Co-localization of vasoactive intestinal polypeptide, $γ$-aminobutyric acid and choline acetyltransferase in neocortical interneurons of the adult rat
Abstract
Interneurons immunoreactive for vasoactive intestinal polypeptide (VIP) are integral elements of columnar organization patterns in the rat cerebral cortex. By application of the sensitive mirror technique, the co-localization of VIP with the classical inhibitory neurotransmitter gamma-aminobutyric acid (GABA) and the acetylcholine-synthesizing enzyme, choline acetyltransferase (ChAT), was investigated in neocortical neurons. Furthermore, the frequency of co-localization of ChAT with GABA was determined. In a sample of 118 VIP-immunoreactive neurons, mostly from the primary somatosensory cortex, it was demonstrated that virtually all of them reveal immunoreactivity for GABA and, therefore, are to be GABAergic. Moreover, 34% of mostly bipolar, VIP-positive neurons contained ChAT and are, thus, supposedly cholinergic as well. Co-localization of VIP and ChAT varied according to cortical laminae. Finally, 88% of a total of 60 ChAT-immunoreactive neurons were also immunostained for GABA. It is concluded that almost all VIP-immunoreactive neurons and most of the cholinergic neurons in rat neocortex represent partly overlapping subpopulations of inhibitory interneurons utilizing GABA.
Integrity signals
Registry
Cites
Statistics
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?
Bipolar cortical interneurons expressing VIP and ChAT were first identified by immunohistochemistry in rodents and account for about one third of all VIP+ cortical neurons.
“Bipolar cortical interneurons expressing vasoactive intestinal polypeptide (VIP) and ChAT were first identified using immunohistochemistry in rodents and account for $1/3 of all VIP+ cortical neurons.92,93”
From Synaptic and circuit functions of multitransmitter neurons in the mammalian brain (2023) · cites this paper as [92]
Cites
Alzheimer's Disease: A Disorder of Cortical Cholinergic Innervation
Coyle, J. T., Price, D. L., & DeLong, M. R. (1983) · Science · doi:10.1126/science.6338589 · Cited by 3,050 · see citing works
The structural organization of layer IV in the somatosensory region (S I) of mouse cerebral cortex
Woolsey, T. A., & Van der Loos, H. (1970) · Brain Research · doi:10.1016/0006-8993(70)90079-x · Cited by 2,254 · see citing works
McCormick, D. A. (1992) · Progress in Neurobiology · doi:10.1016/0301-0082(92)90012-4 · Cited by 1,117 · see citing works
Nucleus basalis and thalamic control of neocortical activity in the freely moving rat
Buzsáki, G., Bickford, R. G., Ponomareff, G., Thal, L. J., Mandel, R. J., & Gage, F. H. (1988) · Journal of Neuroscience · doi:10.1523/jneurosci.08-11-04007.1988 · Cited by 1,039 · see citing works
Zilles, K. (1985) · Springer eBooks · doi:10.1007/978-3-642-70573-1 · Cited by 756 · see citing works
Self-citationBuhl, E. H., Halasy, K., & Somogyi, P. (1994) · Nature · doi:10.1038/368823a0 · Cited by 728 · see citing works
The Cortex of the Rat: A Stereotaxic Atlas
Zilles, K. (1985) · Medical Entomology and Zoology · Cited by 657 · see citing works
Self-citationWelker, C., & Woolsey, T. A. (1974) · The Journal of Comparative Neurology · doi:10.1002/cne.901580405 · Cited by 454 · see citing works
Neocortical cholinergic innervation: A description of extrinsic and intrinsic components in the rat
Johnston, M. V., McKinney, M., & Coyle, J. T. (1981) · Experimental Brain Research · doi:10.1007/bf00237760 · Cited by 441 · see citing works
Kosaka, T., Tauchi, M., & Dahl, J. L. (1988) · Experimental Brain Research · doi:10.1007/bf00247609 · Cited by 417 · see citing works
Three distinct subpopulations of GABAergic neurons in rat frontal agranular cortex
