Prolonged disynaptic inhibition in the cortex mediated by slow, non-α7 nicotinic excitation of a specific subset of cortical interneurons
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Cholinergic activation of nicotinic receptors in the cortex plays a critical role in arousal, attention, and learning. Here we demonstrate that cholinergic axons from the basal forebrain of mice excite a specific subset of cortical interneurons via a remarkably slow, non-α7 nicotinic receptor-mediated conductance. In turn, these inhibitory cells generate a delayed and prolonged wave of disynaptic inhibition in neighboring cortical neurons, altering the spatiotemporal pattern of inhibition in cortical circuits.
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Anatomical, pharmacological, and optogenetic evidence support the view that neuromodulatory centers rapidly activate Vip interneurons.
“Anatomical, pharmacological and optogenetic evidence support this view (Acsady et al., 1993; Arroyo et al., 2012; Choi and Callaway, 2011; Ferezou et al., 2002; Lee et al., 2010).”
From GABAergic Interneurons in the Neocortex: From Cellular Properties to Circuits (2016) · cites this paper as Arroyo et al., 2012
The Results show that brief optogenetic stimulation of basal-forebrain cholinergic fibers elicited nicotinic responses in ChAT-expressing bipolar interneurons; the Discussion refers to cortical ChAT/VIP interneurons. But the Discussion says these bipolar cells exhibited only a slow response, and the Results place most evoked action potentials at 30–180 ms. The source supports activation of this interneuron subset, not the unqualified description of it as rapid. (LLM, conf=0.84)
Experimental — accuracy not yet measuredFS cells express high levels of voltage-gated K+ channels of the Kv3 subfamily with depolarized activation and fast deactivation, specialized for rapid repolarization with little interference during the inter-spike interval.
“Expression of high levels of voltage-gated K+ channels with a depolarized activation voltage and fast deactivation rates of the Kv3 subfamily; channels specialized for rapid repolarization with little interference during the inter-spike interval.”
From GABAergic Interneurons in the Neocortex: From Cellular Properties to Circuits (2016) · cites this paper as [10]
Materials and Methods (Identification of interneuron subtypes; page unavailable) describes how fast-spiking cells were identified and reports their firing pattern. Searches for Kv3 channels, their activation and deactivation, and their role in repolarization found no passage in our copy addressing those claims. (LLM, conf=0.76)
Experimental — accuracy not yet measuredKv3 channels contribute to a large and fast afterhyperpolarization that facilitates recovery of Na+ channels from inactivation.
“Kv3 channels also contribute to the generation of a large and fast AHP that facilitates the recovery of Na+ channels from inactivation9–11.”
From GABAergic Interneurons in the Neocortex: From Cellular Properties to Circuits (2016) · cites this paper as [10]
The Results and Discussion passages describe nicotinic receptor-mediated responses and inhibition, not Kv3 channels or afterhyperpolarization. Searches for Kv3, AHP, and Na+ channel recovery found no passage in our copy addressing the attributed mechanism; page numbers were not available. (LLM, conf=0.76)
Experimental — accuracy not yet measuredThe fast inhibition is at least partially mediated by the actions of both nicotinic and muscarinic receptors that increase the excitability and firing rates of dendrite-targeting GABAergic interneurons.
“The fast inhibition is at least partially mediated by the actions of both nAChRs and mAChRs that increase the excitability and firing rates of dendrite-targeting GABAergic interneurons (Arroyo et al., 2012; Couey et al., 2007; Fanselow et al., 2008; Ferezou et al., 2002; Gulledge et al., 2007; Kawaguchi and Kubota, 1997).”
From Acetylcholine as a Neuromodulator: Cholinergic Signaling Shapes Nervous System Function and Behavior (2012) · cites this paper as Arroyo et al., 2012
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Cites
The distinct modes of vision offered by feedforward and recurrent processing
Lamme, V. A. F., & Roelfsema, P. R. (2000) · Trends in Neurosciences · doi:10.1016/s0166-2236(00)01657-x · Cited by 2,338 · cited 1× · see citing works
“Moreover we propose that, given the delayed kinetics of the IPSC barrage, sensory activation of the BF will preferentially impact long latency intracortical activity over the initial feedforward sensory response (Lamme and Roelfsema, 2000).”
