Synaptic interactions of late-spiking neocortical neurons in layer 1
Open accessAbstract
Layer 1 of the neocortex is an important zone in which synaptic integration of inputs originating from a variety of cerebral regions is thought to take place. Layer 1 does not contain pyramidal cells, and several histochemical studies have suggested that most layer 1 neurons are GABAergic. However, although layer 1 neurons could be an important source of inhibition in this layer, the synaptic action of these neurons and the identity of their postsynaptic targets are unknown. We studied the physiological properties and synaptic interactions of a class of cells within layer 1 called late-spiking (LS) cells. The dendrites and axons of layer 1 LS cells were confined primarily to layer 1. Using paired recording, we showed that LS cells formed GABAergic connections with other LS cells as well as with non-LS cells in layer 1 and with pyramidal cells in layer 2/3. We also found that layer 2/3 pyramidal neurons provide excitatory inputs to LS cells. It has been suggested previously that GABAergic neurons belonging to the same class in the cortex are electrically coupled. In agreement with that hypothesis, we found that LS cells were interconnected by electrical coupling (83%), whereas electrical coupling between LS cells and non-LS cells was infrequent (2%). Thus, we provide evidence showing that a group of GABAergic neurons within layer 1 are specifically interconnected by electrical coupling and can provide significant inhibitory inputs to neurons in layer 1 and to distal dendrites of pyramidal cells.
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
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.
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?
Layer 1 cells are almost all inhibitory and interconnect strongly via electrical connections and chemical synapses.
“These L1 cells are almost all inhibitory and interconnect strongly with each other, via electrical connections and chemical synapses (Chu et al., 2003).”
From Canonical Microcircuits for Predictive Coding (2012) · cites this paper as Chu et al., 2003
The Abstract says histochemical studies suggest most layer 1 neurons are GABAergic, but it does not establish that almost all are inhibitory. The ‘Electrical coupling and inhibitory connections among LS cells’ section reports electrical coupling in 83% and chemical connections in 26.2% of tested late-spiking cell pairs. Those findings support interconnection within that cell class, not a strong interconnection among layer 1 cells generally. (LLM, conf=0.88)
Experimental — accuracy not yet measuredLayer 1 cells provide strong monosynaptic inhibition to L2/3 pyramidal cells whose apical dendrites project into L1.
“Simultaneous whole cell patch clamp recordings show that they provide strong monosynaptic inhibition to L2/3 pyramidal cells, whose apical dendrites project into L1 (Chu et al., 2003; Wozny and Williams, 2011).”
From Canonical Microcircuits for Predictive Coding (2012) · cites this paper as Chu et al., 2003
NGFCs of layer 2/3 (but not layer 1) of rat somatosensory cortex are highly interconnected via electrical synapses and also make widespread electrical synapses with PVBCs, regular spiking nonpyramidal cells, AACs as well as many other unidentified interneuron cell types.
“One interesting deviation from this canonical rule are NGFCs of layer 2/3 (but not layer 1) (206) of rat somatosensory cortex. Although these cells were highly interconnected via electrical synapses, they also made widespread electrical synapses with PVBCs, regular spiking nonpyramidal cells, AACs as well as many other unidentified interneuron cell types (1017).”
