Two Types of Nicotinic Receptors Mediate an Excitation of Neocortical Layer I Interneurons
Open accessAbstract
Nicotinic acetylcholine receptors are widely expressed in the neocortex but their functional roles remain largely unknown. Here we investigated the effect of nicotinic receptor activation on interneurons of layer I, which contains a high density of cholinergic fiber terminals. Ninety-seven of 101 neurons recorded in whole cell configuration in rat acute slices were excited by local pressure application of nicotinic agonists, acetylcholine (500 μM), 1,1-dimethyl-4-phenyl-piperazinium (500 μM) or choline (10 mM). Biocytin labeling confirmed that our sample included different morphological types of layer I interneurons. The responses to nicotinic agonists persisted in presence of glutamate and muscarinic receptor antagonists and on further addition of Cd 2+or tetrodotoxin, indicating that they were mediated by direct activation of postsynaptic nicotinic receptors. The kinetics of the currents and their sensitivity to nicotinic receptor antagonists, methyllycaconitine (1–10 nM) or dihydro-β-erythroidine (500 nM), suggested that early and late components of the responses were mediated by α7 and non-α7 types of receptors. Both components had inwardly rectifying I-V curves, which differed when intracellular spermine was omitted. Single-cell RT-PCR experiments identified α4, α7, and β2 as the predominantly expressed mRNAs, suggesting that the receptors consisted of α7 homomers and α4β2 heteromers. Finally, selective excitation of layer I interneurons through activation of their nicotinic receptors resulted in a tetrodotoxin-sensitive increase of inhibitory synaptic currents recorded in nonpyramidal cells but not in pyramidal cells of layer II/III. These results suggest that acetylcholine released in layer I may induce a disinhibition of the cortical network through activation of nicotinic receptors expressed by layer I interneurons.
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The relative influence of external input can be enhanced by cholinergic depolarization of selective sets of inhibitory interneurons, coupled with cholinergic suppression of evoked GABAergic synaptic transmission.
“The relative influence of external input can also be enhanced by cholinergic depolarization of selective sets of inhibitory interneurons (Xiang et al., 1998; McQuiston and Madison, 1999a, b, c; Christophe et al., 2002), coupled with the cholinergic suppression of evoked GABAergic synaptic transmission (Pitler and Alger, 1992; Behrends and ten Bruggencate, 1993; Patil and Hasselmo, 1999).”
From Modes and models of forebrain cholinergic neuromodulation of cognition (2011) · cites this paper as Christophe et al., 2002
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Cites
Central cholinergic pathways in the rat: An overview based on an alternative nomenclature (Ch1–Ch6)
Mesulam, M. M., Mufson, E. J., Wainer, B. H., & Levey, A. I. (1983) · Neuroscience · doi:10.1016/0306-4522(83)90108-2 · Cited by 2,329 · see citing works
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 · see citing works
Self-citationKlink, R., d'Exaerde, A. D. K., Zoli, M., & Changeux, J.-P. (2001) · The Journal of Neuroscience · doi:10.1523/jneurosci.21-05-01452.2001 · Cited by 674 · see citing works
Trajectories of cholinergic pathways within the cerebral hemispheres of the human brain
Selden, N. (1998) · Brain · doi:10.1093/brain/121.12.2249 · Cited by 657 · see citing works
Differential regulation of neocortical synapses by neuromodulators and activity
Gil, Z., Connors, B. W., & Amitai, Y. (1997) · Neuron · doi:10.1016/s0896-6273(00)80380-3 · Cited by 553 · see citing works
AMPA receptor subunits expressed by single purkinje cells
Lambolez, B., Audinat, É., Bochet, P., Crépel, F., & Rossier, J. (1992) · Neuron · doi:10.1016/0896-6273(92)90164-9 · Cited by 544 · see citing works
Alkondon, M., & Albuquerque, E. X. (1993) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1016/s0022-3565(25)38283-2 · Cited by 538 · see citing works
Kawaguchi, Y. (1995) · The Journal of Neuroscience · doi:10.1523/jneurosci.15-04-02638.1995 · Cited by 533 · see citing works
Mechanisms of action of acetylcholine in the guinea‐pig cerebral cortex in vitro.