Corbetta, M., Miezin, F. M., Dobmeyer, S., Shulman, G. L., & Petersen, S. (1991) · Journal of Neuroscience · doi:10.1523/jneurosci.11-08-02383.1991 · Cited by 1,590 · see citing works
Three groups of interneurons account for nearly 100% of neocortical GABAergic neurons
Rudy, B., Fishell, G., Lee, S., & Hjerling‐Leffler, J. (2011) · Developmental Neurobiology · doi:10.1002/dneu.20853 · Cited by 1,420 · see citing works
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 · see citing works
Tamamaki, N., Yanagawa, Y., Tomioka, R., Miyazaki, J., Obata, K., & Kaneko, T. (2003) · The Journal of Comparative Neurology · doi:10.1002/cne.10905 · Cited by 1,277 · see citing works
Nicotinic Acetylcholine Receptors and Nicotinic Cholinergic Mechanisms of the Central Nervous System
Dani, J. A., & Bertrand, D. (2007) · Annual Review of Pharmacology and Toxicology · doi:10.1146/annurev.pharmtox.47.120505.105214 · Cited by 1,197 · see citing works
Steinlein, O. K., Mulley, J. C., Propping, P., Wallace, R. H., Phillips, H. A., Sutherland, G. R., Scheffer, I. E., & Berkovic, S. F. (1995) · Nature Genetics · doi:10.1038/ng1095-201 · Cited by 1,134 · see citing works
Gong, S., Doughty, M., Harbaugh, C. R., Cummins, A., Hatten, M. E., Heintz, N., & Gerfen, C. R. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.2707-07.2007 · Cited by 977 · see citing works
A disinhibitory microcircuit for associative fear learning in the auditory cortex
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
Rye, D. B., Wainer, B. H., Mesulam, M.-M., Mufson, E. J., & Saper, C. B. (1984) · Neuroscience · doi:10.1016/0306-4522(84)90083-6 · Cited by 743 · see citing works
Optogenetic interrogation of neural circuits: technology for probing mammalian brain structures
Zhang, F., Gradinaru, V., Adamantidis, A. R., Durand, R., Airan, R. D., de Lecea, L., & Deisseroth, K. (2010) · Nature Protocols · doi:10.1038/nprot.2009.226 · Cited by 692 · see citing works
Rossi, J., Balthasar, N., Olson, D., Scott, M., Berglund, E., Lee, C. E., Choi, M. J., Lauzon, D., Lowell, B. B., & Elmquist, J. K. (2011) · Cell Metabolism · doi:10.1016/j.cmet.2011.01.010 · Cited by 672 · see citing works
Cortical GABA Interneurons in Neurovascular Coupling: Relays for Subcortical Vasoactive Pathways
Cauli, B., Tong, X., Rancillac, A., Serluca, N., Lambolez, B., Rossier, J., & Hamel, É. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.3065-04.2004 · Cited by 568 · see citing works
Kawaguchi, Y. (1995) · The Journal of Neuroscience · doi:10.1523/jneurosci.15-04-02638.1995 · Cited by 533 · see citing works
Azouz, R., & Gray, C. M. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.130200797 · Cited by 526 · 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
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
Cognitive functions of the basal forebrain
Baxter, M. G., & Chiba, A. A. (1999) · Current Opinion in Neurobiology · doi:10.1016/s0959-4388(99)80024-5 · Cited by 351 · see citing works
Phasic acetylcholine release and the volume transmission hypothesis: time to move on
Sarter, M. F., Parikh, V., & Howe, W. M. (2009) · Nature reviews. Neuroscience · doi:10.1038/nrn2635 · Cited by 340 · see citing works
Timing-Dependent Septal Cholinergic Induction of Dynamic Hippocampal Synaptic Plasticity
Gu, Z., & Yakel, J. L. (2011) · Neuron · doi:10.1016/j.neuron.2011.04.026 · Cited by 286 · see citing works
Alkondon, M., Pereira, E. F. R., & Albuquerque, E. X. (1998) · Brain Research · doi:10.1016/s0006-8993(98)00880-4 · Cited by 263 · 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
Umbriaco, D., Watkins, K. C., Descarries, L., Cozzari, C., & Hartman, B. K. (1994) · The Journal of Comparative Neurology · doi:10.1002/cne.903480304 · Cited by 237 · see citing works
Ji, D., & Dani, J. A. (2000) · Journal of Neurophysiology · doi:10.1152/jn.2000.83.5.2682 · Cited by 231 · see citing works
Heterogeneity of phasic cholinergic signaling in neocortical neurons
Gulledge, A. T., Park, S. B., Kawaguchi, Y., & Stuart, G. J. (2007) · Journal of Neurophysiology · doi:10.1152/jn.00493.2006 · Cited by 194 · see citing works
Nicotinic acetylcholine receptor β2 subunits in the medial prefrontal cortex control attention