From Hippocampal GABAergic Inhibitory Interneurons (2017) · cites this paper as [206]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Distributed hierarchical processing in the primate cerebral cortex
Felleman, D. J., & Van Essen, D. C. (1991) · Cerebral Cortex · doi:10.1093/cercor/1.1.1 · Cited by 7,783 · see citing works
Preface: Cerebral Cortex Has Come of Age
Goldman, P. S., & RAKIC, P. T. (1991) · Cerebral Cortex · doi:10.1093/cercor/1.1.1-a · Cited by 3,412 · 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
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 · see citing works
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 · see citing works
Self-citationProximally 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 · see citing works
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 580 · see citing works
Kawaguchi, Y. (1995) · The Journal of Neuroscience · doi:10.1523/jneurosci.15-04-02638.1995 · Cited by 533 · see citing works
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 · see citing works
Electrical synapses between Gaba-Releasing interneurons
Galarreta, M., & Hestrin, S. (2001) · Nature Reviews Neuroscience · doi:10.1038/35077566 · Cited by 434 · see citing works
Self-citationSubmillisecond AMPA receptor-mediated signaling at a principal neuron-interneuron synapse
Geiger, J. R. P., Lübke, J., Roth, A., Frotscher, M., & Jonas, P. (1997) · Neuron · doi:10.1016/s0896-6273(00)80339-6 · Cited by 407 · see citing works
Spike Transmission and Synchrony Detection in Networks of GABAergic Interneurons
Galarreta, M., & Hestrin, S. (2001) · Science · doi:10.1126/science.1061395 · Cited by 389 · see citing works
Self-citationIn vivo dendritic calcium dynamics in deep-layer cortical pyramidal neurons
Helmchen, F., Svoboda, K., Denk, W. T., & Tank, D. W. (1999) · Nature Neuroscience · doi:10.1038/14788 · Cited by 380 · see citing works
Kim, H., & Connors, B. W. (1993) · Journal of Neuroscience · doi:10.1523/jneurosci.13-12-05301.1993 · Cited by 302 · see citing works
Functional Properties of Channels Formed by the Neuronal Gap Junction Protein Connexin36
Srinivas, M., Rozental, R., Kojima, T., Dermietzel, R., Mehler, M., Condorelli, D. F., Kessler, J. A., & Spray, D. C. (1999) · The Journal of Neuroscience · doi:10.1523/jneurosci.19-22-09848.1999 · Cited by 290 · see citing works
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 286 · see citing works
Quantitative distribution of GABA-immunoreactive neurons in the visual cortex (area 17) of the cat
Gabbott, P. L. A., & Somogyi, P. (1986) · Experimental Brain Research · doi:10.1007/bf00239522 · Cited by 269 · see citing works
Beaulieu, C., Kisvarday, Z., Somogyi, P., Cynader, M., & Cowey, A. (1992) · Cerebral Cortex · doi:10.1093/cercor/2.4.295 · Cited by 269 · see citing works
Llinás, R. R., Leznik, E., & Urbano, F. J. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.012604899 · Cited by 262 · see citing works
Synaptic physiology of horizontal afferents to layer I in slices of rat SI neocortex
Cauller, L., & Connors, B. W. (1994) · Journal of Neuroscience · doi:10.1523/jneurosci.14-02-00751.1994 · Cited by 252 · see citing works
Larkum, M. E., & Zhu, J. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-16-06991.2002 · Cited by 249 · 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
Self-citationZhu, J. (2000) · The Journal of Physiology · doi:10.1111/j.1469-7793.2000.00571.x · Cited by 170 · see citing works
Cauller, L., & Kulics, A. T. (1991) · Experimental Brain Research · doi:10.1007/bf00230973 · Cited by 147 · see citing works
Szabadics, J., Lörincz, A., & Tamás, G. (2001) · Journal of Neuroscience · doi:10.1523/jneurosci.21-15-05824.2001 · Cited by 134 · see citing works
y Cajal, S. R. (1988) · Cited by 119 · see citing works
Recruitment of GABAergic Inhibition and Synchronization of Inhibitory Interneurons in Rat Neocortex
Benardo, L. S. (1997) · Journal of Neurophysiology · doi:10.1152/jn.1997.77.6.3134 · Cited by 96 · 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
Corticocortical and thalamocortical projections to layer I of the frontal neocortex in rats
Mitchell, B. D., & Cauller, L. J. (2001) · Brain Research · doi:10.1016/s0006-8993(01)03084-0 · Cited by 71 · see citing works
The Role of Layer I in Cortical Function
Vogt, B. A. (1991) · Cerebral cortex · doi:10.1007/978-1-4615-6622-9_2 · Cited by 70 · see citing works
Layer I neurons of rat neocortex. I. Action potential and repetitive firing properties
Zhou, F. M., & Hablitz, J. J. (1996) · Journal of Neurophysiology · doi:10.1152/jn.1996.76.2.651 · Cited by 68 · 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
Rapid Kinetics and Inward Rectification of Miniature EPSCs in Layer I Neurons of Rat Neocortex
Zhou, F.-M., & Hablitz, J. J. (1997) · Journal of Neurophysiology · doi:10.1152/jn.1997.77.5.2416 · Cited by 28 · see citing works
Oakley, J. C., Schwindt, P. C., & Crill, W. E. (2001) · Journal of Neurophysiology · doi:10.1152/jn.2001.86.1.503 · Cited by 26 · see citing works
The neurons in layer 1 of cat visual cortex
Anderson, J. C., Martin, K. A. C., & Diniz, C. W. P. (1992) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.1992.0038 · Cited by 13 · see citing works
The voltage‐dependent conductances of rat neocortical layer I neurons
Budde, T., & White, J. A. (1998) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.1998.00242.x · Cited by 12 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Canonical Microcircuits for Predictive Coding
Bastos, A. M., Usrey, W. M., Adams, R. A., Mangun, G. R., Fries, P., & Friston, K. J. (2012) · Neuron · doi:10.1016/j.neuron.2012.10.038 · Cited by 2,421 · see citing works
“These L1 cells are almost all inhibitory and interconnect strongly with each other, via electrical connections and chemical synapses (Chu et al., 2003).”