McCormick, D. A., & Prince, D. A. (1986) · The Journal of Physiology · doi:10.1113/jphysiol.1986.sp016112 · Cited by 499 · see citing works
Nicotinic acetylcholine binding sites in Alzheimer's disease
Whitehouse, P. J., Martino, A. M., Antuono, P., Lowenstein, P. R., Coyle, J. T., Price, D. L., & Kellar, K. J. (1986) · Brain Research · doi:10.1016/0006-8993(86)90819-x · Cited by 485 · see citing works
Choline is a Selective Agonist of α7 Nicotinic Acetylcholine Receptors in the Rat Brain Neurons
Alkondon, M., Pereira, E. F. R., Cartes, W. S., Maelicke, A., & Albuquerque, E. X. (1997) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.1997.tb01702.x · Cited by 441 · see citing works
Cholinergic Switching Within Neocortical Inhibitory Networks
Xiang, Z., Huguenard, J. R., & Prince, D. A. (1998) · Science · doi:10.1126/science.281.5379.985 · Cited by 438 · see citing works
Identification of Four Classes of Brain Nicotinic Receptors Using β2 Mutant Mice
Zoli, M., Léna, C., Picciotto, M. R., & Changeux, J. (1998) · Journal of Neuroscience · doi:10.1523/jneurosci.18-12-04461.1998 · Cited by 401 · see citing works
Identification of four classes of brain nicotinic receptors using beta2 mutant mice.
Zoli, M., Léna, C., Picciotto, M. R., & Changeux, J. (1998) · PubMed Central · doi:10.1523/jneurosci.18-12-04461.1996 · Cited by 387 · see citing works
Frazier, C. J., Rollins, Y. D., Breese, C. R., Leonard, S., Freedman, R., & Dunwiddie, T. V. (1998) · The Journal of Neuroscience · doi:10.1523/jneurosci.18-04-01187.1998 · Cited by 374 · see citing works
Fakler, B., Brändle, U., Glowatzki, E., et al. (1995) · Cell · doi:10.1016/0092-8674(95)90459-x · Cited by 355 · see citing works
Alkondon, M., Pereira, E. F. R., Eisenberg, H. M., & Albuquerque, E. X. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-07-02693.1999 · Cited by 332 · see citing works
Alkondon, M., Pereira, E. F. R., Barbosa, C. T. F., & Albuquerque, E. X. (1997) · PubMed · Cited by 326 · see citing works
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 · see citing works
Selective Excitation of Subtypes of Neocortical Interneurons by Nicotinic Receptors
Porter, J. T., Cauli, B., Tsuzuki, K., Lambolez, B., Rossier, J., & Audinat, E. (1999) · The Journal of Neuroscience · doi:10.1523/jneurosci.19-13-05228.1999 · Cited by 262 · see citing works
Self-citationVidal, C., & Changeux, J. (1993) · Neuroscience · doi:10.1016/0306-4522(93)90558-w · Cited by 240 · see citing works
Nicotinic Receptor Activation Excites Distinct Subtypes of Interneurons in the Rat Hippocampus
McQuiston, A. R., & Madison, D. V. (1999) · The Journal of Neuroscience · doi:10.1523/jneurosci.19-08-02887.1999 · Cited by 239 · see citing works
Palma, E., Bertrand, S., Binzoni, T., & Bertrand, D. (1996) · The Journal of Physiology · doi:10.1113/jphysiol.1996.sp021203 · Cited by 218 · see citing works
Khiroug, S. S., Harkness, P. C., Lamb, P. W., Sudweeks, S. N., Khiroug, L. S., Millar, N. S., & Yakel, J. L. (2002) · The Journal of Physiology · doi:10.1113/jphysiol.2001.013847 · Cited by 215 · see citing works
Sudweeks, S. N., & Yakel, J. L. (2000) · The Journal of Physiology · doi:10.1111/j.1469-7793.2000.00515.x · Cited by 197 · see citing works
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 · see citing works
Polyamine-dependent facilitation of postsynaptic AMPA receptors counteracts paired-pulse depression
Rozov, A., & Burnashev, N. (1999) · Nature · doi:10.1038/44151 · Cited by 192 · see citing works