Guillem, K., Bloem, B., Poorthuis, R. B., Loos, M., Smit, A. B., Maskos, U., Spijker, S., & Mansvelder, H. D. (2011) · Science · doi:10.1126/science.1207079 · Cited by 191 · see citing works
Gap-Junctional Coupling between Neurogliaform Cells and Various Interneuron Types in the Neocortex
Simon, A., Oláh, S., Molnár, G., Szabadics, J., & Tamás, G. (2005) · The Journal of Neuroscience · doi:10.1523/jneurosci.1431-05.2005 · Cited by 163 · see citing works
Howe, W. M., Ji, J., Parikh, V., Williams, S., Mocaër, E., Trocmé-Thibierge, C., & Sarter, M. (2010) · Neuropsychopharmacology · doi:10.1038/npp.2010.9 · Cited by 150 · cited 2× · see citing works
“Nicotinic acetylcholine receptors (nAChRs) have been shown to play an important role in attention (Howe et al., 2010; Guillem et al., 2011) and learning (Letzkus et al., 2011), and gain of function mutations in a non- 7 receptor subunit has been linked to a heritable form of epilepsy (Steinlein et…”
BackgroundKocharyan, A., Fernandes, P., Tong, X., Vaucher, E., & Hamel, É. (2007) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1038/sj.jcbfm.9600558 · Cited by 146 · see citing works
Turrini, P., Casu, M. A., Wong, T. P., De Koninck, Y., Ribeiro-da-Silva, A., & Cuello, A. C. (2001) · Neuroscience · doi:10.1016/s0306-4522(01)00172-5 · Cited by 135 · see citing works
Two Types of Nicotinic Receptors Mediate an Excitation of Neocortical Layer I Interneurons
Christophe, E., Roebuck, A., Staiger, J. F., Lavery, D. J., Charpak, S., & Audinat, E. (2002) · Journal of Neurophysiology · doi:10.1152/jn.2002.88.3.1318 · Cited by 130 · see citing works
Cholinergic synapses in human cerebral cortex: an ultrastructural study in serial sections
Smiley, J. F., Morrell, F., & Mesulam, M. M. (1997) · Experimental Neurology · doi:10.1006/exnr.1997.6413 · Cited by 79 · see citing works
Mapping the Visual Recognition Memory Network with PET in the Behaving Baboon
Blaizot, X., Landeau, B., Baron, J., & Chavoix, C. (2000) · Journal of Cerebral Blood Flow & Metabolism · doi:10.1097/00004647-200002000-00001 · Cited by 31 · see citing works
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GABAergic Interneurons in the Neocortex: From Cellular Properties to Circuits
Tremblay, R., Lee, S., & Rudy, B. (2016) · Neuron · doi:10.1016/j.neuron.2016.06.033 · Cited by 2,033 · see citing works
Acetylcholine as a Neuromodulator: Cholinergic Signaling Shapes Nervous System Function and Behavior
Picciotto, M. R., Higley, M. J., & Mineur, Y. S. (2012) · Neuron · doi:10.1016/j.neuron.2012.08.036 · Cited by 1,404 · see citing works
Cortical interneurons that specialize in disinhibitory control
Pi, H.-J., Hangya, B., Kvitsiani, D., Sanders, J. I., Huang, Z. J., & Kepecs, A. (2013) · Nature · doi:10.1038/nature12676 · Cited by 1,136 · see citing works
A Cortical Circuit for Gain Control by Behavioral State
Fu, Y., Tucciarone, J. M., Espinosa, J. S., Sheng, N., Darcy, D. P., Nicoll, R. A., Huang, Z. J., & Stryker, M. P. (2014) · Cell · doi:10.1016/j.cell.2014.01.050 · Cited by 937 · see citing works
“No fast nAChR component like that shown in layer I inhibitory neurons (Letzkus et al., 2011) was evident; our findings showed instead a response with slow kinetics resembling what has been found in ChATpositive bipolar neurons (Arroyo et al., 2012).”
BackgroundResultInfluentialCorticostriatal connectivity and its role in disease
Shepherd, G. M. G. (2013) · Nature Reviews Neuroscience · doi:10.1038/nrn3469 · Cited by 824 · see citing works
Balancing Plasticity/Stability Across Brain Development
Takesian, A. E., & Hensch, T. K. (2013) · Progress in Brain Research · doi:10.1016/b978-0-444-63327-9.00001-1 · Cited by 667 · see citing works
Inhibition dominates sensory responses in the awake cortex
Haider, B., Häusser, M., & Carandini, M. (2012) · Nature · doi:10.1038/nature11665 · Cited by 541 · see citing works
Pakan, J. M., Lowe, S. C., Dylda, E., Keemink, S. W., Currie, S. P., Coutts, C. A., & Rochefort, N. L. (2016) · eLife · doi:10.7554/elife.14985 · Cited by 282 · see citing works
“Previous work has demonstrated cholinergic facilitation of cortical inhibitory neurons (Kawaguchi, 1997; Xiang et al., 1998; Arroyo et al., 2012; Alitto and Dan, 2012), including SST neurons (Kawaguchi, 1997; Fanselow et al., 2008; Xu et al., 2013; Chen et al., 2015).”
