New insights into the classification and nomenclature of cortical GABAergic interneurons
Open accessAbstract
A systematic classification and accepted nomenclature of neuron types is much needed but is currently lacking. This article describes a possible taxonomical solution for classifying GABAergic interneurons of the cerebral cortex based on a novel, web-based interactive system that allows experts to classify neurons with pre-determined criteria. Using Bayesian analysis and clustering algorithms on the resulting data, we investigated the suitability of several anatomical terms and neuron names for cortical GABAergic interneurons. Moreover, we show that supervised classification models could automatically categorize interneurons in agreement with experts' assignments. These results demonstrate a practical and objective approach to the naming, characterization and classification of neurons based on community consensus.
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Chandelier interneurons are the most morphologically recognizable interneurons due to candlestick-like synaptic terminal arrays targeting the axon initial segment of pyramidal cells.
“Chandelier INs, also known as axo-axonic neurons, are the most recognizable INs in terms of morphology (DeFelipe et al., 2013) due to the unique candlestick-like synaptic terminal arrays they form to specifically target the axon initial segment of pyramidal cells.”
From GABAergic Interneurons in the Neocortex: From Cellular Properties to Circuits (2016) · cites this paper as DeFelipe et al., 2013
The Historical overview (page unavailable) says chandelier cells are readily distinguished by clear morphological attributes, but it does not rank them as the most recognizable interneurons. The Anatomical section (page unavailable) identifies chandelier cells as axo-axonic cells targeting the axon initial segment of pyramidal cells; the cited passages do not describe candlestick-like terminal arrays. (LLM, conf=0.82)
Experimental — accuracy not yet measuredA systematic attempt to classify neocortical interneurons by morphology alone showed too many ambiguities for experts to agree on most subtype identities.
“an attempt to produce a systematic classification of neocortical INs based on morphological features alone by a large number of investigators showed that there are too many ambiguities for “experts” to agree on the identity of most IN subtypes when strictly relying on morphological data”
From GABAergic Interneurons in the Neocortex: From Cellular Properties to Circuits (2016) · cites this paper as DeFelipe et al., 2013
The definition of a cell type in the brain remains controversial.
“the definition of a cell type in the brain remains controversial20,21”
From Systems biology and gene networks in neurodevelopmental and neurodegenerative disorders (2015) · cites this paper as [21]
The field has not readily converged on a consensus number or definition of neuronal cell types.
“the field has not readily converged on a consensus number, or even definition, of neuronal cell types”
From Integrated Morphoelectric and Transcriptomic Classification of Cortical GABAergic Cells (2020) · cites this paper as DeFelipe et al., 2013
In V1 L4 of adult mice, seven inhibitory types of neurons were identified using whole-cell recordings with morphological recovery.
“Using whole-cell recordings with morphological recovery, we identified one major excitatory and seven inhibitory types of neurons in L4 of adult mouse visual cortex (V1).”
From Layer 4 of mouse neocortex differs in cell types and circuit organization between sensory areas (2019) · cites this paper as [41]
Rigorous, quantitative and scalable analysis of interneuron morphology remains difficult.
“A century after Ramon y Cajal described ‘short axon cells’, rigorous, quantitative and scalable analysis of interneuron morphology remains difficult11.”
From The diversity of GABAergic neurons and neural communication elements (2019) · cites this paper as [11]
The issue of interneuron diversity remains contentious.
“Consequently, the issue of interneuron diversity remains contentious11.”
From The diversity of GABAergic neurons and neural communication elements (2019) · cites this paper as [11]
Differences in morphology among neurons of one class can look continuous and hard to parse, yet they might correspond to more precise, discrete wiring patterns between particular pre- and postsynaptic partners.
“Similarly, morphological variations between neurons of the same class may seem continuous and intractable11 but may belie the more specific and discrete connectivity patterns between certain presynaptic and postsynaptic elements56,67.”
