Morphological and Functional Characterization of Non-fast-Spiking GABAergic Interneurons in Layer 4 Microcircuitry of Rat Barrel Cortex
Open accessAbstract
GABAergic interneurons are notorious for their heterogeneity, despite constituting a small fraction of the neuronal population in the neocortex. Classification of interneurons is crucial for understanding their widespread cortical functions as they provide a complex and dynamic network, balancing excitation and inhibition. Here, we investigated different types of non-fast-spiking (nFS) interneurons in Layer 4 (L4) of rat barrel cortex using whole-cell patch-clamp recordings with biocytin-filling. Based on a quantitative analysis on a combination of morphological and electrophysiological parameters, we identified 5 distinct types of L4 nFS interneurons: 1) trans-columnar projecting interneurons, 2) locally projecting non-Martinotti-like interneurons, 3) supra-granular projecting Martinotti-like interneurons, 4) intra-columnar projecting VIP-like interneurons, and 5) locally projecting neurogliaform-like interneurons. Trans-columnar projecting interneurons are one of the most striking interneuron types, which have not been described so far in Layer 4. They feature extensive axonal collateralization not only in their home barrel but also in adjacent barrels. Furthermore, we identified that most of the L4 nFS interneurons express somatostatin, while few are positive for the transcription factor Prox1. The morphological and electrophysiological characterization of different L4 nFS interneuron types presented here provides insights into their synaptic connectivity and functional role in cortical information processing.
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?
Previous studies reported three types of fast-spiking (FS), parvalbumin-positive (PV+) interneurons and five types of non-FS interneurons, all with distinct morphologies.
“Previous studies have reported three types of fast-spiking (FS), parvalbumin-positive (PV+) interneurons11 and five types of non-FS interneurons12, all of which have distinct morphologies.”
From Layer 4 of mouse neocortex differs in cell types and circuit organization between sensory areas (2019) · cites this paper as [12]
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
Silhouettes: A graphical aid to the interpretation and validation of cluster analysis
Rousseeuw, P. J. (1987) · Journal of Computational and Applied Mathematics · doi:10.1016/0377-0427(87)90125-7 · Cited by 21,392 · see citing works
Hierarchical Grouping to Optimize an Objective Function
Ward, J. H. (1963) · Journal of the American Statistical Association · doi:10.1080/01621459.1963.10500845 · Cited by 21,341 · see citing works
Evaluating the use of exploratory factor analysis in psychological research.
Fabrigar, L. R., Wegener, D. T., MacCallum, R. C., & Strahan, E. J. (1999) · Psychological Methods · doi:10.1037/1082-989x.4.3.272 · Cited by 9,587 · see citing works
Shrestha, S., & Offer, S. M. (2016) · Medical Epigenetics · doi:10.1159/000444713 · Cited by 8,949 · see citing works
Cell types in the mouse cortex and hippocampus revealed by single-cell RNA-seq
Zeisel, A., Muñoz-Manchado, A. B., Codeluppi, S., Lönnerberg, P., La Manno, G., Juréus, A., Marques, S., Munguba, H., He, L., Betsholtz, C., et al. (2015) · Science · doi:10.1126/science.aaa1934 · Cited by 3,124 · see citing works
Interneurons of the neocortical inhibitory system