BackgroundThalamic control of layer 1 circuits in prefrontal cortex
Cruikshank, S. J., Ahmed, O. J., Stevens, T. R., Patrick, S. L., Gonzalez, A. N., Elmaleh, M., & Connors, B. W. (2012) · The Journal of Neuroscience · doi:10.1523/jneurosci.3231-12.2012 · Cited by 212 · see citing works
An acetylcholine-activated microcircuit drives temporal dynamics of cortical activity
Chen, N., Sugihara, H., & Sur, M. (2015) · Nature Neuroscience · doi:10.1038/nn.4002 · Cited by 210 · see citing works
Corelease of acetylcholine and GABA from cholinergic forebrain neurons
Saunders, A., Granger, A. J., & Sabatini, B. L. (2015) · eLife · doi:10.7554/elife.06412 · Cited by 200 · see citing works
Nelson, A., & MOONEY, R. D. (2016) · Neuron · doi:10.1016/j.neuron.2016.03.031 · Cited by 190 · see citing works
Nicotine reverses hypofrontality in animal models of addiction and schizophrenia
Koukouli, F., Rooy, M., Tziotis, D., Sailor, K. A., O’Neill, H. C., Levenga, J., Witte, M., Nilges, M., Changeux, J., Hoeffer, C. A., et al. (2017) · Nature Medicine · doi:10.1038/nm.4274 · Cited by 182 · see citing works
Layer- and Cell Type-Specific Modulation of Excitatory Neuronal Activity in the Neocortex
Radnikow, G., & Feldmeyer, D. (2018) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2018.00001 · Cited by 180 · see citing works
Neuromodulation by acetylcholine: examples from schizophrenia and depression
Higley, M. J., & Picciotto, M. R. (2014) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2014.06.004 · Cited by 184 · see citing works
A transcriptomic axis predicts state modulation of cortical interneurons
Bugeon, S., Duffield, J. A. M., Dipoppa, M., Ritoux, A., Prankerd, I., Nicoloutsopoulos, D., Orme, D., Shinn, M., Peng, H., Forrest, H., et al. (2022) · Nature · doi:10.1038/s41586-022-04915-7 · Cited by 177 · see citing works
Layer 6 Corticothalamic Neurons Activate a Cortical Output Layer, Layer 5a
Kim, J., Matney, C. J., Blankenship, A. G., Hestrin, S., & Brown, S. P. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.1325-14.2014 · Cited by 169 · see citing works
Self-citationFan, L. Z., Kheifets, S., Böhm, U. L., Wu, H., Piatkevich, K. D., Xie, M. E., Parot, V., Ha, Y., Evans, K. E., Boyden, E. S., et al. (2020) · Cell · doi:10.1016/j.cell.2020.01.001 · Cited by 155 · see citing works
Cell-type-specific modulation of neocortical activity by basal forebrain input
Alitto, H. J., & Dan, Y. (2013) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2012.00079 · Cited by 156 · see citing works
Bloem, B., Poorthuis, R. B., & Mansvelder, H. D. (2014) · Frontiers in Neural Circuits · doi:10.3389/fncir.2014.00017 · Cited by 146 · see citing works
Therapeutic Potential of α7 Nicotinic Acetylcholine Receptors
Bertrand, D., Lee, C., Flood, D. G., Marger, F., & Donnelly‐Roberts, D. L. (2015) · Pharmacological Reviews · doi:10.1124/pr.113.008581 · Cited by 139 · see citing works
Bloem, B., Schoppink, L., Rotaru, D. C., Faiz, A., Hendriks, P., Mansvelder, H. D., van de Berg, W. D. J., & Wouterlood, F. G. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.3011-14.2014 · Cited by 133 · see citing works
Cholinergic modulation of spatial learning, memory and navigation
Solari, N., & Hangya, B. (2018) · European Journal of Neuroscience · doi:10.1111/ejn.14089 · Cited by 139 · see citing works
Importance of the nicotinic acetylcholine receptor system in the prefrontal cortex
Wallace, T. L., & Bertrand, D. (2013) · Biochemical Pharmacology · doi:10.1016/j.bcp.2013.04.001 · Cited by 133 · see citing works
Cellular, Synaptic and Network Effects of Acetylcholine in the Neocortex
Colangelo, C., Shichkova, P., Keller, D. X., Markram, H., & Ramaswamy, S. (2019) · Frontiers in Neural Circuits · doi:10.3389/fncir.2019.00024 · Cited by 134 · see citing works
Spatiotemporal specificity in cholinergic control of neocortical function