From The diversity of GABAergic neurons and neural communication elements (2019) · cites this paper as [11]
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Cites
Seel, N. M. (2012) · Springer eBooks · doi:10.1007/978-1-4419-1428-6_5195 · Cited by 19,525 · see citing works
Statistical pattern recognition: a review
Jain, A. K., Duin, P., & Mao, J. (2000) · IEEE Transactions on Pattern Analysis and Machine Intelligence · doi:10.1109/34.824819 · Cited by 6,795 · see citing works
Abe, S. (2001) · Springer eBooks · doi:10.1007/978-1-4471-0285-4 · Cited by 3,740 · see citing works
Probabilistic Reasoning in Intelligent Systems
(1988) · Elsevier eBooks · doi:10.1016/c2009-0-27609-4 · Cited by 3,371 · 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
Raykar, V. C., Yu, S., Zhao, L. H., Valadez, G. H., Florin, C., Bogoni, L., & Moy, L. P. (2010) · Journal of Machine Learning Research · doi:10.5555/1756006.1859894 · Cited by 1,195 · see citing works
(2006) · doi:10.1093/acprof:oso/9780195100273.001.0001 · Cited by 1,186 · see citing works
Microstructure of the neocortex: comparative aspects
DeFelipe, J., Alonso-Nanclares, L., & Arellano, J. I. (2002) · Journal of Neurocytology · doi:10.1023/a:1024130211265 · Cited by 686 · see citing works
Self-citationNeuroMorpho.Org: A Central Resource for Neuronal Morphologies
Ascoli, G. A., Donohue, D. E., & Halavi, M. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.2055-07.2007 · Cited by 664 · see citing works
Self-citationPerceptual Neuroscience: The Cerebral Cortex
Mountcastle, V. B. (1998) · Cited by 481 · see citing works
Cajal–Retzius cells and the development of the neocortex
Marín‐Padilla, M. (1998) · Trends in Neurosciences · doi:10.1016/s0166-2236(97)01164-8 · Cited by 444 · 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-citationHof, P. R., Glezer, I. I., Condé, F., Flagg, R. A., Rubin, M. B., Nimchinsky, E. A., & Weisenhorn, D. M. V. (1999) · Journal of Chemical Neuroanatomy · doi:10.1016/s0891-0618(98)00065-9 · Cited by 411 · see citing works
Self-citationThe Human Brain and Spinal Cord
Heimer, L. (1983) · Springer eBooks · doi:10.1007/978-1-4684-0150-9 · Cited by 370 · see citing works
Long-range-projecting GABAergic neurons modulate inhibition in hippocampus and entorhinal cortex
Melzer, S., Michael, M., Caputi, A., Eliava, M., Fuchs, E. C., Whittington, M. A., & Monyer, H. (2012) · Science · doi:10.1126/science.1217139 · Cited by 333 · see citing works
Self-citationA Blueprint for the Spatiotemporal Origins of Mouse Hippocampal Interneuron Diversity
Tricoire, L., Pelkey, K. A., Erkkila, B. E., Jeffries, B. W., Yuan, X., & McBain, C. J. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.0323-11.2011 · Cited by 292 · see citing works
Self-citationClarke, E., & O'Malley, C. D. (1968) · University of California Press eBooks · Cited by 270 · 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
Self-citationInhibitory 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
Self-citationKubota, 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
Self-citationStaiger, J. F. (2004) · Cerebral Cortex · doi:10.1093/cercor/bhh029 · Cited by 226 · see citing works
Self-citationMobilizing the base of neuroscience data: the case of neuronal morphologies
Ascoli, G. A. (2006) · Nature reviews. Neuroscience · doi:10.1038/nrn1885 · Cited by 221 · see citing works
Self-citationRakic, P. (1975) · PubMed · Cited by 220 · see citing works
Hevner, R. F., Neogi, T., Englund, C., Daza, R. A. M., & Fink, A. (2003) · Developmental Brain Research · doi:10.1016/s0165-3806(02)00641-7 · Cited by 197 · see citing works
Chapter 17 Cortical interneurons: from Cajal to 2001
DeFelipe, J. (2002) · Progress in brain research · doi:10.1016/s0079-6123(02)36019-9 · Cited by 186 · see citing works
Self-citationPorter, 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
Self-citationHandbuch der Lehre von den Geweben des Menschen und der Thiere
Stricker, S. (1871) · Cited by 168 · see citing works
Meyer, G. (1999) · Cerebral Cortex · doi:10.1093/cercor/9.8.765 · Cited by 155 · see citing works
RAKIC, P. T. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0807271105 · Cited by 154 · see citing works
Long‐distance corticocortical GABAergic neurons in the adult monkey white and gray matter
Tomioka, R., & Rockland, K. S. (2007) · The Journal of Comparative Neurology · doi:10.1002/cne.21504 · Cited by 144 · see citing works
Self-citationCortical columns as devices for maximizing neuronal diversity
Malach, R. (1994) · Trends in Neurosciences · doi:10.1016/0166-2236(94)90113-9 · Cited by 101 · see citing works
Fate of Cajal-Retzius neurons in the postnatal mouse neocortex
Chowdhury, T. G. (2010) · Frontiers in Neuroanatomy · doi:10.3389/neuro.05.010.2010 · Cited by 86 · see citing works
Rockland, K. S. (2010) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2010.00022 · Cited by 82 · see citing works
Self-citationNUEVA CONCEPTA DE LA HISTOLOGIA DE LOS CENTROS NERVOSOS
CAJAL, D. S. R. Y. (1893) · Annals of Surgery · doi:10.1097/00000658-189307000-00018 · Cited by 73 · see citing works
Ontologies for neuroscience: What are they and what are they good for?