Markram, H., Toledo-Rodriguez, M., Wang, Y., Gupta, A., Silberberg, G., & Wu, C. (2004) · Nature Reviews Neuroscience · doi:10.1038/nrn1519 · Cited by 2,954 · see citing works
The structural organization of layer IV in the somatosensory region (S I) of mouse cerebral cortex
Woolsey, T. A., & Van der Loos, H. (1970) · Brain Research · doi:10.1016/0006-8993(70)90079-x · Cited by 2,254 · see citing works
Cluster analysis of multivariate data : efficiency versus interpretability of classifications
Forgy, E. W. (1965) · Biometrics · Cited by 2,124 · see citing works
Neuronal Diversity and Temporal Dynamics: The Unity of Hippocampal Circuit Operations
Klausberger, T., & Somogyi, P. (2008) · Science · doi:10.1126/science.1149381 · Cited by 2,050 · see citing works
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
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
Petilla terminology: nomenclature of features of GABAergic interneurons of the cerebral cortex
The Petilla Interneuron Nomenclature Group (PING) (2008) · Nature Reviews Neuroscience · doi:10.1038/nrn2402 · Cited by 1,491 · 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
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
Interneuron cell types are fit to function
Kepecs, A., & Fishell, G. (2014) · Nature · doi:10.1038/nature12983 · Cited by 1,110 · see citing works
Organizing principles for a diversity of GABAergic interneurons and synapses in the neocortex
Gupta, A., Wang, Y., & Markram, H. (2000) · Science · doi:10.1126/science.287.5451.273 · Cited by 1,036 · see citing works
A Neuroligin-3 Mutation Implicated in Autism Increases Inhibitory Synaptic Transmission in Mice
Tabuchi, K., Blundell, J., Etherton, M. R., Hammer, R. E., Liu, X., Powell, C. M., & Südhof, T. C. (2007) · Science · doi:10.1126/science.1146221 · Cited by 997 · see citing works
Neuronal subtypes and diversity revealed by single-nucleus RNA sequencing of the human brain
Lake, B. B., Ai, R., Kaeser, G. E., Salathia, N. S., Yung, Y. C., Liu, R., Wildberg, A., Gao, D., Fung, H.-L., Chen, S., et al. (2016) · Science · doi:10.1126/science.aaf1204 · Cited by 957 · see citing works
Principles of connectivity among morphologically defined cell types in adult neocortex
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 · see citing works
Neuronal cell-type classification: challenges, opportunities and the path forward
Zeng, H., & Sanes, J. R. (2017) · Nature Reviews Neuroscience · doi:10.1038/nrn.2017.85 · Cited by 841 · see citing works
New insights into the classification and nomenclature of cortical GABAergic interneurons
DeFelipe, J., López-Cruz, P. L., Benavides-Piccione, R., Bielza, C., Larrañaga, P., Anderson, S., Burkhalter, A., Cauli, B., Fairén, A., Feldmeyer, D., et al. (2013) · Nature Reviews Neuroscience · doi:10.1038/nrn3444 · Cited by 833 · see citing works
Self-citationStuart, G. J., Dodt, H., & Sakmann, B. J. (1993) · Pflügers Archiv - European Journal of Physiology · doi:10.1007/bf00374949 · Cited by 804 · see citing works
A cellular mechanism for cortical associations: an organizing principle for the cerebral cortex
Larkum, M. (2013) · Trends in Neurosciences · doi:10.1016/j.tins.2012.11.006 · Cited by 755 · see citing works
A neural circuit for spatial summation in visual cortex
Adesnik, H., Bruns, W., Taniguchi, H., Huang, Z. J., & Scanziani, M. (2012) · Nature · doi:10.1038/nature11526 · Cited by 702 · see citing works
Thalamocortical responses of mouse somatosensory (barrel) cortexin vitro