Muñoz, W., & Rudy, B. (2014) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2014.02.015 · Cited by 122 · see citing works
A Dendritic Substrate for the Cholinergic Control of Neocortical Output Neurons
Williams, S. R., & Fletcher, L. N. (2018) · Neuron · doi:10.1016/j.neuron.2018.11.035 · Cited by 125 · see citing works
Impact of Basal Forebrain Cholinergic Inputs on Basolateral Amygdala Neurons
Ünal, Ç. T., Paré, D., & Záborszky, L. (2015) · Journal of Neuroscience · doi:10.1523/jneurosci.2706-14.2015 · Cited by 124 · see citing works
Chrna2-Martinotti cells synchronize layer 5 type A pyramidal cells via rebound excitation
Hilscher, M. M., Leão, R. N., Edwards, S. J., Leão, K. E., & Kullander, K. (2017) · PLoS Biology · doi:10.1371/journal.pbio.2001392 · Cited by 118 · see citing works
Lin, S., Brown, R. E., Shuler, M. G. H., Petersen, C. C. H., & Kepecs, Á. (2015) · Journal of Neuroscience · doi:10.1523/jneurosci.2590-15.2015 · Cited by 117 · see citing works
Normalization and the Cholinergic Microcircuit: A Unified Basis for Attention
Schmitz, T. W., & Duncan, J. (2018) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2018.02.011 · Cited by 116 · see citing works
The Cortical States of Wakefulness
Poulet, J. F. A., & Crochet, S. (2019) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2018.00064 · Cited by 119 · see citing works
Lecrux, C., & Hamel, É. (2016) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2015.0350 · Cited by 117 · see citing works
Cotransmission of acetylcholine and GABA
Granger, A. J., Mulder, N., Saunders, A. B., & Sabatini, B. L. (2015) · Neuropharmacology · doi:10.1016/j.neuropharm.2015.07.031 · Cited by 98 · see citing works
Obermayer, J., Heistek, T. S., Kerkhofs, A., Goriounova, N. A., Kroon, T., Baayen, J. C., Idema, S., Testa-Silva, G., Couey, J. J., & Mansvelder, H. D. (2018) · Nature Communications · doi:10.1038/s41467-018-06628-w · Cited by 102 · see citing works
Borden, P. M., Zhang, P., Shivange, A. V., Marvin, J. S., Cichon, J., Dan, C., Podgorski, K., Figueiredo, A. M. P. D., Novák, O., Tanimoto, M., et al. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.02.07.939504 · Cited by 94 · see citing works
Obermayer, J., Verhoog, M. B., Luchicchi, A., & Mansvelder, H. D. (2017) · Frontiers in Neural Circuits · doi:10.3389/fncir.2017.00100 · Cited by 98 · see citing works
Layer-specific cholinergic control of human and mouse cortical synaptic plasticity
Verhoog, M. B., Obermayer, J., Kortleven, C., Wilbers, R., Wester, J., Baayen, J. C., de Kock, C. P. J., Meredith, R. M., & Mansvelder, H. D. (2016) · Nature Communications · doi:10.1038/ncomms12826 · Cited by 95 · see citing works
Precisely Timed Nicotinic Activation Drives SST Inhibition in Neocortical Circuits
Urban-Ciecko, J., Jouhanneau, J.-S., Myal, S. E., Poulet, J. F. A., & Barth, A. L. (2018) · Neuron · doi:10.1016/j.neuron.2018.01.037 · Cited by 93 · see citing works
From circuit motifs to computations: mapping the behavioral repertoire of cortical interneurons
Hangya, B., Pi, H.-J., Kvitsiani, D., Ranade, S., & Kepecs, Á. (2014) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2014.01.007 · Cited by 90 · see citing works
Zhang, G., Sun, W., Zingg, B., Shen, L., He, J., Xiong, Y., Tao, H. W., & Zhang, L. I. (2017) · Neuron · doi:10.1016/j.neuron.2017.12.010 · Cited by 90 · see citing works
Cell-type-specific nicotinic input disinhibits mouse barrel cortex during active sensing
Gasselin, C., Hohl, B., Vernet, A., Crochet, S., & Petersen, C. C. H. (2021) · Neuron · doi:10.1016/j.neuron.2020.12.018 · Cited by 90 · 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
Activity-Dependent Modulation of Layer 1 Inhibitory Neocortical Circuits by Acetylcholine
Brombas, A., Fletcher, L. N., & Williams, S. R. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.4470-13.2014 · Cited by 88 · see citing works
