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Electrical and chemical synapses among parvalbumin fast-spiking GABAergic interneurons in adult mouse neocortex
Open accessAbstract
Networks of γ-aminobutyric acid (GABA)ergic interneurons connected via electrical and chemical synapses are thought to play an important role in detecting and promoting synchronous activity in the cerebral cortex. Although the properties of electrical and chemical synaptic interactions among inhibitory interneurons are critical for their function as a network, they have only been studied systematically in juvenile animals. Here, we have used transgenic mice expressing the enhanced green fluorescent protein in cells containing parvalbumin (PV) to study the synaptic connectivity among fast-spiking (FS) cells in slices from adult animals (2–7 months old). We have recorded from pairs of PV-FS cells and found that the majority of them were electrically coupled (61%, 14 of 23 pairs). In addition, 78% of the pairs were connected via GABAergic chemical synapses, often reciprocally. The average coupling coefficient for step injections was 1.5% ( n = 14), a smaller value than that reported in juvenile animals. GABA-mediated inhibitory postsynaptic currents and potentials decayed with exponential time constants of 2.6 and 5.9 ms, respectively, and exhibited paired-pulse depression (50-ms interval). The inhibitory synaptic responses in the adult were faster than those observed in young animals. Our results indicate that PV-FS cells are highly interconnected in the adult cerebral cortex by both electrical and chemical synapses, establishing networks that can have important implications for coordinating activity in cortical circuits.
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“PV-INs in the cortex are highly interconnected via electrical and chemical synapses [69].”
From Parvalbumin interneuron vulnerability and brain disorders (2021) · cites this paper as [69]
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Cites
Whittington, M. A., Traub, R. D., & Jefferys, J. G. R. (1995) · Nature · doi:10.1038/373612a0 · Cited by 1,613
Gamma Oscillation by Synaptic Inhibition in a Hippocampal Interneuronal Network Model
Wang, X., & Buzsáki, G. (1996) · Journal of Neuroscience · doi:10.1523/jneurosci.16-20-06402.1996 · Cited by 1,561
Gamma (40-100 Hz) oscillation in the hippocampus of the behaving rat
Bragin, A., Jando, G., Nadasdy, Z., Hetke, J., Wise, K., & Buzsaki, G. (1995) · The Journal of Neuroscience · doi:10.1523/jneurosci.15-01-00047.1995 · Cited by 1,527
Synchronization of neuronal activity in hippocampus by individual GABAergic interneurons
Cobb, S. R., Buhl, E. H., Halasy, K., Paulsen, O., & Somogyi, P. (1995) · Nature · doi:10.1038/378075a0 · Cited by 1,498
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
Two networks of electrically coupled inhibitory neurons in neocortex
Gibson, J. R., Beierlein, M., & Connors, B. W. (1999) · Nature · doi:10.1038/47035 · Cited by 1,404
Huang, Z. J., Kirkwood, A., Pizzorusso, T., Porciatti, V., Morales, B., Bear, M. F., Maffei, L., & Tonegawa, S. (1999) · Cell · doi:10.1016/s0092-8674(00)81509-3 · Cited by 1,198
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
Self-citationWhen inhibition not excitation synchronizes neural firing
van Vreeswijk, C., Abbott, L. F., & Ermentrout, B. (1994) · Journal of Computational Neuroscience · doi:10.1007/bf00961879 · Cited by 771
Inhibitory threshold for critical-period activation in primary visual cortex
Fagiolini, M., & Hensch, T. K. (2000) · Nature · doi:10.1038/35004582 · Cited by 716
Proximally targeted GABAergic synapses and gap junctions synchronize cortical interneurons
Tamás, G., Buhl, E. H., Lörincz, A., & Somogyi, P. (2000) · Nature Neuroscience · doi:10.1038/73936 · Cited by 648
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
Deans, M. R., Gibson, J. R., Sellitto, C., Connors, B. W., & Paul, D. L. (2001) · Neuron · doi:10.1016/s0896-6273(01)00373-7 · Cited by 579
Kawaguchi, Y., & Kubota, Y. (1993) · Journal of Neurophysiology · doi:10.1152/jn.1993.70.1.387 · Cited by 558
Kawaguchi, Y. (1995) · The Journal of Neuroscience · doi:10.1523/jneurosci.15-04-02638.1995 · Cited by 533
Impaired Electrical Signaling Disrupts Gamma Frequency Oscillations in Connexin 36-Deficient Mice
Hormuzdi, S. G., Pais, I., LeBeau, F. E. N., Towers, S. K., Rozov, A., Buhl, E. H., Whittington, M. A., & Monyer, H. (2001) · Neuron · doi:10.1016/s0896-6273(01)00387-7 · Cited by 522