Agmon, A., & Connors, B. W. (1991) · Neuroscience · doi:10.1016/0306-4522(91)90333-j · Cited by 673 · see citing works
Liquid junction potentials and small cell effects in patch-clamp analysis
Barry, P. H., & Lynch, J. W. (1991) · The Journal of Membrane Biology · doi:10.1007/bf01870526 · Cited by 668 · see citing works
Barry, P. H. (1994) · Journal of Neuroscience Methods · doi:10.1016/0165-0270(94)90031-0 · Cited by 611 · 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
Electrophysiological, transcriptomic and morphologic profiling of single neurons using Patch-seq
Cadwell, C. R., Palasantza, A., Jiang, X., Berens, P., Deng, Q., Yilmaz, M., Reimer, J., Shen, S., Bethge, M., Tolias, K. F., et al. (2016) · Nature Biotechnology · doi:10.1038/nbt.3445 · Cited by 581 · see citing works
McBain, C. J., & Fisahn, A. (2001) · Nature Reviews Neuroscience · doi:10.1038/35049047 · Cited by 581 · 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
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
Kalanithi, P. S. A., Zheng, W., Kataoka, Y., DiFiglia, M., Grantz, H., Saper, C. B., Schwartz, M. L., Leckman, J. F., & Vaccarino, F. M. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0502624102 · Cited by 543 · see citing works
Alterations in Cortical Network Oscillations and Parvalbumin Neurons in Schizophrenia
Gonzalez-Burgos, G., Cho, R. Y., & Lewis, D. A. (2015) · Biological Psychiatry · doi:10.1016/j.biopsych.2015.03.010 · Cited by 497 · see citing works
Active properties of neocortical pyramidal neuron dendrites
Major, G., Larkum, M. E., & Schiller, J. (2013) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-062111-150343 · Cited by 443 · see citing works
Feldmeyer, D., Egger, V., Lübke, J., & Sakmann, B. (1999) · The Journal of Physiology · doi:10.1111/j.1469-7793.1999.00169.x · Cited by 441 · see citing works
Self-citationUnique functional properties of somatostatin-expressing GABAergic neurons in mouse barrel cortex
Gentet, L. J., Kremer, Y., Taniguchi, H., Huang, Z. J., Staiger, J. F., & Petersen, C. C. H. (2012) · Nature Neuroscience · doi:10.1038/nn.3051 · Cited by 438 · see citing works
Distinct Subtypes of Somatostatin-Containing Neocortical Interneurons Revealed in Transgenic Mice
Ma, Y., Hu, H., Berrebi, A. S., Mathers, P. H., & Agmon, A. (2006) · The Journal of Neuroscience · doi:10.1523/jneurosci.0661-06.2006 · Cited by 432 · see citing works
Transcriptional Architecture of Synaptic Communication Delineates GABAergic Neuron Identity
Paul, A., Crow, M., Raudales, R., He, M., Gillis, J., & Huang, Z. J. (2017) · Cell · doi:10.1016/j.cell.2017.08.032 · Cited by 421 · see citing works
Fuzik, J., Zeisel, A., Máté, Z., Calvigioni, D., Yanagawa, Y., Szabó, G., Linnarsson, S., & Harkany, T. (2016) · Nature Biotechnology · doi:10.1038/nbt.3443 · Cited by 386 · see citing works
How many subtypes of inhibitory cells in the hippocampus?
Parra, P., Gulyás, A., & Miles, R. (1998) · Neuron · doi:10.1016/s0896-6273(00)80479-1 · Cited by 369 · see citing works
Neocortical Somatostatin-Expressing GABAergic Interneurons Disinhibit the Thalamorecipient Layer 4
Xu, H., Jeong, H.-Y., Tremblay, R., & Rudy, B. (2013) · Neuron · doi:10.1016/j.neuron.2012.11.004 · Cited by 366 · see citing works
Identified sources and targets of slow inhibition in the neocortex
Tamás, G., Simon, A. L., & Szabadics, J. (2003) · Science · doi:10.1126/science.1082053 · Cited by 359 · see citing works
Surround Suppression in Primate V1