Acetylcholine excites neocortical pyramidal neurons via nicotinic receptors
Hedrick, T. P., & Waters, J. (2015) · Journal of Neurophysiology · doi:10.1152/jn.00716.2014 · Cited by 86 · see citing works
Obermayer, 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
Mechanisms Generating Dual-Component Nicotinic EPSCs in Cortical Interneurons
Bennett, C., Arroyo, S., Berns, D. S., & Hestrin, S. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.3565-12.2012 · Cited by 80 · see citing works
Self-citationSun, Y.-G., Pita‐Almenar, J. D., Wu, C., Renger, J. J., Uebele, V. N., Lu, H., & Beierlein, M. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.3177-12.2013 · Cited by 79 · see citing works
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Action and learning shape the activity of neuronal circuits in the visual cortex
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Ren, C., Peng, K., Yang, R., Liu, W., Liu, C., & Komiyama, T. (2022) · Neuron · doi:10.1016/j.neuron.2022.04.031 · Cited by 74 · see citing works
Functional diversity of supragranular GABAergic neurons in the barrel cortex
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Antagonism of the 5-HT 6 receptor – Preclinical rationale for the treatment of Alzheimer's disease
de Jong, I. E. M., & Mørk, A. (2017) · Neuropharmacology · doi:10.1016/j.neuropharm.2017.07.010 · Cited by 76 · see citing works
Rapid Neuromodulation of Layer 1 Interneurons in Human Neocortex
Poorthuis, R. B., Muhammad, K., Wang, M., Verhoog, M. B., Junek, S., Wrana, A., Mansvelder, H. D., & Letzkus, J. J. (2018) · Cell Reports · doi:10.1016/j.celrep.2018.03.111 · Cited by 70 · see citing works
Mesik, L., Ma, W., Li, L., Ibrahim, L. A., Huang, Z. J., Zhang, L. I., & Tao, H. W. (2015) · Frontiers in Neural Circuits · doi:10.3389/fncir.2015.00022 · Cited by 69 · see citing works
Luchicchi, A., Bloem, B., Viaña, J. N. M., Mansvelder, H. D., & Role, L. W. (2014) · Frontiers in Synaptic Neuroscience · doi:10.3389/fnsyn.2014.00024 · Cited by 70 · see citing works
Target selectivity of septal cholinergic neurons in the medial and lateral entorhinal cortex
Desikan, S., Koser, D. E., Neitz, A., & Monyer, H. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1716531115 · Cited by 69 · see citing works
Yiannakas, A., & Rosenblum, K. (2017) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2017.00335 · Cited by 69 · see citing works
Helboe, L., Egebjerg, J., & de Jong, I. E. M. (2015) · Neuroscience · doi:10.1016/j.neuroscience.2015.09.064 · Cited by 66 · see citing works
Nicotinic modulation of cortical circuits
Arroyo, S., Bennett, C., & Hestrin, S. (2014) · Frontiers in Neural Circuits · doi:10.3389/fncir.2014.00030 · Cited by 64 · see citing works
Self-citationPoorthuis, R. B., Enke, L., & Letzkus, J. J. (2014) · The Journal of Physiology · doi:10.1113/jphysiol.2014.273862 · Cited by 64 · see citing works
Response-dependent dynamics of cell-specific inhibition in cortical networks in vivo
El-Boustani, S., & Sur, M. (2014) · Nature Communications · doi:10.1038/ncomms6689 · Cited by 61 · see citing works
Synaptic mechanisms underlying cholinergic control of thalamic reticular nucleus neurons
Beierlein, M. (2014) · The Journal of Physiology · doi:10.1113/jphysiol.2014.277376 · Cited by 61 · see citing works
Wester, J. C., & McBain, C. J. (2014) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2014.07.007 · Cited by 52 · see citing works
Hay, Y. A., Lambolez, B., & Tricoire, L. (2015) · Cerebral Cortex · doi:10.1093/cercor/bhv085 · Cited by 51 · see citing works
Demars, M. P., & Morishita, H. (2014) · Molecular Brain · doi:10.1186/s13041-014-0075-9 · Cited by 51 · see citing works
Poorthuis, R. B., & Mansvelder, H. D. (2013) · Biochemical Pharmacology · doi:10.1016/j.bcp.2013.07.003 · Cited by 48 · see citing works