Larson, S. (2009) · Frontiers in Neuroscience · doi:10.3389/neuro.01.007.2009 · Cited by 62 · see citing works
Neocortical neuron types in Xenarthra and Afrotheria: implications for brain evolution in mammals
Sherwood, C. C., Stimpson, C. D., Butti, C., Bonar, C. J., Newton, A. L., Allman, J. M., & Hof, P. R. (2008) · Brain Structure and Function · doi:10.1007/s00429-008-0198-9 · Cited by 45 · see citing works
Self-citationAn ontological approach to describing neurons and their relationships
Hamilton, D. J., Shepherd, G. M., Martone, M. E., & Ascoli, G. A. (2012) · Frontiers in Neuroinformatics · doi:10.3389/fninf.2012.00015 · Cited by 42 · see citing works
Self-citationCerebral cortex. Volume 1. Cellular components of the cerebral cortex
(1986) · Comparative Biochemistry and Physiology Part A Physiology · doi:10.1016/0300-9629(86)90744-9 · Cited by 36 · see citing works
Origins of neocortical interneurons in mice
Welagen, J., & Anderson, S. A. (2010) · Developmental Neurobiology · doi:10.1002/dneu.20857 · Cited by 34 · see citing works
Self-citationModels and Simulation of 3D Neuronal Dendritic Trees Using Bayesian Networks
López-Cruz, P. L., Bielza, C., Larrañaga, P., Benavides‐Piccione, R., & DeFelipe, J. (2011) · Neuroinformatics · doi:10.1007/s12021-011-9103-4 · Cited by 23 · see citing works
Self-citation
Flagged first, then by citations
Research works printed but not linked: 3
- [8]8. Golgi C. Sulla struttura della sostanza grigia del cervello (Comunicazione preventiva). Gazz Med Ital Lombardia. 1873; 33:244-246. (in Italian).
- [9]9. Cajal SR. Nuevo concepto de la histología de los centros nerviosos. Revista de Ciencias Médicas de Barcelona. 1892; 18:361-376. English translation available in DeFelipe, J. & Jones, E. G. Cajal on the Cerebral Cortex (Oxford Univ. Press, 1988).