Jones, H. E., Grieve, K. L., Wang, W., & Sillito, A. M. (2001) · Journal of Neurophysiology · doi:10.1152/jn.2001.86.4.2011 · Cited by 357 · see citing works
Porter, J. T., Johnson, C. K., & Agmon, A. (2001) · Journal of Neuroscience · doi:10.1523/jneurosci.21-08-02699.2001 · Cited by 344 · see citing works
Larkum, M. E., Kaiser, K. M. M., & Sakmann, B. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.25.14600 · Cited by 342 · see citing works
Layer-specific modulation of neocortical dendritic inhibition during active wakefulness
Muñoz, W., Tremblay, R., Levenstein, D., & Rudy, B. (2017) · Science · doi:10.1126/science.aag2599 · Cited by 305 · see citing works
Visualizing unstained neurons in living brain slices by infrared DIC-videomicroscopy
Dodt, H., & Zieglgänsberger, W. (1990) · Brain Research · doi:10.1016/0006-8993(90)90380-t · Cited by 291 · see citing works
Chmielowska, J., Carvell, G. E., & Simons, D. J. (1989) · The Journal of Comparative Neurology · doi:10.1002/cne.902850304 · Cited by 272 · see citing works
Classification of NPY-Expressing Neocortical Interneurons
Karagiannis, A., Gallopin, T., Dávid, C., Battaglia, D., Geoffroy, H., Rossier, J., Hillman, E. M. C., Staiger, J. F., & Cauli, B. (2009) · The Journal of Neuroscience · doi:10.1523/jneurosci.0058-09.2009 · Cited by 256 · see citing works
Petersen, C., & Sakmann, B. (2001) · Journal of Neuroscience · doi:10.1523/jneurosci.21-21-08435.2001 · Cited by 255 · see citing works
Inhibitory interneurons in a cortical column form hot zones of inhibition in layers 2 and 5A
Meyer, H. S., Schwarz, D., Wimmer, V. C., Schmitt, A. C., Kerr, J. N. D., Sakmann, B., & Helmstaedter, M. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1113648108 · Cited by 254 · 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
Sun, Q., Huguenard, J. R., & Prince, D. A. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.4727-04.2006 · Cited by 242 · see citing works
Opening Holes in the Blanket of Inhibition: Localized Lateral Disinhibition by VIP Interneurons
Karnani, M. M., Jackson, J., Ayzenshtat, I., Hamzehei Sichani, A., Manoocheri, K., Kim, S., & Yuste, R. (2016) · The Journal of Neuroscience · doi:10.1523/jneurosci.3646-15.2016 · Cited by 236 · 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
Uematsu, M., Hirai, Y., Karube, F., Ebihara, S., Kato, M., Abe, K., Obata, K., Yoshida, S., Hirabayashi, M., Yanagawa, Y., et al. (2008) · Cerebral Cortex · doi:10.1093/cercor/bhm056 · Cited by 232 · see citing works
Network-Level Control of Frequency Tuning in Auditory Cortex
Kato, H., Asinof, S. K., & Isaacson, J. S. (2017) · Neuron · doi:10.1016/j.neuron.2017.06.019 · Cited by 216 · see citing works
Prönneke, A., Scheuer, B., Wagener, R. J., Möck, M., Witte, M., & Staiger, J. F. (2015) · Cerebral Cortex · doi:10.1093/cercor/bhv202 · Cited by 204 · see citing works
Lübke, J. H. R. (2003) · Cerebral Cortex · doi:10.1093/cercor/13.10.1051 · Cited by 202 · see citing works
Imaging spatiotemporal dynamics of surround inhibition in the barrels somatosensory cortex
Derdikman, D., Hildesheim, R., Ahissar, E., Arieli, A., & Grinvald, A. (2003) · The Journal of Neuroscience · doi:10.1523/jneurosci.23-08-03100.2003 · Cited by 177 · cited 1× · see citing works
“In the somatosensory barrel cortex, suppression of the neuronal activity in surround barrels may be involved in contrast enhancement of principal whisker signaling (Brumberg et al. 1996; Derdikman et al. 2003; Sachdev et al. 2012).”
