The DOI matches its Crossref record.
Correlation of physiological subgroupings of nonpyramidal cells with parvalbumin- and calbindinD28k-immunoreactive neurons in layer V of rat frontal cortex
Abstract
1. To test the hypothesis that physiologically and morphologically different cortical nonpyramidal cells express different calcium-binding proteins, whole-cell current-clamp recording in vitro was combined with intracellular staining and double immunofluorescence in layer V of frontal cortex of rats 16-20 days old. 2. Nonpyramidal cells were first characterized as fast-spiking (FS) or low-threshold spike (LTS) cells, injected with biocytin, and subsequently stained immunohistochemically for parvalbumin and calbindinD28k. 3. FS cells were identified by input resistances < 350 M omega, spike width at half amplitude < 0.8 ms, and virtually no spike frequency adaptation of spike trains by depolarizing pulses. LTS cells were identified by input resistances > 350 M omega, spike width at half amplitude > 0.8 ms, and the discharge of low-threshold spikes from hyperpolarized potentials. Repetitive firing could be induced by a combination of stimulation-induced excitatory postsynaptic potentials with depolarization in FS cells. Repetitive firing was not observed in LTS cells under these conditions. 4. After biocytin injection of layer V cells characterized in this way, subsequent double immunostaining showed that all biocytin-labeled parvalbumin-immunoreactive cells (n = 18) belonged to the FS cells (FS-PV cells), whereas all biocytin-labeled calbindinD28k-immunoreactive cells (n = 10) belonged to the LTS cells (LTS-Calb cells). 5. FS-PV cells had smooth or sparsely spiny dendrites, whereas LTS-Calb cells had dendrites with a modest number of spines but fewer than pyramidal cells. FS-PV cells showed denser axonal branches near their somata and extended axons in a more horizontal direction. Some of them could be identified as basket cells by the presence of terminal boutons surrounding somata of other cells. LTS-Calb cells extended their main axons more vertically up to layer I. 6. Double immunofluorescent staining revealed that very few cells in layer V showed immunoreactivity for both calcium-binding proteins but that most cells immunoreactive for the calcium-binding proteins in layer V were also immunoreactive for gamma-aminobutyric acid. 7. These results suggest that GABAergic nonpyramidal cells in layer V of neocortex can be divided into two functional groups on the basis of different firing modes, axonal distributions, and calcium-binding protein immunoreactivity: 1) FS-PV cells show repetitive firing by synaptic activation, have axonal arborizations that are more dense near their somata and oriented horizontally, and the cells exhibit parvalbumin immunoreactivity and 2) LTS cells show low-threshold spikes, have more vertical axonal arborizations up to layer I, and exhibit calbindinD28K immunoreactivity.
Overview
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Citations
Cited by
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
Neurophysiological and Computational Principles of Cortical Rhythms in Cognition
Wang, X.-J. (2010) · Physiological Reviews · doi:10.1152/physrev.00035.2008 · Cited by 1,939
Large-scale recording of neuronal ensembles
Buzsáki, G. (2004) · Nature Neuroscience · doi:10.1038/nn1233 · Cited by 1,875
Reconstruction and Simulation of Neocortical Microcircuitry
Markram, H., Muller, E., Ramaswamy, S., Reimann, M. W., Abdellah, M., Sanchez, C. A., Ailamaki, A., Alonso-Nanclares, L., Antille, N., Arsever, S., et al. (2015) · Cell · doi:10.1016/j.cell.2015.09.029 · Cited by 1,557
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
Self-citationHomayoun, H., & Moghaddam, B. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.2213-07.2007 · Cited by 1,231
GABAergic Interneurons Implications for Understanding Schizophrenia and Bipolar Disorder
Benes, F. (2001) · Neuropsychopharmacology · doi:10.1016/s0893-133x(01)00225-1 · Cited by 1,082
A network of fast-spiking cells in the neocortex connected by electrical synapses
Galarreta, M., & Hestrin, S. (1999) · Nature · doi:10.1038/47029 · Cited by 960
Common circuit defect of excitatory-inhibitory balance in mouse models of autism
Gogolla, N., LeBlanc, J. J., Quast, K. B., Südhof, T. C., Fagiolini, M., & Hensch, T. K. (2009) · Journal of Neurodevelopmental Disorders · doi:10.1007/s11689-009-9023-x · Cited by 610
DeFelipe, J. (1997) · Journal of Chemical Neuroanatomy · doi:10.1016/s0891-0618(97)10013-8 · Cited by 550
Rhythmic and dysrhythmic thalamocortical dynamics: GABA systems and the edge effect
Llinás, R., Urbano, F. J., Leznik, E., Ramírez, R. R., & van Marle, H. J. F. (2005) · Trends in Neurosciences · doi:10.1016/j.tins.2005.04.006 · Cited by 549
The Role of the Medial Prefrontal Cortex in the Conditioning and Extinction of Fear
Giustino, T. F., & Maren, S. (2015) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2015.00298 · Cited by 519
Wang, Y., Toledo‐Rodriguez, M., Gupta, A., Wu, C., Silberberg, G., Luo, J., & Markram, H. (2004) · The Journal of Physiology · doi:10.1113/jphysiol.2004.073353 · Cited by 491
Pharmacology and behavioral pharmacology of the mesocortical dopamine system
Tzschentke, T. M. (2001) · Progress in Neurobiology · doi:10.1016/s0301-0082(00)00033-2 · Cited by 481
Functional maps of neocortical local circuitry.