Kubota, Y., Hattori, R., & Yui, Y. (1994) · Brain Research · doi:10.1016/0006-8993(94)91060-x · Cited by 365 · see citing works
Eckenstein, F., & Baughman, R. W. (1984) · Nature · doi:10.1038/309153a0 · Cited by 356 · see citing works
An anatomical study of cholinergic innervation in rat cerebral cortex
Eckenstein, F. P., Baughman, R. P., & Quinn, J. F. (1988) · Neuroscience · doi:10.1016/0306-4522(88)90251-5 · Cited by 348 · see citing works
Kosaka, T., Kosaka, K., Tateishi, K., Hamaoka, Y., Yanaihara, N., Wu, J., & Hama, K. (1985) · The Journal of Comparative Neurology · doi:10.1002/cne.902390408 · Cited by 324 · see citing works
Lysakowski, A., Wainer, B. H., Bruce, G., & Hersh, L. B. (1989) · Neuroscience · doi:10.1016/0306-4522(89)90180-2 · Cited by 239 · see citing works
Innervation of different peptide-containing neurons in the hippocampus by gabaergic septal afferents
Gulyás, A. I., Görcs, T. J., & Freund, T. F. (1990) · Neuroscience · doi:10.1016/0306-4522(90)90189-b · Cited by 234 · see citing works
Self-citationCentral Nervous Mechanisms in Mechanoreceptive Sensibility
Mountcastle, V. B. (1984) · Comprehensive physiology · doi:10.1002/cphy.cp010318 · Cited by 212 · see citing works
Acsády, L., Arabadzisz, D., & Freund, T. F. (1996) · Neuroscience · doi:10.1016/0306-4522(95)00610-9 · Cited by 187 · see citing works
Self-citationMorrison, J., Magistretti, P., Benoit, R., & Bloom, F. (1984) · Brain Research · doi:10.1016/0006-8993(84)90763-7 · Cited by 176 · see citing works
The effects of acetylcholine on response properties of cat somatosensory cortical neurons
Metherate, R., Tremblay, N. A., & Dykes, R. W. (1988) · Journal of Neurophysiology · doi:10.1152/jn.1988.59.4.1231 · Cited by 138 · see citing works
Cerebral circulatory and metabolic effects of vasoactive intestinal polypeptide
McCulloch, J., & Edvinsson, L. I. (1980) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.1980.238.4.h449 · Cited by 135 · see citing works
Orsetti, M., Casamenti, F., & Pepeu, G. (1996) · Brain Research · doi:10.1016/0006-8993(96)00292-2 · Cited by 126 · see citing works
Effect of acetylcholine and vasoactive intestinal peptide on cerebral blood flow
Heistad, D. D., Marcus, M. L., Said, S. I., et al. (1980) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.1980.239.1.h73 · Cited by 116 · see citing works
Lamour, Y. A., Dutar, P., & Jobert, A. (1982) · Neuroscience · doi:10.1016/0306-4522(82)90259-7 · Cited by 115 · see citing works
Vasoactive intestinal polypeptide-immunoreactive neurons in rat visual cortex.
Connor, J., & Peters, A. (1984) · Neuroscience · doi:10.1016/0306-4522(84)90002-2 · Cited by 101 · see citing works
Classical transmitters and transmitter receptors in the CNS
Björklund, A., Hökfelt, T. G. M., & Kuhar, M. J. (1984) · Elsevier eBooks · Cited by 100 · see citing works
Welker, E., Rao, S., Dörfl, J., Melzer, P., & der Loos, H. V. (1992) · Journal of Neuroscience · doi:10.1523/jneurosci.12-01-00153.1992 · Cited by 95 · see citing works
Magistretti, P. J., & Morrison, J. H. (1988) · Neuroscience · doi:10.1016/0306-4522(88)90338-7 · Cited by 94 · see citing works
Szabat, E., Soinila, S. O., Häppölä, O., et al. (1992) · Neuroscience · doi:10.1016/0306-4522(92)90255-z · Cited by 93 · see citing works
Chédotal, A., Umbriaco, D., Descarries, L., Hartman, B. K., & Hamel, É. (1994) · The Journal of Comparative Neurology · doi:10.1002/cne.903430105 · Cited by 88 · see citing works
Human fetal hippocampal development: II. The neuronal cytoskeleton
Arnold, S. E., & Trojanowski, J. Q. (1996) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19960401)367:2 · Cited by 87 · see citing works
Quantitative aspects of the GABA circuitry in the primary visual cortex of the adult rat