InfluentialGABAergic 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
Adult mouse cortical cell taxonomy revealed by single cell transcriptomics
Tasic, B., Menon, V., Nguyen, T. N., Kim, T. K., Jarsky, T., Yao, Z., Levi, B., Gray, L. T., Sorensen, S. A., Dolbeare, T., et al. (2016) · Nature Neuroscience · doi:10.1038/nn.4216 · Cited by 1,714 · see citing works
Large-scale model of mammalian thalamocortical systems
Izhikevich, E. M., & Edelman, G. M. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0712231105 · Cited by 1,021 · see citing works
Hippocampal GABAergic Inhibitory Interneurons
Pelkey, K. A., Chittajallu, R., Craig, M. T., Tricoire, L., Wester, J. C., & McBain, C. J. (2017) · Physiological Reviews · doi:10.1152/physrev.00007.2017 · Cited by 889 · 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
ELECTRICAL SYNAPSES IN THE MAMMALIAN BRAIN
Connors, B. W., & Long, M. A. (2004) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.26.041002.131128 · Cited by 784 · see citing works
Lee, S., Hjerling-Leffler, J., Zagha, E., Fishell, G., & Rudy, B. (2010) · The Journal of Neuroscience · doi:10.1523/jneurosci.1869-10.2010 · Cited by 600 · see citing works
Two dynamically distinct inhibitory networks in layer 4 of the neocortex
Beierlein, M., Gibson, J. R., & Connors, B. W. (2003) · Journal of Neurophysiology · doi:10.1152/jn.00283.2003 · Cited by 591 · see citing works
Miyoshi, G., Hjerling-Leffler, J., Karayannis, T., Sousa, V. H., Butt, S. J. B., Battiste, J., Johnson, J. E., Machold, R. P., & Fishell, G. (2010) · The Journal of Neuroscience · doi:10.1523/jneurosci.4515-09.2010 · Cited by 559 · see citing works
Selective Activation of the Deep Layers of the Human Primary Visual Cortex by Top-Down Feedback
Kok, P., Bains, L. J., van Mourik, T., Norris, D. G., & de Lange, F. P. (2016) · Current Biology · doi:10.1016/j.cub.2015.12.038 · Cited by 397 · see citing works
Supralinear increase of recurrent inhibition during sparse activity in the somatosensory cortex
Kapfer, C., Glickfeld, L. L., Atallah, B. V., & Scanziani, M. (2007) · Nature Neuroscience · doi:10.1038/nn1909 · Cited by 427 · see citing works
Disinhibition, a Circuit Mechanism for Associative Learning and Memory
Letzkus, J. J., Wolff, S. B. E., & Lüthi, A. (2015) · Neuron · doi:10.1016/j.neuron.2015.09.024 · Cited by 401 · see citing works
Neural elements for predictive coding
Shipp, S. (2016) · Frontiers in Psychology · doi:10.3389/fpsyg.2016.01792 · Cited by 340 · see citing works
The organization of two new cortical interneuronal circuits
Jiang, X., Wang, G., Lee, A. J., Stornetta, R. L., & Zhu, J. J. (2013) · Nature Neuroscience · doi:10.1038/nn.3305 · Cited by 338 · see citing works
Repetition suppression and its contextual determinants in predictive coding
Auksztulewicz, R., & Friston, K. (2016) · Cortex · doi:10.1016/j.cortex.2015.11.024 · Cited by 307 · see citing works
Ibrahim, L. A., Mesik, L., Ji, X., Fang, Q., Li, H.-F., Li, Y.-T., Zingg, B., Zhang, L. I., & Tao, H. W. (2016) · Neuron · doi:10.1016/j.neuron.2016.01.027 · Cited by 287 · see citing works
The Cellular Basis of GABA <sub>B</sub> -Mediated Interhemispheric Inhibition
Palmer, L. M., Schulz, J. M., Murphy, S. C., Ledergerber, D., Murayama, M., & Larkum, M. E. (2012) · Science · doi:10.1126/science.1217276 · Cited by 284 · see citing works