Thomson, A. M. (2007) · Frontiers in Neuroscience · doi:10.3389/neuro.01.1.1.002.2007 · Cited by 434
Electrical synapses between Gaba-Releasing interneurons
Galarreta, M., & Hestrin, S. (2001) · Nature Reviews Neuroscience · doi:10.1038/35077566 · Cited by 434
Rajkowska, G., O'Dwyer, G., Teleki, Z., Stockmeier, C. A., & Miguel-Hidalgo, J. J. (2007) · Neuropsychopharmacology · doi:10.1038/sj.npp.1301234 · Cited by 430
Role of the calcium-binding protein parvalbumin in short-term synaptic plasticity
Caillard, O., Moreno, H., Schwaller, B., Llano, I., Celio, M. R., & Marty, A. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.230362997 · Cited by 406
Somatostatin-expressing neurons in cortical networks
Urban-Ciecko, J., & Barth, A. L. (2016) · Nature Reviews Neuroscience · doi:10.1038/nrn.2016.53 · Cited by 374
Kawaguchi, Y., & Kondo, S. (2002) · Journal of Neurocytology · doi:10.1023/a:1024126110356 · Cited by 395
Self-citationGalarreta, M., & Hestrin, S. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.192159599 · Cited by 387
Kawaguchi, Y., & Kubota, Y. (1996) · The Journal of Neuroscience · doi:10.1523/jneurosci.16-08-02701.1996 · Cited by 380
Self-citationFeedforward Mechanisms of Excitatory and Inhibitory Cortical Receptive Fields
Bruno, R. M., & Simons, D. J. (2002) · The Journal of Neuroscience · doi:10.1523/jneurosci.22-24-10966.2002 · Cited by 354
Cho, K. K. A., Hoch, R., Lee, A. T., Patel, T., Rubenstein, J. L. R., & Sohal, V. S. (2015) · Neuron · doi:10.1016/j.neuron.2015.02.019 · Cited by 329
Gain Modulation by Nicotine in Macaque V1
Disney, A. A., Aoki, C., & Hawken, M. J. (2007) · Neuron · doi:10.1016/j.neuron.2007.09.034 · Cited by 331
Kinney, J. W., Davis, C. N., Tabarean, I., Conti, B., Bartfai, T., & Behrens, M. M. (2006) · The Journal of Neuroscience · doi:10.1523/jneurosci.4722-05.2006 · Cited by 329
Classification of fusiform neocortical interneurons based on unsupervised clustering
Cauli, B., Porter, J. T., Tsuzuki, K., Lambolez, B., Rossier, J., Quenet, B., & Audinat, E. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.97.11.6144 · Cited by 316
Pawelzik, H., Hughes, D. I., & Thomson, A. M. (2002) · Journal of Comparative Neurology · doi:10.1002/cne.10118 · Cited by 262
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
Lewis, D., Volk, D., & Hashimoto, T. (2004) · Psychopharmacology · doi:10.1007/s00213-003-1673-x · Cited by 253
Mechanisms of Inhibition within the Telencephalon: “Where the Wild Things Are”
Fishell, G., & Rudy, B. (2011) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-061010-113717 · Cited by 233
Uematsu, M., Hirai, Y., Karube, F., Ebihara, S., Kato, M., Abe, K., Obata, K., Yoshida, S., Hirabayashi, M., Yanagawa, Y., et al. (2008) · Cerebral Cortex · doi:10.1093/cercor/bhm056 · Cited by 232
Self-citationParvalbumin-Expressing Inhibitory Interneurons in Auditory Cortex Are Well-Tuned for Frequency
Moore, A. K., & Wehr, M. (2013) · The Journal of Neuroscience · doi:10.1523/jneurosci.0663-13.2013 · Cited by 225
Calcium Microdomains in Aspiny Dendrites
Goldberg, J. H., Tamas, G., Aronov, D., & Yuste, R. (2003) · Neuron · doi:10.1016/s0896-6273(03)00714-1 · Cited by 212
Fukuda, T., Kosaka, T., Singer, W., & Galuske, R. A. W. (2006) · The Journal of Neuroscience · doi:10.1523/jneurosci.4076-05.2006 · Cited by 209
Stimulus feature selectivity in excitatory and inhibitory neurons in primary visual cortex
Cardin, J. A., Palmer, L. A., & Contreras, D. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.1692-07.2007 · Cited by 185