Zwart, R., & Vijverberg, H. P. M. (1997) · Molecular Pharmacology · doi:10.1124/mol.52.5.886 · Cited by 157 · see citing works
Morphology and spatial distribution of GABAergic neurons in cat primary auditory cortex (AI)
Prieto, J. J., Peterson, B. A., & Winer, J. A. (1994) · The Journal of Comparative Neurology · doi:10.1002/cne.903440304 · Cited by 148 · see citing works
Yu, C., & Role, L. W. (1998) · The Journal of Physiology · doi:10.1111/j.1469-7793.1998.651bm.x · Cited by 148 · see citing works
Granon, S., Poucet, B., Thinus‐Blanc, C., Changeux, J., & Vidal, C. (1995) · Psychopharmacology · doi:10.1007/bf02246154 · Cited by 141 · see citing works
Mike, Á., Castro, N. G., & Albuquerque, E. X. (2000) · Brain Research · doi:10.1016/s0006-8993(00)02863-8 · Cited by 131 · see citing works
Alkondon, M., Pereira, E. F. R., Barbosa, C. T. F., & Albuquerque, E. X. (1997) · The Journal of Pharmacology and Experimental Therapeutics · doi:10.1016/s0022-3565(24)37139-3 · Cited by 127 · see citing works
Everitt, B. J., Sirkiä, T. E., Roberts, A., Jones, G. H., & Robbins, T. W. (1988) · The Journal of Comparative Neurology · doi:10.1002/cne.902710406 · Cited by 112 · see citing works
Neurons in layer I of the developing occipital cortex of the rat
Bradford, R., Parnavels, J. G., & Lieberman, A. R. (1977) · The Journal of Comparative Neurology · doi:10.1002/cne.901760108 · Cited by 103 · see citing works
James, J. R., & Nordberg, A. K. (1995) · Behavior Genetics · doi:10.1007/bf02196924 · Cited by 98 · see citing works
Albuquerque, E. X., Pereira, E. F. R., Mike, Á., Eisenberg, H. M., Maelicke, A., & Alkondon, M. (2000) · Behavioural Brain Research · doi:10.1016/s0166-4328(00)00208-4 · Cited by 95 · see citing works
Haghighi, A. P., & Cooper, E. (1998) · Journal of Neuroscience · doi:10.1523/jneurosci.18-11-04050.1998 · Cited by 94 · see citing works
Morphological properties of intracellularly labeled layer I neurons in rat neocortex
Zhou, F.-M., & Hablitz, J. J. (1996) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19961209)376:2 · Cited by 79 · see citing works
Populations of GABAergic neurons and axons in layer I of rat auditory cortex
Winer, J. A., & Larue, D. T. (1989) · Neuroscience · doi:10.1016/0306-4522(89)90402-8 · Cited by 76 · see citing works
Haghighi, A. P., & Cooper, E. (2000) · Journal of Neuroscience · doi:10.1523/jneurosci.20-02-00529.2000 · Cited by 75 · see citing works
M-current in human neocortical neurones
Halliwell, J. V. (1986) · Neuroscience Letters · doi:10.1016/0304-3940(86)90198-9 · Cited by 73 · see citing works
Uchida, S., Kagitani, F., Nakayama, H., & Sato, A. (1997) · Neuroscience Letters · doi:10.1016/s0304-3940(97)00401-1 · Cited by 70 · see citing works
Kristt, D. A., McGowan, R. A., Martin-MacKinnon, N., & Solomon, J. (1985) · Brain Research · doi:10.1016/0006-8993(85)91606-3 · Cited by 69 · see citing works
Muscarinic and nicotinic contributions to cognitive function and cortical blood flow
Gitelman, D. R., & Prohovnik, I. (1992) · Neurobiology of Aging · doi:10.1016/0197-4580(92)90044-x · Cited by 66 · see citing works
Buhler, A. V., & Dunwiddie, T. V. (2001) · Neuroscience · doi:10.1016/s0306-4522(01)00257-3 · Cited by 54 · see citing works
Gabbott, P. L. A., & Bacon, S. J. (1997) · Brain Research · doi:10.1016/s0006-8993(96)01232-2 · Cited by 37 · see citing works
Distribution and proportions of GABA‐Immunoreactive neurons in cat primary somatosensory cortex