Dasgupta, R., Seibt, F., & Beierlein, M. (2018) · The Journal of Neuroscience · doi:10.1523/jneurosci.0566-18.2018 · Cited by 47 · see citing works
Soma, S., Shimegi, S., Suematsu, N., Tamura, H., & Sato, H. (2013) · PLoS ONE · doi:10.1371/journal.pone.0068430 · Cited by 46 · see citing works
Mechanisms of Plasticity in the Developing and Adult Visual Cortex
Sur, M., Nagakura, I., Chen, N., & 杉原, 弘. (2013) · Progress in brain research · doi:10.1016/b978-0-444-63327-9.00002-3 · Cited by 42 · see citing works
Proenneke, A., Witte, M., Möck, M., & Staiger, J. F. (2019) · Cerebral Cortex · doi:10.1093/cercor/bhz102 · Cited by 45 · see citing works
Enhancing Channelrhodopsins: An Overview
Wietek, J., & Prigge, M. (2016) · Methods in molecular biology · doi:10.1007/978-1-4939-3512-3_10 · Cited by 40 · see citing works
Estakhr, J., Abazari, D., Frisby, K., McIntosh, J. M., & Nashmi, R. (2017) · Current Biology · doi:10.1016/j.cub.2017.05.084 · Cited by 40 · see citing works
Hay, Y. A., Andjelić, S., Badr, S., & Lambolez, B. (2014) · Brain Structure and Function · doi:10.1007/s00429-014-0869-7 · Cited by 39 · see citing works
Distinct Roles of SOM and VIP Interneurons during Cortical Up States
Neske, G. T., & Connors, B. W. (2016) · Frontiers in Neural Circuits · doi:10.3389/fncir.2016.00052 · Cited by 38 · see citing works
Mechanisms Underlying Desynchronization of Cholinergic-Evoked Thalamic Network Activity
Pita‐Almenar, J. D., Yu, D., Lu, H., & Beierlein, M. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.2321-14.2014 · Cited by 36 · see citing works
Gaykema, R. P. A., Nguyen, X.-M. T., Boehret, J. M., Lambeth, P. S., Joy-Gaba, J., Warthen, D. M., & Scott, M. M. (2014) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2014.00060 · Cited by 35 · see citing works
Kimura, R., Safari, M.-S., Mirnajafi‐Zadeh, J., Kimura, R., Ebina, T., Yanagawa, Y., Sohya, K., & Tsumoto, T. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.0863-14.2014 · Cited by 31 · see citing works
R-(+) and S-(−) Isomers of Cotinine Augment Cholinergic Responses In Vitro and In Vivo
Terry, A. V., Callahan, P. M., & Bertrand, D. (2014) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.114.219881 · Cited by 30 · see citing works
Rodríguez-García, G., & Miranda, M. I. (2016) · Journal of Neuroscience · doi:10.1523/jneurosci.2340-15.2016 · Cited by 30 · see citing works
Coronel‐Oliveros, C., Cofré, R., & Orio, P. (2021) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1008737 · Cited by 30 · see citing works
Bell, L. A., Bell, K. A., & McQuiston, A. R. (2015) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2015.00115 · Cited by 29 · see citing works
Campbell, M. G., & Giocomo, L. M. (2018) · Journal of Neurophysiology · doi:10.1152/jn.00686.2017 · Cited by 27 · see citing works
A transcriptomic axis predicts state modulation of cortical interneuronsPreprint
Bugeon, S., Duffield, J. A. M., Dipoppa, M., Ritoux, A., Prankerd, I., Nicoloutsopoulos, D., Orme, D., Shinn, M., Peng, H., Forrest, H., et al. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.10.24.465600 · Cited by 24 · see citing works
Basal ganglia—thalamus and the “crowning enigma”
Garcia-Munoz, M., & Arbuthnott, G. W. (2015) · Frontiers in Neural Circuits · doi:10.3389/fncir.2015.00071 · Cited by 26 · see citing works
Sun, Y.-G., Rupprecht, V., Zhou, L., Dasgupta, R., Seibt, F., & Beierlein, M. (2016) · Journal of Neuroscience · doi:10.1523/jneurosci.0409-16.2016 · Cited by 23 · see citing works
Zhong, P., Cao, Q., & Yan, Z. (2022) · Cerebral Cortex · doi:10.1093/cercor/bhac036 · Cited by 22 · see citing works
Aracri, P., Meneghini, S., Coatti, A., Amadeo, A., & Becchetti, A. (2016) · Neuroscience · doi:10.1016/j.neuroscience.2016.10.045 · Cited by 22 · see citing works
Barrel cortex VIP/ChAT interneurons suppress sensory responses in vivo