- [11]11. DeFelipe J. Cortical interneurons: from Cajal to 2001. Prog Brain Res. 2002; 136:215-238. [PubMed: 12143384]
Cited by
Sorted by citations
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
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
Self-citationAdult 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
Reconstruction and Simulation of Neocortical Microcircuitry
Markram, H., Muller, E., Ramaswamy, S., Reimann, M. W., Abdellah, M., Sanchez, C. A., Ailamaki, A., Alonso-Nanclares, L., Antille, N., Arsever, S., et al. (2015) · Cell · doi:10.1016/j.cell.2015.09.029 · Cited by 1,705 · see citing works
Self-citationPfeffer, C. K., Xue, M., He, M., Huang, Z. J., & Scanziani, M. (2013) · Nature Neuroscience · doi:10.1038/nn.3446 · Cited by 1,353 · see citing works
Self-citationThe neocortical circuit: themes and variations
Harris, K. D., & Shepherd, G. M. G. (2015) · Nature Neuroscience · doi:10.1038/nn.3917 · Cited by 1,215 · see citing works
Self-citationHu, H., Gan, J., & Jonas, P. (2014) · Science · doi:10.1126/science.1255263 · Cited by 1,197 · see citing works
Duman, R. S., Sanacora, G., & Krystal, J. H. (2019) · Neuron · doi:10.1016/j.neuron.2019.03.013 · Cited by 1,026 · 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
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
Self-citationMolecular logic of neocortical projection neuron specification, development and diversity
Greig, L. C., Woodworth, M. B., Galazo, M. J., Padmanabhan, H., & Macklis, J. D. (2013) · Nature Reviews Neuroscience · doi:10.1038/nrn3586 · Cited by 863 · see citing works
Epigenomic Signatures of Neuronal Diversity in the Mammalian Brain
Mo, A., Mukamel, E. A., Davis, F. P., Luo, C., Henry, G. L., Picard, S., Urich, M. A., Nery, J. R., Sejnowski, T. J., Lister, R., et al. (2015) · Neuron · doi:10.1016/j.neuron.2015.05.018 · Cited by 739 · see citing works
Development and Functional Diversification of Cortical Interneurons
Lim, L., Mi, D., Llorca, A., & Marín, O. (2018) · Neuron · doi:10.1016/j.neuron.2018.10.009 · Cited by 714 · see citing works
“For example, Nkx6-2+ progenitor cells produce several types of SST+ neurons along with some PV+ basket cells and chandelier cells, and a mixed progeny of interneurons from the SST+ and PV+ classes has also been described for Etv1+ progenitor cells (He et al., 2016).”
InfluentialMechanisms of epileptogenesis: a convergence on neural circuit dysfunction
Goldberg, E. M., & Coulter, D. A. (2013) · Nature Reviews Neuroscience · doi:10.1038/nrn3482 · Cited by 542 · see citing works
Integrated Morphoelectric and Transcriptomic Classification of Cortical GABAergic Cells
Gouwens, N. W., Sorensen, S. A., Baftizadeh, F., Budzillo, A., Lee, B. R., Jarsky, T., Alfiler, L., Baker, K., Barkan, E., Berry, K., et al. (2020) · Cell · doi:10.1016/j.cell.2020.09.057 · Cited by 538 · see citing works
“example, in the Sst subclass, the Sst Calb2 Pdlim5 type had a L1-dominant (Martinotti-type) axon (DeFelipe et al., 2013), while Sst Tac1 Htr1d had a L2/3-dominant axon, Sst Hpse Cbln4 had a L4-dominant axon, and Sst Rxfp1 Prdm8 had a L5/L6-dominant axon.”
Architectonic Mapping of the Human Brain beyond Brodmann
Amunts, K., & Zilles, K. (2015) · Neuron · doi:10.1016/j.neuron.2015.12.001 · Cited by 533 · see citing works
Gao, R., & Penzes, P. (2015) · Current Molecular Medicine · doi:10.2174/1566524015666150303003028 · Cited by 516 · see citing works
“For a more comprehensive review on interneuron classification and function, we would like to direct the reader to pertinent articles [27, 34].”
BackgroundAlterations 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
Self-citationThe Central Amygdala as an Integrative Hub for Anxiety and Alcohol Use Disorders
Gilpin, N. W., Herman, M. A., & Roberto, M. (2015) · Biological Psychiatry · doi:10.1016/j.biopsych.2014.09.008 · Cited by 457 · see citing works
Classification of electrophysiological and morphological neuron types in the mouse visual cortex
Gouwens, N. W., Sorensen, S. A., Berg, J., Lee, C., Jarsky, T., Ting, J., Sunkin, S. M., Feng, D., Anastassiou, C. A., Barkan, E., et al. (2019) · Nature Neuroscience · doi:10.1038/s41593-019-0417-0 · Cited by 456 · see citing works