Pérez‐Garci, E., Gassmann, M., Bettler, B., & Larkum, M. E. (2006) · Neuron · doi:10.1016/j.neuron.2006.04.019 · Cited by 262 · see citing works
Electrical synapses define networks of neocortical GABAergic neurons
Hestrin, S., & Galarreta, M. (2005) · Trends in Neurosciences · doi:10.1016/j.tins.2005.04.001 · Cited by 258 · see citing works
Self-citationClassification 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
Oscillations and Filtering Networks Support Flexible Routing of Information
Akam, T., & Kullmann, D. M. (2010) · Neuron · doi:10.1016/j.neuron.2010.06.019 · Cited by 245 · see citing works
Kubota, Y., Shigematsu, N., Karube, F., Sekigawa, A., Kato, S., Yamaguchi, N., Hirai, Y., Morishima, M., & Kawaguchi, Y. (2011) · Cerebral Cortex · doi:10.1093/cercor/bhq252 · Cited by 235 · see citing works
Prediction and memory: A predictive coding account
Barron, H. C., Auksztulewicz, R., & Friston, K. (2020) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2020.101821 · Cited by 220 · see citing works
Learning-Related Plasticity in Dendrite-Targeting Layer 1 Interneurons
Abs, E., Poorthuis, R. B., Apelblat, D., Muhammad, K., Pardi, M. B., Enke, L., Kushinsky, D., Pu, D.-L., Eizinger, M. F., Conzelmann, K., et al. (2018) · Neuron · doi:10.1016/j.neuron.2018.09.001 · Cited by 212 · see citing works
Thalamic 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
Synchronization of Electrically Coupled Pairs of Inhibitory Interneurons in Neocortex
Mancilla, J. G., Lewis, T. J., Pinto, D. J., Rinzel, J., & Connors, B. W. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.2715-06.2007 · Cited by 210 · see citing works
Electrical synapses coordinate activity in the suprachiasmatic nucleus
Long, M. A., Jutras, M. J., Connors, B. W., & Burwell, R. D. (2004) · Nature Neuroscience · doi:10.1038/nn1361 · Cited by 194 · see citing works
Anatomy and physiology of the thick-tufted layer 5 pyramidal neuron
Ramaswamy, S., & Markram, H. (2015) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2015.00233 · Cited by 186 · see citing works
Four Unique Interneuron Populations Reside in Neocortical Layer 1
Schuman, B., Machold, R. P., Hashikawa, Y., Fuzik, J., Fishell, G. J., & Rudy, B. (2019) · The Journal of Neuroscience · doi:10.1523/jneurosci.1613-18.2018 · Cited by 184 · see citing works
“Previous studies of L1 INs agree that an important component of this population is neurogliaform cells (NGFCs), INs that mediate long-lasting GABAA and GABAB inhibition of PCs and have a late-spiking (LS) firing pattern when depolarized to near threshold membrane potentials (Chu et al., 2003; Tamás et al., 2003; Overs…”
BackgroundInfluentialFunctional properties and projections of neurons in the medial amygdala
Keshavarzi, S., Sullivan, R. K. P., Ianno, D. J., & Sah, P. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.1176-14.2014 · Cited by 176 · see citing works
Szabadics, J., Tamás, G., & Soltesz, I. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0707204104 · Cited by 170 · 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
Fan, 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
Activity-Dependent Long-Term Depression of Electrical Synapses
Haas, J. S., Zavala, B., & Landisman, C. E. (2011) · Science · doi:10.1126/science.1207502 · Cited by 152 · see citing works
Neocortical Layer 1: an elegant solution to top-down and bottom-up integration
Schuman, B., Dellal, S., Prönneke, A., Machold, R., & Rudy, B. (2021) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-100520-012117 · Cited by 148 · see citing works