Influence of the hippocampus on interneurons of the rat prefrontal cortex
Tierney, P. L., Dégenètais, E., Thierry, A., Glowinski, J., & Gioanni, Y. (2004) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2004.03501.x · Cited by 192
Morphology and physiology of cortical neurons in layer I
Hestrin, S., & Armstrong, W. E. (1996) · The Journal of Neuroscience · doi:10.1523/jneurosci.16-17-05290.1996 · Cited by 194
Neuronal circuits in barrel cortex for whisker sensory perception
Staiger, J. F., & Petersen, C. C. H. (2021) · Physiological Reviews · doi:10.1152/physrev.00019.2019 · Cited by 165
Physiological properties of inhibitory interneurons in cat striate cortex
Azouz, R. (1997) · Cerebral Cortex · doi:10.1093/cercor/7.6.534 · Cited by 173
Schwaller, B., Tetko, I. V., Tandon, P., Silveira, D. C., Vreugdenhil, M., Henzi, T., Potier, M.-C., Celio, M. R., & Villa, A. E. P. (2004) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2003.12.006 · Cited by 169
Untangling GABAergic wiring in the cortical microcircuit
Kubota, Y. (2014) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2013.10.003 · Cited by 172
Self-citationSelective modulation of excitatory and inhibitory microcircuits by dopamine
Gao, W.-J., & Goldman-Rakic, P. S. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.262796399 · Cited by 170
Hughes, D. I., Sikander, S., Kinnon, C. M., Boyle, K. A., Watanabe, M., Callister, R. J., & Graham, B. A. (2012) · The Journal of Physiology · doi:10.1113/jphysiol.2012.235655 · Cited by 151
Wingert, J. C., & Sorg, B. A. (2021) · Frontiers in Synaptic Neuroscience · doi:10.3389/fnsyn.2021.673210 · Cited by 129
Hu, H., Cavendish, J. Z., & Agmon, A. (2013) · Frontiers in Neural Circuits · doi:10.3389/fncir.2013.00195 · Cited by 120
Petrache, A. L., Rajulawalla, A., Shi, A., Wetzel, A., Saito, T., Saido, T. C., Harvey, K., & Ali, A. B. (2019) · Cerebral Cortex · doi:10.1093/cercor/bhz016 · Cited by 124
Inhibitory Actions Unified by Network Integration
Seybold, B. A., Phillips, E. A. K., Schreiner, C. E., & Hasenstaub, A. R. (2015) · Neuron · doi:10.1016/j.neuron.2015.09.013 · Cited by 118
Disney, A. A., & Aoki, C. (2008) · Journal of Comparative Neurology · doi:10.1002/cne.21616 · Cited by 109
Kritzer, M. F. (2002) · Cerebral Cortex · doi:10.1093/cercor/12.2.116 · Cited by 106
Staiger, J. F., Zilles, K., & Freund, T. F. (1996) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.1996.tb01191.x · Cited by 98
Disney, A. A., Domakonda, K. V., & Aoki, C. (2006) · The Journal of Comparative Neurology · doi:10.1002/cne.21096 · Cited by 99
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
Two distinct subgroups of cholecystokinin-immunoreactive cortical interneurons
Kubota, Y., & Kawaguchi, Y. (1997) · Brain Research · doi:10.1016/s0006-8993(96)01446-1 · Cited by 93
Self-citationHioki, H., Okamoto, S., Konno, M., Kameda, H., Sohn, J., Kuramoto, E., Fujiyama, F., & Kaneko, T. (2013) · The Journal of Neuroscience · doi:10.1523/jneurosci.2255-12.2013 · Cited by 83
Goldberg, J. H., Tamas, G., & Yuste, R. (2003) · The Journal of Physiology · doi:10.1113/jphysiol.2003.042580 · Cited by 89
A dynamic zone defines interneuron remodeling in the adult neocortex
Lee, W.-C. A., Chen, J. L., Huang, H., Leslie, J. H., Amitai, Y., So, P. T., & Nedivi, E. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0810149105 · Cited by 87
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
Gerfen, C. R. (2004) · The Rat Nervous System · doi:10.1016/b978-012547638-6/50019-5 · Cited by 85