Systems biology and gene networks in neurodevelopmental and neurodegenerative disorders
Parikshak, N. N., Gandal, M. J., & Geschwind, D. H. (2015) · Nature Reviews Genetics · doi:10.1038/nrg3934 · Cited by 430 · 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
General Cortical and Special Prefrontal Connections: Principles from Structure to Function
Barbas, H. (2015) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-071714-033936 · Cited by 395 · see citing works
Cortical GABAergic Dysfunction in Stress and Depression: New Insights for Therapeutic Interventions
Fogaça, M. V., & Duman, R. S. (2019) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2019.00087 · Cited by 396 · see citing works
Buzsáki, G. (2019) · doi:10.1093/oso/9780190905385.001.0001 · Cited by 358 · see citing works
Targeting neurons and photons for optogenetics
Packer, A. M., Roska, B., & Häusser, M. (2013) · Nature Neuroscience · doi:10.1038/nn.3427 · Cited by 345 · see citing works
GABA interneurons are the cellular trigger for ketamine's rapid antidepressant actions
Gerhard, D. M., Pothula, S., Liu, R.-J., Wu, M., Li, X.-Y., Girgenti, M. J., Taylor, S. R., Duman, C. H., Delpire, E., Picciotto, M., et al. (2020) · Journal of Clinical Investigation · doi:10.1172/jci130808 · Cited by 345 · see citing works
Strategies and Tools for Combinatorial Targeting of GABAergic Neurons in Mouse Cerebral Cortex
He, M., Tucciarone, J., Lee, S., Nigro, M. J., Kim, Y., Levine, J. M., Kelly, S. M., Krugikov, I., Wu, P., Chen, Y., et al. (2016) · Neuron · doi:10.1016/j.neuron.2016.08.021 · Cited by 339 · see citing works
Self-citationHashemi, E., Ariza, J., Rogers, H., Noctor, S. C., & Martínez-Cerdeño, V. (2016) · Cerebral Cortex · doi:10.1093/cercor/bhw021 · Cited by 322 · see citing works
Transcriptomic and morphophysiological evidence for a specialized human cortical GABAergic cell type
Boldog, E., Bakken, T. E., Hodge, R. D., Novotny, M., Aevermann, B. D., Baka, J., Bordé, S., Close, J. L., Diez-Fuertes, F., Ding, S.-L., et al. (2018) · Nature Neuroscience · doi:10.1038/s41593-018-0205-2 · Cited by 291 · see citing works
Self-citationGenetic and activity-dependent mechanisms underlying interneuron diversity
Wamsley, B., & Fishell, G. (2017) · Nature Reviews Neuroscience · doi:10.1038/nrn.2017.30 · Cited by 290 · see citing works
Self-citationNeural Subtype Specification from Human Pluripotent Stem Cells
Tao, Y., & Zhang, S.-C. (2016) · Cell Stem Cell · doi:10.1016/j.stem.2016.10.015 · Cited by 287 · see citing works
Alterations in cortical interneurons and cognitive function in schizophrenia
Dienel, S. J., & Lewis, D. A. (2018) · Neurobiology of Disease · doi:10.1016/j.nbd.2018.06.020 · Cited by 267 · see citing works
Self-citationCellular anatomy of the mouse primary motor cortex
Muñoz-Castañeda, R., Zingg, B., Matho, K. S., Chen, X., Wang, Q., Foster, N. N., Li, A., Narasimhan, A., Hirokawa, K. E., Huo, B., et al. (2021) · Nature · doi:10.1038/s41586-021-03970-w · Cited by 262 · see citing works
Self-citationTai, C., Abe, Y., Westenbroek, R. E., Scheuer, T., & Catterall, W. A. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1411131111 · Cited by 266 · see citing works
Ecker, J. R., Geschwind, D. H., Kriegstein, A. R., Ngai, J., Osten, P., Polioudakis, D., Regev, A., Šestan, N., Wickersham, I. R., & Zeng, H. (2017) · Neuron · doi:10.1016/j.neuron.2017.10.007 · Cited by 254 · see citing works
Mapping brain circuitry with a light microscope
Osten, P., & Margrie, T. W. (2013) · Nature Methods · doi:10.1038/nmeth.2477 · Cited by 244 · see citing works
Neurodevelopment, GABA System Dysfunction, and Schizophrenia
Schmidt, M. J., & Mirnics, K. (2014) · Neuropsychopharmacology · doi:10.1038/npp.2014.95 · Cited by 239 · see citing works
Thalamic Inhibition: Diverse Sources, Diverse Scales
Halassa, M. M., & Acsády, L. (2016) · Trends in Neurosciences · doi:10.1016/j.tins.2016.08.001 · Cited by 239 · see citing works
BigNeuron: Large-Scale 3D Neuron Reconstruction from Optical Microscopy Images