Vucurovic, 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
Krimer, L. S., Zaitsev, A. V., Czanner, G., Kröner, S., González‐Burgos, G., Povysheva, N. V., Iyengar, S., Barrionuevo, G., & Lewis, D. A. (2005) · Journal of Neurophysiology · doi:10.1152/jn.00156.2005 · Cited by 135 · see citing works
Mediodorsal and Ventromedial Thalamus Engage Distinct L1 Circuits in the Prefrontal Cortex
Anastasiades, P. G., Collins, D. P., & Carter, A. G. (2020) · Neuron · doi:10.1016/j.neuron.2020.10.031 · Cited by 135 · see citing works
Prior expectations evoke stimulus-specific activity in the deep layers of the primary visual cortex
Aitken, F., Menelaou, G., Warrington, O., Koolschijn, R. S., Corbin, N., Callaghan, M. F., & Kok, P. (2020) · PLoS Biology · doi:10.1371/journal.pbio.3001023 · Cited by 134 · see citing works
Miyoshi, G., Young, A., Petros, T., Karayannis, T., McKenzie Chang, M., Lavado, A., Iwano, T., Nakajima, M., Taniguchi, H., Huang, Z. J., et al. (2015) · The Journal of Neuroscience · doi:10.1523/jneurosci.1164-15.2015 · Cited by 135 · see citing works
C. elegans AWA Olfactory Neurons Fire Calcium-Mediated All-or-None Action Potentials
Liu, Q., Kidd, P. B., Dobosiewicz, M., & Bargmann, C. I. (2018) · Cell · doi:10.1016/j.cell.2018.08.018 · Cited by 129 · see citing works
Lhx6 directly regulates Arx and CXCR7 to determine cortical interneuron fate and laminar position
Vogt, D., Hunt, R. F., Mandal, S., Sandberg, M., Silberberg, S. N., Nagasawa, T., Yang, Z., Baraban, S. C., & Rubenstein, J. L. R. (2014) · Neuron · doi:10.1016/j.neuron.2014.02.030 · Cited by 129 · see citing works
Wozny, C., & Williams, S. R. (2011) · Cerebral Cortex · doi:10.1093/cercor/bhq257 · Cited by 129 · see citing works
Dendritic Branch Typing and Spine Expression Patterns in Cortical Nonpyramidal Cells
Kawaguchi, Y., Karube, F., & Kubota, Y. (2005) · Cerebral Cortex · doi:10.1093/cercor/bhj015 · Cited by 125 · see citing works
Many specialists for suppressing cortical excitation
Burkhalter, A. (2008) · Frontiers in Neuroscience · doi:10.3389/neuro.01.026.2008 · Cited by 122 · see citing works
Regulation of cortical activity and arousal by the matrix cells of the ventromedial thalamic nucleus
Honjoh, S., Sasai, S., Schiereck, S. S., Nagai, H., Tononi, G., & Cirelli, C. (2018) · Nature Communications · doi:10.1038/s41467-018-04497-x · Cited by 118 · see citing works
Output of neurogliaform cells to various neuron types in the human and rat cerebral cortex
Oláh, S. (2007) · Frontiers in Neural Circuits · doi:10.3389/neuro.04.004.2007 · Cited by 118 · see citing works
Electrical Coupling among Irregular-Spiking GABAergic Interneurons Expressing Cannabinoid Receptors
Galarreta, M., Erdélyi, F., Szabó, G., & Hestrin, S. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.3027-04.2004 · Cited by 120 · see citing works
Self-citationGonchar, Y., & Burkhalter, A. (2003) · The Journal of Neuroscience · doi:10.1523/jneurosci.23-34-10904.2003 · Cited by 114 · see citing works
Traumatic Brain Injury and Neuronal Functionality Changes in Sensory Cortex
Carron, S. F., Alwis, D. S., & Rajan, R. (2016) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2016.00047 · Cited by 112 · see citing works
Gi/o-Protein Coupled Receptors in the Aging Brain
