán, J. A., & Prieto, J. J. (1999) · Brain Research Bulletin · doi:10.1016/s0361-9230(99)00056-8 · Cited by 2
Cannarozzo, C., Rubiolo, A., Casarotto, P., & Castrén, E. (2022) · doi:10.1101/2022.04.06.487292 · Cited by 2
Nowacka, A., Śniegocki, M., Bożiłow, D., & Ziółkowska, E. (2025) · International Journal of Molecular Sciences · doi:10.3390/ijms262110766 · Cited by 2
Chen, B., Hu, R., Wu, X., Shi, M., Chen, Y., Zhang, J., Huang, Y., Ying, X., Han, D., & Ma, R. (2026) · Journal of Integrative Neuroscience · doi:10.31083/jin46448 · Cited by 2
Growth Hormone and Insulin-like Growth Factor-I and Their Effects on Astroglial Gap Junctions
Åberg, N. D. (2006) · Elsevier eBooks · doi:10.1016/b978-012088484-1/50015-x · Cited by 1
Regulation of somatosensory cortex development downstream of glutamate
Petrie, A. (2009) · OpenGrey (Institut de l'Information Scientifique et Technique) · Cited by 1
Die Zellen des Nervensystems und ihre Verknüpfungen
Wolburg, H. (2002) · Springer eBooks · doi:10.1007/978-3-642-59371-0_1 · Cited by 1
Involvement of the cerebellum in cocaine-induced memory
Carbo‐Gas, M. (2017) · Tesis Doctorals en Xarxa (Consorci de Serveis Universitaris de Catalunya) · doi:10.6035/14023.2017.208925 · Cited by 1
Membrane Changes in BSE and Scrapie
Ersdal, C., McGovern, G., & Jeffrey, M. (2011) · doi:10.1002/9783527634323.ch10
Synaptic Sweet Talk: How Do Perineuronal Nets Contribute to Epileptogenesis and Neuroplasticity?
Naegele, J. R. (2016) · Epiliepsy currents/Epilepsy currents · doi:10.5698/1535-7597-16.1.29
Niechwiej‐Szwedo, E. (2008) · TSpace (University of Toronto)
Postnatale Gliogenese und Synaptogenese im somatosensorischen Cortex
Neuroanatomie, A. D. A. (2011)
Karthikeyan, S. S. (2017) · uO Research (University of Ottawa) · doi:10.20381/ruor-21084
Al‐Muhtasib, N. (2018) · DigitalGeorgetown (Georgetown University Library)
Mcgillis, K. (2018) · Digital Access to Scholarship at Harvard (DASH) (Harvard University)
PERINEURONAL NETS IN HIPPOCAMPAL AREA CA2: REGULATION BY ACTIVITY AND DISEASE
Carstens, K. E. (2018) · Carolina Digital Repository (University of North Carolina at Chapel Hill) · doi:10.17615/khgn-dw13
Schob, S., Puchta, J., Winter, K., Michalski, D., Mages, B., Martens, H., Emmer, A., Hoffmann, K., Gaunitz, F., Meinicke, A., et al. (2021) · Research Square · doi:10.21203/rs.3.rs-747032/v1
Self-citationda Silva, N. R. (2021) · Digital Library of Theses and Dissertations (Universidade de São Paulo) · doi:10.11606/t.17.2021.tde-05112021-105109
Sajikumar, S., & Benoy, A. (2020) · Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature · doi:10.3410/f.737102802.793571039
Chen, B., Hu, R. H., Wu, X., Shi, M., Chen, Y., Zhang, J., Ying, X., Huang, Y., Han, D., & Ma, R. (2023) · Research Square · doi:10.21203/rs.3.rs-3404696/v1
Energy optimisation predicts the capacity of ion buffering in the brain
Maex, R. (2023) · Biological Cybernetics · doi:10.1007/s00422-023-00980-x
Berrouschot, V., Sonntag, M., Reimann, K., Jäger, C., Martin, S., Holzer, M., Stieler, J., & Morawski, M. (2025) · Scientific Reports · doi:10.1038/s41598-025-14942-9
The role of perineuronal nets in post-stroke neuroplasticity and functional reorganization
Aderinto, N., Abraham, I. C., Kwape, J. M., Gaur, A., Akanbi, C. A., Oyeniyi, D. T., Babalola, A. E., Babalola, D. O., Adeyeye, J., Bukky, S. O., et al. (2025) · Next research. · doi:10.1016/j.nexres.2025.101060
Microglia: Key Players in Perineuronal Net Dynamics