Beaulieu, C., Campistron, G., & Crevier, C. (1994) · The Journal of Comparative Neurology · doi:10.1002/cne.903390407 · Cited by 78 · see citing works
Dauphin, F., Lacombe, P. M., Sercombe, R., Hamel, É., & Seylaz, J. (1991) · Brain Research · doi:10.1016/0006-8993(91)90232-k · Cited by 73 · see citing works
Chédotal, A., Cozzani, C., Faure, M.-P., Hartman, B. K., & Hamel, É. (1994) · Brain Research · doi:10.1016/0006-8993(94)90076-0 · Cited by 71 · see citing works
Vasoactive intestinal polypeptide modulates neuronal excitability in hippocampal slices of the rat
Haas, H. L., & Gähwiler, B. H. (1992) · Neuroscience · doi:10.1016/0306-4522(92)90243-u · Cited by 61 · see citing works
Peters, A. (1990) · Journal of Neurocytology · doi:10.1007/bf01188036 · Cited by 55 · see citing works
Haj�s, F., Zilles, K., Schleicher, A., & K�lm�n, M. (1988) · Anatomy and Embryology · doi:10.1007/bf00318224 · Cited by 42 · see citing works
Self-citationChmielowska, J., Stewart, M. G., & Bourne, R. C. (1988) · Brain Research · doi:10.1016/0006-8993(88)91472-2 · Cited by 36 · see citing works
Galea, E., Fernández‐Shaw, C., Triguero, D., & Estrada, C. (1991) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1038/jcbfm.1991.148 · Cited by 30 · see citing works
Electrophysiological actions of VIP in rat somatosensory cortex
Sessler, F. M., Grady, S. M., Waterhouse, B. D., & Moises, H. C. (1991) · Peptides · doi:10.1016/0196-9781(91)90124-8 · Cited by 23 · see citing works
Haj�s, F., Zilles, K., Gallatz, K., Schleicher, A., Kaplan, I., & Werner, L. (1988) · Anatomy and Embryology · doi:10.1007/bf00318223 · Cited by 23 · see citing works
Self-citationMurphy, P., Grieve, K. L., & Sillito, A. M. (1993) · Journal of Neurophysiology · doi:10.1152/jn.1993.69.5.1465 · Cited by 19 · see citing works
Vasoactive intestinal polypeptide immunoreactive structures in the mouse barrel field
Zilles, K., Hajós, F., Csillag, A., Kálmán, M., Sótonyi, P., & Schleicher, A. (1993) · Brain Research · doi:10.1016/0006-8993(93)90438-s · Cited by 17 · see citing works
Self-citationWang, J.-Y., Yaksh, T. L., & Go, V. L. W. (1985) · Brain Research · doi:10.1016/0006-8993(85)90042-3 · Cited by 16 · see citing works
The Role of Acetylcholine in Barrel Cortex
Juliano, S. L., & Jacobs, S. E. (1995) · Cerebral cortex · doi:10.1007/978-1-4757-9616-2_10 · Cited by 6 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Classification of NPY-Expressing Neocortical Interneurons
Karagiannis, A., Gallopin, T., Dávid, C., Battaglia, D., Geoffroy, H., Rossier, J., Hillman, E. M. C., Staiger, J. F., & Cauli, B. (2009) · The Journal of Neuroscience · doi:10.1523/jneurosci.0058-09.2009 · Cited by 256 · see citing works
Self-citationThe neurovascular unit in brain function and disease: The neurovascular unit function
Lecrux, C., & Hamel, E. (2011) · Acta Physiologica · doi:10.1111/j.1748-1716.2011.02256.x · Cited by 251 · see citing works
Prönneke, A., Scheuer, B., Wagener, R. J., Möck, M., Witte, M., & Staiger, J. F. (2015) · Cerebral Cortex · doi:10.1093/cercor/bhv202 · Cited by 204 · see citing works
Self-citationNeurotherapeutic applications of nanoparticles in Alzheimer’s disease
Sahni, J. K., Doggui, S., Ali, J., Baboota, S., Dao, L., & Ramassamy, C. (2011) · Journal of Controlled Release · doi:10.1016/j.jconrel.2010.11.033 · Cited by 219 · see citing works
Férézou, I., Cauli, B., Hill, E. L., Rossier, J., Hamel, E., & Lambolez, B. (2002) · The Journal of Neuroscience · doi:10.1523/jneurosci.22-17-07389.2002 · Cited by 215 · see citing works
Functional Characterization of Intrinsic Cholinergic Interneurons in the Cortex
von Engelhardt, J., Eliava, M., Meyer, A. H., Rozov, A., & Monyer, H. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.4647-06.2007 · Cited by 177 · see citing works