Dudai, A., Yayon, N., Lerner, V., Tasaka, G., Deitcher, Y., Gorfine, K., Niederhoffer, N., Mizrahi, A., Soreq, H., & London, M. (2020) · PLoS Biology · doi:10.1371/journal.pbio.3000613 · Cited by 23 · see citing works
Schmitz, T. W., & Záborszky, L. (2021) · Handbook of clinical neurology · doi:10.1016/b978-0-12-819975-6.00008-x · Cited by 22 · see citing works
High-Affinity Nicotinic Receptors Modulate Spontaneous Cortical Up States In Vitro
Sigalas, C., Rigas, P., Tsakanikas, P., & Skaliora, I. (2015) · Journal of Neuroscience · doi:10.1523/jneurosci.5222-14.2015 · Cited by 21 · see citing works
Lee, S., & Kim, J. (2019) · Experimental Neurobiology · doi:10.5607/en.2019.28.3.320 · Cited by 21 · see citing works
Endogenous Acetylcholine and Its Modulation of Cortical Microcircuits to Enhance Cognition
Venkatesan, S., Jeoung, H., Chen, T., Power, S. K., Liu, Y., & Lambe, E. K. (2020) · Current topics in behavioral neurosciences · doi:10.1007/7854_2020_138 · Cited by 21 · see citing works
Komal, P., Estakhr, J., Kamran, M., Renda, A., & Nashmi, R. (2015) · The Journal of Physiology · doi:10.1113/jp270469 · Cited by 21 · see citing works
Inhibitory plasticity in layer 1 – dynamic gatekeeper of neocortical associations
Hartung, J., & Letzkus, J. J. (2020) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2020.06.003 · Cited by 22 · see citing works
Abbondanza, A., Urushadze, A., Alves-Barboza, A. R., & Janíčková, H. (2024) · Pharmacological Research · doi:10.1016/j.phrs.2024.107190 · Cited by 20 · see citing works
Stoichiometry of the Heteromeric Nicotinic Receptors of the Renshaw Cell
d’Incamps, B. L., Zorbaz, T., Dingová, D., Krejci, É., & Ascher, P. (2018) · Journal of Neuroscience · doi:10.1523/jneurosci.0070-18.2018 · Cited by 19 · see citing works
High affinity and low affinity heteromeric nicotinic acetylcholine receptors at central synapses
d’Incamps, B. L., & Ascher, P. (2014) · The Journal of Physiology · doi:10.1113/jphysiol.2014.273128 · Cited by 18 · see citing works
Cell-specific modulation of plasticity and cortical state by cholinergic inputs to the visual cortex
杉原, 弘., Chen, N., & Sur, M. (2016) · Journal of Physiology-Paris · doi:10.1016/j.jphysparis.2016.11.004 · Cited by 18 · see citing works
Attention and Dynamic, Task-Related Receptive Field Plasticity in Adult Auditory Cortex
Fritz, J. B., David, S. V., & Shamma, S. (2012) · Springer handbook of auditory research · doi:10.1007/978-1-4614-2350-8_9 · Cited by 16 · see citing works
- Authors
- Arroyo, S., Bennett, C., Aziz, D., Brown, S. P., & Hestrin, S.
- Affiliations
- University of Arizona (US)
- Stanford Medicine (US)
- Johns Hopkins University (US)
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2012-03-14
- Volume
- 32
- Issue
- 11
- Pages
- 3859-3864
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC3320796
- OpenAlex
- W2002108201
- Cited by
- 138
- References
- 33
- Citations by year
- 2026: 1 · 2025: 4 · 2024: 2 · 2023: 4 · 2022: 7 · 2021: 7 · 2020: 8 · 2019: 8 · 2018: 14 · 2017: 9 · 2016: 12 · 2015: 19 · 2014: 27 · 2013: 10 · 2012: 6
- FWCI
- 7.98
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Eye Institute (R01EY012114)
- 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 › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Keywords
- disynaptic inhibition, nicotinic acetylcholine receptors, cortical interneurons, cholinergic stimulation, basal forebrain, cholinergic axons, cortical circuits
- MeSH terms
- Action Potentials, Animals, Axons, Cerebral Cortex, Female, Interneurons, Male, Mice, Transgenic, Neural Inhibition, Reaction Time, Receptors, Nicotinic, Synapses, Time Factors, Mice, Cholinergic Neurons, alpha7 Nicotinic Acetylcholine Receptor
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.
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