Garmendia-Berges, M., & Puerta, E. (2025) · IntechOpen eBooks · doi:10.5772/intechopen.1012413 · Cited by 1
Age dependent seizure susceptibility of CA2 hippocampal neurons
Correa, J., Sablani, S., Wasfi, M., Correa, C., & Bandelow, S. (2025) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2025.1715872
Neurobiology of Saccadic Neurons in Monkeys
Horn, A. K. E., Mayadali, Ü. S., Kuhn, K. S., Abspacher, M., & Shaikh, A. G. (2026) · Contemporary clinical neuroscience · doi:10.1007/978-3-032-07539-0_25
Douceau, S. (2020) · theses.fr (ABES) · doi:10.70675/6f1007f2z8468z4365zb07dz7d863bf32cd5
Castro, A. E., Uriarte, N., Zangrando, D., Camacho, F. J., Paredes, R. G., Portillo, W., & Nogueira, J. (2026) · Brain Structure and Function · doi:10.1007/s00429-026-03177-7
Cheung, S. W., Fogarty, M. J., Zhan, W., Bellingham, M. C., Noakes, P. G., & Sieck, G. C. (2026) · Journal of Neurophysiology · doi:10.1152/jn.00033.2026
The Role of Meprins on the Brain Extracellular Matrix and Perineuronal Nets
Kreiselmaier, S., Keller, M., Nardi, L., Mueller, C., von Wiegen, N., Bickenbach, K., Gröbner, L. S., Abukhalaf, M., Tholey, A., Mueller, M. M., et al. (2026) · The FASEB Journal · doi:10.1096/fj.202601333r
Ashar, M. S., Anwar, M., Singh, A. K., Pradhan, R., Gupta, A., Chakrawarty, A., Haldar, P., Tripathi, M., & Dey, S. (2026) · Journal of Alzheimer s Disease · doi:10.1177/13872877261470815
Yang, J., Huang, T., Wang, M., Yingrui, X., Xuan, L., Li, C., Cao, W., Liyan, H., & Zhou, H. M. (2026) · IBRO Neuroscience Reports · doi:10.1016/j.ibneur.2026.07.016
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
Zujovic (2000) · doi:10.1002/(sici)1098-1136(20000215)29:4
Self-citation
Metadata
- Authors
- Brückner, G., Brauer, K., Härtig, W., Wolff, J. R., Rickmann, M. J., Derouiche, A., Delpech, B., Girard, N., Oertel, W. H., & Reichenbach, A.
- Affiliations
- Leipzig University (DE)
- University of Göttingen (DE)
- Goethe University Frankfurt (DE)
- Centre Henri Becquerel (FR)
- Ludwig-Maximilians-Universität München (DE)
- Corresponding author
- Brückner, Gert
- Venue
- Glia
- Publisher
- Wiley
- Published
- 1993-07
- Volume
- 8
- Issue
- 3
- Pages
- 183-200
- ISSN
- 0894-1491 (ISSN-L)
- 1098-1136
- OpenAlex
- W2099040370
- Cited by
- 358
- References
- 74
- Citations by year
- 2026: 8 · 2025: 13 · 2024: 7 · 2023: 9 · 2022: 17 · 2021: 13 · 2020: 16 · 2019: 13 · 2018: 25 · 2017: 19 · 2016: 17 · 2015: 10 · 2014: 10 · 2013: 13 · 2012: 14
- FWCI
- 2.88
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Glia (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Deutsche Forschungsgemeinschaft
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Proteoglycans and glycosaminoglycans research
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
- Keywords
- perineuronal nets, N-acetylgalactosamine, hyaluronic acid, astrocytes, microglia, glutamine synthetase, S-100 protein, glutamic acid decarboxylase, synaptic boutons, red nucleus, cerebellar nuclei, vestibular nuclei, cerebral cortex, lectin binding
- MeSH terms
- Acetylgalactosamine, Animals, Anions, Brain, Brain Chemistry, Colloids, Cytoplasm, Extracellular Matrix, gamma-Aminobutyric Acid, Glutamate Decarboxylase, Glutamate-Ammonia Ligase, Hyaluronic Acid, Hydroxides, S100 Proteins, Neuroglia, Neurons, Organic Chemicals, Staining and Labeling, Synapses, Biomarkers, Rats, Sprague-Dawley, Rats, Wistar, Microglia, Lectins, Rats, Iron Compounds
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