Neuronal networks for induced ‘40 Hz’ rhythms
Jefferys, J. G. R., Traub, R. D., & Whittington, M. A. (1996) · Trends in Neurosciences · doi:10.1016/s0166-2236(96)10023-0 · Cited by 467
Electrical synapses between Gaba-Releasing interneurons
Galarreta, M., & Hestrin, S. (2001) · Nature Reviews Neuroscience · doi:10.1038/35077566 · Cited by 434
Self-citationSimulations of cortical pyramidal neurons synchronized by inhibitory interneurons
Lytton, W. W., & B, T. J. S. A. (1991) · Journal of Neurophysiology · doi:10.1152/jn.1991.66.3.1059 · Cited by 426
Extensive dye coupling between rat neocortical neurons during the period of circuit formation
Peinado, A., Yuste, R., & Katz, L. C. (1993) · Neuron · doi:10.1016/0896-6273(93)90246-n · Cited by 391
Spike Transmission and Synchrony Detection in Networks of GABAergic Interneurons
Galarreta, M., & Hestrin, S. (2001) · Science · doi:10.1126/science.1061395 · Cited by 389
Self-citationTraub, R. D., Kopell, N., Bibbig, A., Buhl, E. H., LeBeau, F. E. N., & Whittington, M. A. (2001) · Journal of Neuroscience · doi:10.1523/jneurosci.21-23-09478.2001 · Cited by 359
Rapid Signaling at Inhibitory Synapses in a Dentate Gyrus Interneuron Network
Bartos, M., Vida, I., Frotscher, M., Geiger, J. R. P., & Jonas, P. (2001) · The Journal of Neuroscience · doi:10.1523/jneurosci.21-08-02687.2001 · Cited by 325
Mann-Metzer, P., & Yarom, Y. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-09-03298.1999 · Cited by 315
Reyes, A. D., & Sakmann, B. J. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-10-03827.1999 · Cited by 305
Coupling between neurons of the developing rat neocortex
Connors, B. W., Benardo, L. S., & Prince, D. A. (1983) · Journal of Neuroscience · doi:10.1523/jneurosci.03-04-00773.1983 · Cited by 301
Expression of Cx36 in mammalian neurons
Condorelli, D. F., Belluardo, N., Salinaro, A. T., & Mudò, G. (2000) · Brain Research Reviews · doi:10.1016/s0165-0173(99)00068-5 · Cited by 289
Meyer, A. H., Katona, I., Blatow, M., Rozov, A. V., & Monyer, H. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-16-07055.2002 · Cited by 288
Efficacy and Stability of Quantal GABA Release at a Hippocampal Interneuron–Principal Neuron Synapse
Kraushaar, U., & Jonas, P. (2000) · The Journal of Neuroscience · doi:10.1523/jneurosci.20-15-05594.2000 · Cited by 281
Expression of Connexin36 in the adult and developing rat brain
Belluardo, N., Mudò, G., Salinaro, A. T., Gurun, S. L., Charollais, A., Serre‐Beinier, V., Amato, G., Haefliger, J., Meda, P., & Condorelli, D. F. (2000) · Brain Research · doi:10.1016/s0006-8993(00)02300-3 · Cited by 281
Tamás, G., Buhl, E. H., & Somogyi, P. (1997) · The Journal of Physiology · doi:10.1113/jphysiol.1997.sp022054 · Cited by 278
Connexin expression in electrically coupled postnatal rat brain neurons
Venance, L., Rozov, A., Blatow, M., Burnashev, N., Feldmeyer, D., & Monyer, H. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.160037097 · Cited by 273
Otis, T. S., & Módy, I. (1992) · Neuroscience · doi:10.1016/0306-4522(92)90073-b · Cited by 259
Differentially Interconnected Networks of GABAergic Interneurons in the Visual Cortex of the Cat
Tamás, G., Somogyi, P., & Buhl, E. H. (1998) · Journal of Neuroscience · doi:10.1523/jneurosci.18-11-04255.1998 · Cited by 242
Hashimoto, I., Mashiko, T., & Imada, T. (1996) · Electroencephalography and Clinical Neurophysiology/Evoked Potentials Section · doi:10.1016/0168-5597(95)00244-8 · Cited by 234
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
Intracellular Correlates of Fast (>200 Hz) Electrical Oscillations in Rat Somatosensory Cortex
Jones, M. S., MacDonald, K. D., Choi, B., Dudek, F. E., & Barth, D. S. (2000) · Journal of Neurophysiology · doi:10.1152/jn.2000.84.3.1505 · Cited by 184
Kandel, E. R. (1977) · Medical Entomology and Zoology · Cited by 168
Bush, P. C., & B, T. J. S. A. (1996) · Journal of Computational Neuroscience · doi:10.1007/bf00160806 · Cited by 162
Swadlow, H. A., Beloozerova, I. N., & Sirota, M. G. (1998) · Journal of Neurophysiology · doi:10.1152/jn.1998.79.2.567 · Cited by 160
Developmental Regulation of Basket/Stellate Cell→Purkinje Cell Synapses in the Cerebellum
Pouzat, C., & Hestrin, S. (1997) · Journal of Neuroscience · doi:10.1523/jneurosci.17-23-09104.1997 · Cited by 159
Self-citationInhibitory post‐synaptic currents in rat hippocampal CA1 neurones.