BackgroundSpatial gradients and inhibitory summation in the rat whisker barrel system
Brumberg, J. C., Pinto, D. J., & Simons, D. J. (1996) · Journal of Neurophysiology · doi:10.1152/jn.1996.76.1.130 · Cited by 176 · see citing works
Porter, J. T., Cauli, B., Staiger, J. F., Lambolez, B., Rossier, J., & Audinat, E. (1998) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.1998.00367.x · Cited by 173 · see citing works
Synaptic interactions of late-spiking neocortical neurons in layer 1
Chu, Z., Galarreta, M., & Hestrin, S. (2003) · The Journal of Neuroscience · doi:10.1523/jneurosci.23-01-00096.2003 · Cited by 172 · see citing works
McGarry, L. M. (2010) · Frontiers in Neural Circuits · doi:10.3389/fncir.2010.00012 · Cited by 166 · see citing works
Activation of cortical somatostatin interneurons prevents the development of neuropathic pain
Cichon, J., Blanck, T. J. J., Gan, W., & Yang, G. (2017) · Nature Neuroscience · doi:10.1038/nn.4595 · Cited by 163 · see citing works
Communication in Neural Circuits: Tools, Opportunities, and Challenges
Lerner, T. N., Ye, L., & Deisseroth, K. (2016) · Cell · doi:10.1016/j.cell.2016.02.027 · Cited by 159 · see citing works
Neurogliaform cells in cortical circuits
Overstreet-Wadiche, L., & McBain, C. J. (2015) · Nature Reviews Neuroscience · doi:10.1038/nrn3969 · Cited by 152 · 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
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
GABAA,slow: causes and consequences
Capogna, M., & Pearce, R. A. (2011) · Trends in Neurosciences · doi:10.1016/j.tins.2010.10.005 · 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
Weighing the Evidence in Peters’ Rule: Does Neuronal Morphology Predict Connectivity?
Rees, C. L., Moradi, K., & Ascoli, G. A. (2016) · Trends in Neurosciences · doi:10.1016/j.tins.2016.11.007 · Cited by 127 · 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
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
Li, L., Ji, X., Liang, F., Li, Y.-T., Xiao, Z., Tao, H. W., & Zhang, L. I. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.1516-14.2014 · Cited by 117 · see citing works
Helmstaedter, M. N., Sakmann, B. J., & Feldmeyer, D. (2008) · Cerebral Cortex · doi:10.1093/cercor/bhn141 · Cited by 108 · see citing works
Self-citationNarayanan, R. T., Egger, R., Johnson, A. S., Mansvelder, H. D., Sakmann, B. J., de Kock, C. P. J., & Oberlaender, M. (2015) · Cerebral Cortex · doi:10.1093/cercor/bhv053 · Cited by 104 · see citing works
Rozov, A., Jerecic, J., Sakmann, B., & Burnashev, N. (2001) · The Journal of Neuroscience · doi:10.1523/jneurosci.21-20-08062.2001 · Cited by 103 · see citing works
Involvement of cortical fast-spiking parvalbumin-positive basket cells in epilepsy
Jiang, X., Lachance, M., & Rossignol, E. (2016) · Progress in brain research · doi:10.1016/bs.pbr.2016.04.012 · Cited by 98 · see citing works
VIP and PACAP potentiate the action of glutamate on BDNF expression in mouse cortical neurones
Pellegri, G., Magistretti, P. J., & Martin, J. (1998) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.1998.00052.x · Cited by 97 · see citing works
Band-Pass Response Properties of Rat SI Neurons
Garabedian, C. E., Jones, S. R., Merzenich, M. M., Dale, A. M., & Moore, C. I. (2003) · Journal of Neurophysiology · doi:10.1152/jn.01158.2002 · Cited by 95 · see citing works
Improved biocytin labeling and neuronal 3D reconstruction
Marx, M., Günter, R. H., Hucko, W., Radnikow, G., & Feldmeyer, D. (2012) · Nature Protocols · doi:10.1038/nprot.2011.449 · Cited by 86 · see citing works
Self-citationZhu, Y., & Zhu, J. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.4805-03.2004 · Cited by 85 · see citing works
An inhibitory pull–push circuit in frontal cortex