Li, J., & Schwark, H. D. (1994) · The Journal of Comparative Neurology · doi:10.1002/cne.903430302 · Cited by 29 · see citing works
Martin, K. A. C., Friedlander, M. J., & Alones, V. (1989) · The Journal of Comparative Neurology · doi:10.1002/cne.902820307 · Cited by 28 · see citing works
Distribution of mRNAs encoding CRF receptors in brain and pituitary of rat and mouse
Van Pett, K., Viau, V., Bittencourt, J. C., Chan, R. K. W., Li, H.-Y., Arias, C., Prins, G. S., Perrin, M., Vale, W., & Sawchenko, P. E. (2000) · The Journal of Comparative Neurology · doi:10.1002/1096-9861(20001211)428:2
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Letzkus, J. J., Wolff, S. B. E., Meyer, E. M. M., Tovote, P., Courtin, J., Herry, C., & Lüthi, A. (2011) · Nature · doi:10.1038/nature10674 · Cited by 840 · see citing works
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Hasselmo, M. E., & Sarter, M. (2011) · Neuropsychopharmacology · doi:10.1038/npp.2010.104 · Cited by 733 · see citing works
Feldmeyer, D., Brecht, M., Helmchen, F., Petersen, C. C. H., Poulet, J. F. A., Staiger, J. F., Luhmann, H. J., & Schwarz, C. (2013) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2012.11.002 · Cited by 354 · see citing works
“Together, ACh-related effects may increase signal to noise ratio for behaviorally relevant signals (Gil et al., 1997; Oldford and CastroAlamancos, 2003; Gulledge and Stuart, 2005; Eggermann and Feldmeyer, 2009; Gulledge and Kawaguchi, 2007; Porter et al., 1999; Christophe et al., 2002).”
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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
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- Authors
- Christophe, E., Roebuck, A., Staiger, J. F., Lavery, D. J., Charpak, S., & Audinat, E.
- Affiliations
- Inserm (FR)
- GlaxoSmithKline (Switzerland) (CH)
- Heinrich Heine University Düsseldorf (DE)
- Laboratoire de Neurophysiologie, Institut National de la Santé et de la Recherche Médicale EPI 0002, ESPCI, 75231 Paris Cedex 5, France;
- Venue
- Journal of Neurophysiology
- Publisher
- American Physiological Society
- Published
- 2002-09-01
- Volume
- 88
- Issue
- 3
- Pages
- 1318-1327
- ISSN
- 0022-3077 (ISSN-L)
- 1522-1598
- OpenAlex
- W1840472544
- Cited by
- 130
- References
- 50
- Citations by year
- 2026: 2 · 2025: 2 · 2024: 2 · 2023: 2 · 2022: 1 · 2021: 4 · 2020: 4 · 2019: 3 · 2018: 6 · 2017: 4 · 2016: 7 · 2015: 9 · 2014: 17 · 2013: 11 · 2012: 11
- FWCI
- 1.62
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Journal of Neurophysiology (publishedVersion)
- PubMed (publishedVersion)
- Funders
- École Supérieure de Physique et de Chimie Industrielles de la Ville de Paris
- Centre National de la Recherche Scientifique
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Nicotinic Acetylcholine Receptors Study
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Ion channel regulation and function
- Keywords
- nicotinic acetylcholine receptors, acetylcholine, alpha7 nicotinic acetylcholine receptor, alpha4beta2 nicotinic receptor, cholinergic interneurons, disinhibition, methyllycaconitine, dihydro-beta-erythroidine, choline
- MeSH terms
- Animals, Electrophysiology, Interneurons, Receptors, Nicotinic, RNA, Messenger, Synapses, Rats, Wistar, Nicotinic Agonists, Neocortex, Rats, alpha7 Nicotinic Acetylcholine Receptor, In Vitro Techniques
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