Collingridge, G. L., Gage, P. W., & Robertson, B. (1984) · The Journal of Physiology · doi:10.1113/jphysiol.1984.sp015482 · Cited by 150
Propagating Activity Patterns in Large-Scale Inhibitory Neuronal Networks
Rinzel, J., Terman, D. H., Wang, X.-J., & Ermentrout, B. (1998) · Science · doi:10.1126/science.279.5355.1351 · Cited by 150
Szabadics, J., Lörincz, A., & Tamás, G. (2001) · Journal of Neuroscience · doi:10.1523/jneurosci.21-15-05824.2001 · Cited by 135
Gap junctions between dendrites in the primate neocortex
Sloper, J. J. (1972) · Brain Research · doi:10.1016/0006-8993(72)90327-7 · Cited by 131
Dunning, D. D., Hoover, C. L., Soltész, I., Smith, M. A., & O’Dowd, D. K. (1999) · Journal of Neurophysiology · doi:10.1152/jn.1999.82.6.3286 · Cited by 117
Gap junctions between dendrites and somata of neurons in the primate sensori-motor cortex
Sloper, J. J., & Powell, T. P. S. (1978) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.1978.0089 · Cited by 117
Kawai, Y., & Senba, E. (1996) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19960923)373:3 · Cited by 88
Voltage–activated sodium channels amplify inhibition in neocortical pyramidal neurons
Stuart, G. J. (1999) · Nature Neuroscience · doi:10.1038/5698 · Cited by 80
Hutcheon, B., Morley, P., & Poulter, M. O. (2000) · The Journal of Physiology · doi:10.1111/j.1469-7793.2000.t01-5-00003.xm · Cited by 73
Angulo, M. C., Staiger, J. F., Rossier, J., & Audinat, É. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-05-01566.1999 · Cited by 71
Feldman, D. E. (2000) · Nature Neuroscience · doi:10.1038/73849 · Cited by 61
Haueisen, J., Schack, B., Meier, T., Curio, G., & Okada, Y. C. (2001) · Clinical Neurophysiology · doi:10.1016/s1388-2457(01)00504-1 · Cited by 61
Morphological correlates of epilepsy: cells in the cerebral cortex.
Peters, A. (1980) · PubMed · Cited by 20
Gap junction proteins in inhibitory neurons of the adult barrel neocortex
Priest, A. J. T. C. A. (2001) · Somatosensory & Motor Research · doi:10.1080/01421590120089631 · Cited by 18
MK-801-induced expression of Fos protein family members in the rat retrosplenial granular cortex
Zhang, X., Fan, X.-D., Mohapel, P., Yu, P. H., & Boulton, A. A. (1999) · Journal of Neuroscience Research · doi:10.1002/(sici)1097-4547(19990901)57:5 · Cited by 7
Flagged first, then by citations
Research works printed but not linked: 2
- Meyer A. H. Katona I. Blatow M. Rozov A. & Monyer H. (2002) J. Neurosci. in press.
- Peters A. (1980) Adv. Neurol.27,21-48.6769303
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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
How Inhibition Shapes Cortical Activity
Isaacson, J. S., & Scanziani, M. (2011) · Neuron · doi:10.1016/j.neuron.2011.09.027 · Cited by 1,678
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Hu, H., Gan, J., & Jonas, P. (2014) · Science · doi:10.1126/science.1255263 · Cited by 1,197
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Jiang, X., Shen, S., Cadwell, C. R., Berens, P., Sinz, F., Ecker, A. S., Patel, S., & Tolias, A. S. (2015) · Science · doi:10.1126/science.aac9462 · Cited by 908
Metadata
- Authors
- Galarreta, M., & Hestrin, S.
- Affiliations
- Stanford Medicine (US)
- Corresponding author
- Galarreta, Mario
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2002-09-04
- Volume
- 99
- Issue
- 19
- Pages
- 12438-12443
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC129463
- OpenAlex
- W1992424371
- Cited by
- 387
- References
- 56
- Citations by year
- 2026: 5 · 2025: 8 · 2024: 26 · 2023: 9 · 2022: 15 · 2021: 11 · 2020: 11 · 2019: 9 · 2018: 13 · 2017: 17 · 2016: 22 · 2015: 14 · 2014: 20 · 2013: 26 · 2012: 22
- FWCI
- 5.00
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health
- National Eye Institute (R01EY012114, EY12114)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Connexins and lens biology
- Keywords
- parvalbumin interneurons, fast-spiking interneurons, electrical synapses, chemical synapses, GABAergic inhibition, neocortex, synaptic connectivity, coupling coefficient, inhibitory postsynaptic potentials, paired-pulse depression, adult mice, cortical circuits
- MeSH terms
- Action Potentials, Animals, Electrochemistry, gamma-Aminobutyric Acid, Interneurons, Luminescent Proteins, Mice, Inbred C57BL, Mice, Inbred ICR, Mice, Transgenic, Parvalbumins, Promoter Regions, Genetic, Recombinant Proteins, Synapses, Neocortex, Green Fluorescent Proteins, Mice, In Vitro Techniques
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