de Oliveira, P. G., Ramos, M. L., Amaro, A. J. M., Dias, R. A., & Vieira, S. I. (2019) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2019.00089 · Cited by 106 · see citing works
Lee, A. J., Wang, G., Jiang, X., Johnson, S. M., Hoang, E. T., Lanté, F., Stornetta, R. L., Beenhakker, M. P., Shen, Y., & Julius Zhu, J. (2015) · Cerebral Cortex · doi:10.1093/cercor/bhu020 · Cited by 94 · see citing works
Suzuki, N., & Bekkers, J. M. (2010) · Cerebral Cortex · doi:10.1093/cercor/bhq046 · Cited by 92 · see citing works
Zsiros, V., & Maccaferri, G. (2005) · The Journal of Neuroscience · doi:10.1523/jneurosci.2810-05.2005 · Cited by 88 · see citing works
Chartrand, T., Dalley, R., Close, J., Goriounova, N. A., Lee, B. R., Mann, R., Miller, J. A., Molnar, G., Mukora, A., Alfiler, L., et al. (2023) · Science · doi:10.1126/science.adf0805 · Cited by 88 · 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
Larsen, D. D. (2008) · Frontiers in Neural Circuits · doi:10.3389/neuro.04.005.2007 · Cited by 86 · see citing works
Involvement of gap junctions in the development of the neocortex
Sutor, B., & Hagerty, T. (2005) · Biochimica et Biophysica Acta (BBA) - Biomembranes · doi:10.1016/j.bbamem.2005.09.005 · Cited by 85 · see citing works
Zhu, Y., & Zhu, J. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.4805-03.2004 · Cited by 85 · see citing works
Production and organization of neocortical interneurons
Sultan, K. T., Brown, K. N., & Shi, S.-H. (2013) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2013.00221 · Cited by 83 · see citing works
Abrupt Maturation of a Spike-Synchronizing Mechanism in Neocortex
Long, M. A., Cruikshank, S. J., Jutras, M. J., & Connors, B. W. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.0375-05.2005 · Cited by 83 · see citing works
Inhibitory Regulation of Dendritic Activity in vivo
Palmer, L. M., Murayama, M., & Larkum, M. E. (2012) · Frontiers in Neural Circuits · doi:10.3389/fncir.2012.00026 · Cited by 82 · see citing works
Xu, H., Mao, L., Ye, S., Paisansathan, C., Vetri, F., & Pelligrino, D. A. (2007) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00530.2007 · Cited by 82 · 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-citationLi, W., Roberts, A., & Soffe, S. R. (2009) · The Journal of Physiology · doi:10.1113/jphysiol.2008.166942 · Cited by 80 · see citing works
Burkhalter, A., Gonchar, Y., Mellor, R. L., & Nerbonne, J. M. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.2599-06.2006 · Cited by 79 · see citing works
Functional diversity of supragranular GABAergic neurons in the barrel cortex
Gentet, L. J. (2012) · Frontiers in Neural Circuits · doi:10.3389/fncir.2012.00052 · Cited by 75 · 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
Cell-type identity: a key to unlocking the function of neocortical circuits
Brown, S. P., & Hestrin, S. (2009) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2009.07.011 · Cited by 70 · see citing works
Self-citationLegon, W., Punzell, S., Dowlati, E. P., Adams, S. E., Stiles, A. B., & Moran, R. (2015) · Cerebral Cortex · doi:10.1093/cercor/bhv200 · Cited by 67 · see citing works
Electrophysiological Differences Between Neurogliaform Cells From Monkey and Rat Prefrontal Cortex
Povysheva, N. V., Zaitsev, A. V., Kröner, S., Krimer, O. A., Rotaru, D. C., González‐Burgos, G., Lewis, D. A., & Krimer, L. S. (2006) · Journal of Neurophysiology · doi:10.1152/jn.00794.2006 · Cited by 67 · see citing works