Yuen, E. Y., & Yan, Z. (2009) · The Journal of Neuroscience · doi:10.1523/jneurosci.5050-08.2009 · Cited by 81
Axo-dendritic overlap and laminar projection can explain interneuron connectivity to pyramidal cells
Packer, A. M., McConnell, D. J., Fino, E., & Yuste, R. (2013) · Cerebral Cortex · doi:10.1093/cercor/bhs210 · Cited by 73
Koelbl, C., Helmstaedter, M., Lübke, J., & Feldmeyer, D. (2015) · Cerebral Cortex · doi:10.1093/cercor/bht263 · Cited by 68
Nomura, T., Musial, T. F., Marshall, J. J., Zhu, Y., Remmers, C. L., Xu, J., Nicholson, D. A., & Contractor, A. (2017) · The Journal of Neuroscience · doi:10.1523/jneurosci.2893-16.2017 · Cited by 64
Fukuda, T., & Kosaka, T. (2000) · Neuroscience Research · doi:10.1016/s0168-0102(00)00163-2 · Cited by 63
Slaker, M. L., Jorgensen, E. T., Hegarty, D. M., Liu, X., Kong, Y., Zhang, F., Linhardt, R. J., Brown, T. E., Aicher, S. A., & Sorg, B. A. (2018) · eneuro · doi:10.1523/eneuro.0221-18.2018 · Cited by 64
“The electrophysiological findings in FSIs, which are likely PV-containing cells (Kawaguchi and Kubota, 1993), are consistent with the idea that an increase in the inhibitory/excitatory balance in PV/PNN cells reduces inhibitory output to pyramidal neurons, contributing to the hyperexcitability of these neurons that we…”
BackgroundResultInfluentialRupert, D. D., & Shea, S. D. (2022) · Frontiers in Neural Circuits · doi:10.3389/fncir.2022.886629 · Cited by 58
The role of GABAergic inhibition in ocular dominance plasticity
Heimel, J. A., van Versendaal, D., & Levelt, C. N. (2011) · Neural Plasticity · doi:10.1155/2011/391763 · Cited by 57
Staiger, J. F., Masanneck, C., Schleicher, A., & Zuschratter, W. (2004) · Journal of Comparative Neurology · doi:10.1002/cne.10953 · Cited by 53
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
Vijayraghavan, S., Major, A. J., & Everling, S. (2018) · Neuron · doi:10.1016/j.neuron.2018.05.027 · Cited by 51
Wędzony, K., & Chocyk, A. (2009) · Pharmacological Reports · doi:10.1016/s1734-1140(09)70161-6 · Cited by 50
Subpopulations of neurons expressing parvalbumin in the human amygdala
Pantazopoulos, H., Lange, N., Hassinger, L., & Berretta, S. (2006) · Journal of Comparative Neurology · doi:10.1002/cne.20961 · Cited by 45
Disney, A. A., & Reynolds, J. H. (2014) · Journal of Comparative Neurology · doi:10.1002/cne.23456 · Cited by 40
“The authors did not stain for PV in these fast-spiking neurons, but given their physiological properties it is likely that they were PV-ir neurons (Kawaguchi and Kubota, 1993).”
BackgroundZhong, P., Qin, L., & Yan, Z. (2020) · Cerebral Cortex · doi:10.1093/cercor/bhaa027 · Cited by 34
Disney, A. A., Alasady, H. A., & Reynolds, J. H. (2014) · Brain and Behavior · doi:10.1002/brb3.225 · Cited by 28
Metadata
- Authors
- Kawaguchi, Y., & Kubota, Y.
- Venue
- Journal of Neurophysiology
- Publisher
- American Physiological Society
- Published
- 1993-07-01
- Volume
- 70
- Issue
- 1
- Pages
- 387-396
- ISSN
- 0022-3077 (ISSN-L)
- 1522-1598
- OpenAlex
- W2264255990
- Cited by
- 558
- References
- 0
- FWCI
- 10.09
- Type
- journal article
- Language
- en
- Open access
- closed
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
Data sources
Bibliographic data: Semantic Scholar, OpenAlex, Crossref.
Contains information from the Semantic Scholar Academic Graph Datasets, made available under the ODC Attribution License (ODC-BY 1.0).
Semantic Scholar’s data is described in: Kinney, R., et al. (2023). The Semantic Scholar Open Data Platform. arXiv:2301.10140.