García‐Junco‐Clemente, P., Ikrar, T., Tring, E., Xu, X., Ringach, D. L., & Trachtenberg, J. T. (2017) · Nature Neuroscience · doi:10.1038/nn.4483 · Cited by 84 · see citing works
Walker, F., Möck, M., Feyerabend, M., Guy, J., Wagener, R. J., Schubert, D., Staiger, J. F., & Witte, M. (2016) · Nature Communications · doi:10.1038/ncomms13664 · Cited by 82 · see citing works
Neurogliaform cells dynamically regulate somatosensory integration via synapse-specific modulation
Chittajallu, R., Pelkey, K. A., & McBain, C. J. (2013) · Nature Neuroscience · doi:10.1038/nn.3284 · Cited by 73 · see citing works
Helmstaedter, M. N., Sakmann, B. J., & Feldmeyer, D. (2008) · Cerebral Cortex · doi:10.1093/cercor/bhn130 · Cited by 73 · see citing works
Self-citationRubin, A. N., & Kessaris, N. (2013) · PLoS ONE · doi:10.1371/journal.pone.0077339 · Cited by 69 · see citing works
Koelbl, C., Helmstaedter, M., Lübke, J., & Feldmeyer, D. (2015) · Cerebral Cortex · doi:10.1093/cercor/bht263 · Cited by 68 · see citing works
Self-citationSynaptic 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
Surround suppression and sparse coding in visual and barrel cortices
Sachdev, R. N. S., Krause, M. R., & Mazer, J. A. (2012) · Frontiers in Neural Circuits · doi:10.3389/fncir.2012.00043 · Cited by 65 · see citing works
Region-Specific Spike-Frequency Acceleration in Layer 5 Pyramidal Neurons Mediated by Kv1 Subunits
Miller, M. N., Okaty, B. W., & Nelson, S. B. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.2940-08.2008 · Cited by 60 · see citing works
Helmstaedter, M. N., Sakmann, B. J., & Feldmeyer, D. (2008) · Cerebral Cortex · doi:10.1093/cercor/bhn138 · Cited by 60 · see citing works
Self-citationFunctional Independence of Layer IV Barrels
Laaris, N., & Keller, A. (2002) · Journal of Neurophysiology · doi:10.1152/jn.00512.2001 · Cited by 59 · see citing works
Beyond the frontiers of neuronal types
Battaglia, D. A., Karagiannis, A., Gallopin, T., Gutch, H. W., & Cauli, B. (2013) · Frontiers in Neural Circuits · doi:10.3389/fncir.2013.00013 · Cited by 56 · see citing works
Kolomiets, B. P., Marzo, A., Caboche, J., Vanhoutte, P., & Otani, S. (2009) · Cerebral Cortex · doi:10.1093/cercor/bhp047 · Cited by 56 · see citing works
Cerebral cortical neuron diversity and development at single-cell resolution
Johnson, M. B., & Walsh, C. A. (2016) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2016.11.001 · Cited by 51 · see citing works
Zhou, X., Rickmann, M., Hafner, G., & Staiger, J. F. (2017) · Cerebral Cortex · doi:10.1093/cercor/bhx220 · Cited by 51 · see citing works
Qi, G., van Aerde, K. I., Abel, T. G., & Feldmeyer, D. (2016) · Cerebral Cortex · doi:10.1093/cercor/bhw243 · Cited by 47 · see citing works
Self-citationRepresentation of moving wavefronts of whisker deflection in rat somatosensory cortex.
Drew, P., & Feldman, D. (2007) · Journal of Neurophysiology · doi:10.1152/jn.00056.2007 · Cited by 39 · see citing works
Name-calling in the hippocampus (and beyond): coming to terms with neuron types and properties
Hamilton, D. J., Wheeler, D. W., White, C. M., Rees, C. L., Komendantov, A. O., Bergamino, M., & Ascoli, G. A. (2016) · Brain Informatics · doi:10.1007/s40708-016-0053-3 · Cited by 35 · see citing works
Classification of neocortical interneurons using affinity propagation
Santana, R., McGarry, L. M., Bielza, C., Larrañaga, P., & Yuste, R. (2013) · Frontiers in Neural Circuits · doi:10.3389/fncir.2013.00185 · Cited by 30 · see citing works
Somatotopic organization of rat thalamocortical slices
Land, P. W., & Kandler, K. (2002) · Journal of Neuroscience Methods · doi:10.1016/s0165-0270(02)00150-4 · Cited by 26 · see citing works
Surround Suppression in the Early Visual System: Figure 1.