Ohira, K., Funatsu, N., Homma, K. J., Sahara, Y., Hayashi, M., Kaneko, T., & Nakamura, S. (2007) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2007.05282.x · Cited by 68 · see citing works
Synaptic and cellular organization of layer 1 of the developing rat somatosensory cortex
Muralidhar, S., Wang, Y., & Markram, H. (2014) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2013.00052 · Cited by 67 · see citing works
Extensive overlap of mu-opioid and nicotinic sensitivity in cortical interneurons
Ferezou, I., Hill, E. L., Cauli, B., Gibelin, N., Kaneko, T., Rossier, J., & Lambolez, B. (2007) · Cerebral Cortex · doi:10.1093/cercor/bhl104 · Cited by 65 · see citing works
Poorthuis, R. B., Enke, L., & Letzkus, J. J. (2014) · The Journal of Physiology · doi:10.1113/jphysiol.2014.273862 · Cited by 64 · see citing works
Role of Interneuron Diversity in the Cortical Microcircuit for Attention
Buia, C., & Tiesinga, P. H. E. (2008) · Journal of Neurophysiology · doi:10.1152/jn.01004.2007 · Cited by 64 · see citing works
Chu, Z., & Moenter, S. M. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.3171-06.2006 · Cited by 62 · see citing works
Self-citationGap junction plasticity as a mechanism to regulate network-wide oscillations
Pernelle, G., Nicola, W., & Clopath, C. (2018) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1006025 · Cited by 58 · see citing works
Guzman, P. D., D’Antuono, M., & Avoli, M. (2004) · Neuroscience · doi:10.1016/j.neuroscience.2003.11.013 · Cited by 60 · see citing works
Development of Layer 1 Neurons in the Mouse Neocortex
Ma, J., Yao, X.-H., Fu, Y., & Yu, Y. (2013) · Cerebral Cortex · doi:10.1093/cercor/bht114 · Cited by 57 · see citing works
The Potential Role of Gap Junctional Plasticity in the Regulation of State
Coulon, P., & Landisman, C. E. (2017) · Neuron · doi:10.1016/j.neuron.2017.02.041 · Cited by 56 · see citing works
Properties of external plexiform layer interneurons in mouse olfactory bulb slices
Hamilton, K. A., Heinbockel, T., Ennis, M. J., Szabó, G., Erdélyi, F., & Hayar, A. M. (2005) · Neuroscience · doi:10.1016/j.neuroscience.2005.03.008 · Cited by 57 · see citing works
Ma, Y., Hioki, H., Konno, M., Pan, S., Nakamura, H., Nakamura, K., Furuta, T., Li, J., & Kaneko, T. (2011) · Cerebral Cortex · doi:10.1093/cercor/bhr051 · Cited by 55 · see citing works
Wu, J., & Hablitz, J. J. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.1405-05.2005 · Cited by 55 · see citing works
Activity-dependent tuning of intrinsic excitability in mouse and human neurogliaform cells
Chittajallu, R., Auville, K., Mahadevan, V., Lai, M., Hunt, S., Calvigioni, D., Pelkey, K. A., Zaghloul, K. A., & McBain, C. J. (2020) · eLife · doi:10.7554/elife.57571 · Cited by 51 · see citing works
Changes in Calcium-Binding Protein Expression in Human Cortical Contusion Tissue
Buriticá, E., Villamil, L., Guzmán, F., Escobar, M. I., Garcia‐Cairasco, N., & Pimienta, H. J. (2009) · Journal of Neurotrauma · doi:10.1089/neu.2009.0894 · Cited by 50 · see citing works
Generation of diverse cortical inhibitory interneurons
Sultan, K. T., & Shi, S. (2017) · Wiley Interdisciplinary Reviews Developmental Biology · doi:10.1002/wdev.306 · Cited by 48 · see citing works
Structural Organization of the Gap Junction Network in the Cerebral Cortex
Fukuda, T. (2007) · The Neuroscientist · doi:10.1177/1073858406296760 · Cited by 49 · see citing works