Porter, J. T., Cauli, B., Staiger, J. F., Lambolez, B., Rossier, J., & Audinat, E. (1998) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.1998.00367.x · Cited by 173 · see citing works
Self-citationVucurovic, K., Gallopin, T., Ferezou, I., Rancillac, A., Chameau, P., van Hooft, J. A., Geoffroy, H., Monyer, H., Rossier, J., & Vitalis, T. (2010) · Cerebral Cortex · doi:10.1093/cercor/bhp310 · Cited by 139 · see citing works
Dávid, C., Schleicher, A., Zuschratter, W., & Staiger, J. F. (2007) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2007.05496.x · Cited by 120 · see citing works
Self-citationGranger, A. J., Wang, W., Robertson, K., El-Rifai, M., Zanello, A. F., Bistrong, K., Saunders, A., Chow, B. W., Nuñez, V., Turrero García, M., et al. (2020) · eLife · doi:10.7554/elife.57749 · Cited by 124 · see citing works
Cortical sources of CRF, NKB, and CCK and their effects on pyramidal cells in the neocortex
Gallopin, T., Geoffroy, H., Rossier, J., & Lambolez, B. (2006) · Cerebral Cortex · doi:10.1093/cercor/bhj081 · Cited by 97 · see citing works
Multi-transmitter neurons in the mammalian central nervous system
Granger, A. J., Wallace, M. L., & Sabatini, B. L. (2017) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2017.04.007 · Cited by 95 · see citing works
Revisiting enigmatic cortical calretinin-expressing interneurons
Cauli, B., Zhou, X., Tricoire, L., Toussay, X., & Staiger, J. F. (2014) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2014.00052 · Cited by 86 · see citing works
Self-citationObermayer, J., Luchicchi, A., Heistek, T. S., de Kloet, S. F., Terra, H., Bruinsma, B., Mnie-Filali, O., Kortleven, C., Galakhova, A. A., Khalil, A. J., et al. (2019) · Nature Communications · doi:10.1038/s41467-019-13244-9 · Cited by 83 · see citing works
Synaptic and circuit functions of multitransmitter neurons in the mammalian brain
Wallace, M. L., & Sabatini, B. L. (2023) · Neuron · doi:10.1016/j.neuron.2023.06.003 · Cited by 59 · see citing works
Staiger, J. F., Masanneck, C., Schleicher, A., & Zuschratter, W. (2004) · Journal of Comparative Neurology · doi:10.1002/cne.10953 · Cited by 53 · see citing works
Self-citationObermayer, J., Luchicchi, A., de Kloet, S. F., Terra, H., Bruinsma, B., Heistek, T. S., Mnie-Filali, O., Kortleven, C., Kroon, T., Jonker, A. J., et al. (2018) · doi:10.1101/461723 · Cited by 83 · see citing works
- Authors
- Bayraktar, T., Staiger, J. F., Acsady, L., Cozzari, C., Freund, T. F., & Zilles, K.
- Affiliations
- Heinrich Heine University Düsseldorf (DE)
- HUN-REN Institute of Experimental Medicine (HU)
- Corresponding author
- Staiger, J.F
- Venue
- Brain Research
- Publisher
- Elsevier BV
- Published
- 1997-05
- Volume
- 757
- Issue
- 2
- Pages
- 209-217
- ISSN
- 0006-8993 (ISSN-L)
- OpenAlex
- W2046281188
- Cited by
- 99
- References
- 45
- Citations by year
- 2024: 5 · 2023: 3 · 2022: 3 · 2021: 3 · 2020: 4 · 2019: 1 · 2018: 4 · 2017: 2 · 2016: 3 · 2015: 5 · 2014: 6 · 2013: 3 · 2012: 2
- FWCI
- 1.44
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Brain Research (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuropeptides and Animal Physiology
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Keywords
- vasoactive intestinal peptide, GABA, choline acetyltransferase, neocortical interneurons, colocalization, GABAergic neurons, cholinergic neurons, primary somatosensory cortex, cortical layers, columnar organization, inhibitory neurotransmitter, rats
- MeSH terms
- Animals, Cerebral Cortex, Choline O-Acetyltransferase, gamma-Aminobutyric Acid, Immunohistochemistry, Interneurons, Male, Tissue Distribution, Vasoactive Intestinal Peptide, Rats, Wistar, 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