Smith, M. A. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.0236-06.2006 · Cited by 23 · see citing works
Encoding and Decoding Cortical Representations of Tactile Features in the Vibrissa System
Boloori, A., Jenks, R. A., Desbordes, G., & Stanley, G. B. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.0807-10.2010 · Cited by 22 · see citing works
Neuronal network analysis : concepts and experimental approaches
Fellin, T., & Halassa, M. M. (2012) · Cited by 21 · see citing works
New Aspects of Axonal Structure and Function
Feldmeyer, D., & Lübke, J. H. R. (2010) · Springer eBooks · doi:10.1007/978-1-4419-1676-1 · Cited by 19 · see citing works
Self-citationBartlett, T. E., Lu, J., & Wang, Y. T. (2011) · Molecular Brain · doi:10.1186/1756-6606-4-41 · Cited by 17 · see citing works
Helmstaedter, M. N., & Feldmeyer, D. (2010) · Springer eBooks · doi:10.1007/978-1-4419-1676-1_8 · Cited by 11 · see citing works
Self-citation
Flagged first, then by citations
Research works printed but not linked: 1
- Ma Y, Hu H, Berrebi AS, Mathers PH, Agmon A 2006b. Distinct subtypes of somatostatin-containing neocortical interneurons revealed in transgenic mice. J Neurosci. 26: 5069– 5082. 16687498 PMC2020857
Cited by
Sorted by citations
Layer 4 of mouse neocortex differs in cell types and circuit organization between sensory areas
Scala, F., Kobak, D., Shan, S., Bernaerts, Y., Laturnus, S., Cadwell, C. R., Hartmanis, L., Froudarakis, E., Castro, J. R., Tan, Z. H., et al. (2019) · Nature Communications · doi:10.1038/s41467-019-12058-z · Cited by 193 · see citing works
Zhou, X., Mansori, I., Fischer, T., Witte, M., & Staiger, J. F. (2020) · Journal of Comparative Neurology · doi:10.1002/cne.24756 · Cited by 18 · see citing works
- Authors
- Emmenegger, V., Qi, G., Wang, H., & Feldmeyer, D.
- Affiliations
- Forschungszentrum Jülich (DE)
- Corresponding author
- Feldmeyer, Dirk
- Venue
- Cerebral Cortex
- Publisher
- Oxford University Press (OUP)
- Published
- 2018-01-10
- Volume
- 28
- Issue
- 4
- Pages
- 1439-1457
- ISSN
- 1047-3211 (ISSN-L)
- 1460-2199
- PMC
- PMC6093438
- OpenAlex
- W2751409073
- Cited by
- 26
- References
- 110
- Citations by year
- 2026: 1 · 2025: 3 · 2024: 2 · 2023: 2 · 2022: 4 · 2021: 4 · 2020: 5 · 2019: 3 · 2018: 2
- FWCI
- 1.34
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Cerebral Cortex (publishedVersion, cc-by-nc)
- Europe PMC (PubMed Central) (publishedVersion, cc-by-nc)
- PubMed Central (publishedVersion, cc-by-nc)
- PubMed (publishedVersion)
- RWTH Publications (RWTH Aachen) (submittedVersion, other-oa)
- Repository for Publications and Research Data (ETH Zurich) (submittedVersion, cc-by-nc)
- ETH Zürich Research Collection
- Funders
- Helmholtz Society, the DFG Research Group
- DFG International Research Training Group (1328)
- Natural Science Fund for Colleges
- Universities in the Jiangsu (14KJB140007)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Keywords
- GABAergic interneurons, barrel cortex, layer 4, interneuron classification, somatostatin, Prox1, synaptic connectivity, cortical microcircuitry
- MeSH terms
- Animals, Animals, Newborn, Axons, Cerebral Cortex, Dendrites, Female, Lysine, Male, Membrane Potentials, Models, Neurological, Nerve Net, Vasoactive Intestinal Peptide, Patch-Clamp Techniques, Imaging, Three-Dimensional, Principal Component Analysis, Rats, GABAergic Neurons, In Vitro Techniques
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