Bistable Network Behavior of Layer I Interneurons in Auditory Cortex
Merriam, E. B., Netoff, T. I., & Banks, M. I. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.0512-05.2005 · Cited by 46 · see citing works
GABAergic Inhibitory Interneurons in the Posterior Piriform Cortex of the GAD67-GFP Mouse
Young, A., & Sun, Q. (2009) · Cerebral Cortex · doi:10.1093/cercor/bhp072 · Cited by 43 · see citing works
Integration of Synaptic Responses to Neighboring Whiskers in Rat Barrel Cortex In Vivo
Higley, M. J., & Contreras, D. (2004) · Journal of Neurophysiology · doi:10.1152/jn.00917.2004 · Cited by 43 · see citing works
Hu, H., & Agmon, A. (2015) · Journal of Neurophysiology · doi:10.1152/jn.00304.2015 · Cited by 44 · see citing works
Helbig, I., Sammler, E. M., Eliava, M., Bolshakov, A. P., Rozov, A. V., Bruzzone, R., Monyer, H., & Hormuzdi, S. G. (2010) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2010.05.008 · Cited by 40 · see citing works
Kirkcaldie, M. (2011) · Elsevier eBooks · doi:10.1016/b978-0-12-369497-3.10004-4 · Cited by 40 · see citing works
Ectopic action potential generation in cortical interneurons during synchronized GABA responses
Keros, S., & Hablitz, J. J. (2005) · Neuroscience · doi:10.1016/j.neuroscience.2004.12.010 · Cited by 40 · see citing works
Connexon connexions in the thalamocortical system
Cruikshank, S. J., Landisman, C. E., Mancilla, J. G., & Connors, B. W. (2005) · Progress in brain research · doi:10.1016/s0079-6123(05)49004-4 · Cited by 36 · see citing works
Krauss, M. I., Weiss, T., Langnaese, K., Richter, K., Kowski, A. B., Veh, R. W., & Laube, G. (2007) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2007.04770.x · Cited by 37 · see citing works
Electrical coupling regulates layer 1 interneuron microcircuit formation in the neocortex
Yao, X.-H., Wang, M., He, X.-N., He, F., Zhang, S.-Q., Lu, W., Qiu, Z., & Yu, Y. (2016) · Nature Communications · doi:10.1038/ncomms12229 · Cited by 36 · see citing works
Castejon, C., Barros-Zulaica, N., & Núñez, Á. (2016) · PLoS ONE · doi:10.1371/journal.pone.0148169 · Cited by 35 · see citing works
- Authors
- Chu, Z., Galarreta, M., & Hestrin, S.
- Affiliations
- Stanford Medicine (US)
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2003-01-01
- Volume
- 23
- Issue
- 1
- Pages
- 96-102
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC6742162
- OpenAlex
- W2171308715
- Semantic Scholar
- 02a53e21726fd337b87f5d80b53b76713176c7e6
- Cited by
- 172
- References
- 38
- Citations by year
- 2026: 3 · 2025: 3 · 2024: 4 · 2023: 2 · 2022: 5 · 2021: 1 · 2020: 8 · 2019: 4 · 2018: 11 · 2017: 6 · 2016: 10 · 2015: 8 · 2014: 10 · 2013: 6 · 2012: 16
- FWCI
- 3.81
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Journal of Neuroscience (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health
- National Eye Institute (R01EY012114, EY12114, EY09120, R01EY009120)
- 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
- GABAergic interneurons, electrical coupling, synaptic integration, pyramidal neurons, layer 2/3, inhibitory interneurons, postsynaptic targets, paired recordings
- MeSH terms
- Animals, Cells, Cultured, Electric Conductivity, gamma-Aminobutyric Acid, Kinetics, Neural Inhibition, Neural Pathways, Synaptic Transmission, Neurons, Rats, Sprague-Dawley, Pyramidal Cells, Patch-Clamp Techniques, Neocortex, Excitatory Postsynaptic Potentials, 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