Peng, H., Hawrylycz, M., Roskams, J., Hill, S., Spruston, N., Meijering, E. H. W., & Ascoli, G. A. (2015) · Neuron · doi:10.1016/j.neuron.2015.06.036 · Cited by 232 · see citing works
Self-citationTasks for inhibitory interneurons in intact brain circuits
Roux, L., & Buzsáki, G. (2015) · Neuropharmacology · doi:10.1016/j.neuropharm.2014.09.011 · Cited by 218 · see citing works
Inhibitory control of the excitatory/inhibitory balance in psychiatric disorders
Selten, M. M., van Bokhoven, H., & Kasri, N. N. (2018) · F1000Research · doi:10.12688/f1000research.12155.1 · Cited by 208 · see citing works
Inhibitory and Excitatory Spike-Timing-Dependent Plasticity in the Auditory Cortex
D’amour, J. A., & Froemke, R. C. (2015) · Neuron · doi:10.1016/j.neuron.2015.03.014 · Cited by 201 · see citing works
Optogenetic dissection of medial prefrontal cortex circuitry
Riga, D., Matos, M. R., Glas, A., Smit, A. B., Spijker, S., & Van den Oever, M. C. (2014) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2014.00230 · Cited by 208 · 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
Self-citationGABAergic Inhibitory Interneuron Deficits in Alzheimer’s Disease: Implications for Treatment
Xu, Y., Zhao, M., Han, Y., & Zhang, H. (2020) · Frontiers in Neuroscience · doi:10.3389/fnins.2020.00660 · Cited by 203 · see citing works
The diversity of GABAergic neurons and neural communication elements
Huang, Z. J., & Paul, A. (2019) · Nature Reviews Neuroscience · doi:10.1038/s41583-019-0195-4 · Cited by 201 · see citing works
Distinct Roles of Parvalbumin- and Somatostatin-Expressing Interneurons in Working Memory
Kim, D., Jeong, H., Lee, J., Ghim, J.-W., Her, E. S., Lee, S.-H., & Jung, M. W. (2016) · Neuron · doi:10.1016/j.neuron.2016.09.023 · Cited by 201 · see citing works
Xing, B., Li, Y.-C., & Gao, W.-J. (2016) · Brain Research · doi:10.1016/j.brainres.2016.01.005 · Cited by 196 · see citing works
Baker, A. L., Kalmbach, B. E., Morishima, M., Kim, J., Juavinett, A., Li, N., & Dembrow, N. C. (2018) · Journal of Neuroscience · doi:10.1523/jneurosci.0150-18.2018 · Cited by 187 · see citing works
Interneuron Types as Attractors and Controllers
Fishell, G., & Kepecs, Á. (2019) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-070918-050421 · Cited by 197 · see citing works
Self-citationThe Astrocyte: Powerhouse and Recycling Center
Weber, B., & Barros, L. F. (2015) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a020396 · Cited by 195 · see citing works
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
A Topological Representation of Branching Neuronal Morphologies
Kanari, L., Dłotko, P., Scolamiero, M., Levi, R., Shillcock, J. C., Hess, K. P., & Markram, H. (2017) · Neuroinformatics · doi:10.1007/s12021-017-9341-1 · Cited by 179 · see citing works
Self-citationPham, T. H., & Gardier, A. M. (2019) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2019.02.017 · Cited by 186 · see citing works
Integration of GABAergic interneurons into cortical cell assemblies: lessons from embryos and adults
Bartolini, G., Ciceri, G., & Marín, O. (2013) · Neuron · doi:10.1016/j.neuron.2013.08.014 · Cited by 185 · see citing works
The Diversity of Cortical Inhibitory Synapses
Kubota, Y., Karube, F., Nomura, M., & Kawaguchi, Y. (2016) · Frontiers in Neural Circuits · doi:10.3389/fncir.2016.00027 · Cited by 180 · see citing works
Self-citationSomatostatin, neuronal vulnerability and behavioral emotionality
Lin, L., & Sibille, E. L. (2015) · Molecular Psychiatry · doi:10.1038/mp.2014.184 · Cited by 178 · see citing works
Untangling GABAergic wiring in the cortical microcircuit
Kubota, Y. (2014) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2013.10.003 · Cited by 172 · see citing works
Self-citationActivation 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
Portraits of communication in neuronal networks
Hahn, G., Ponce-Alvarez, A., Deco, G., Aertsen, A., & Kumar, A. (2019) · Nature reviews. Neuroscience · doi:10.1038/s41583-018-0094-0 · Cited by 171 · see citing works
Excitotoxicity in ALS: Overstimulation, or overreaction?
King, A. E., Woodhouse, A., Kirkcaldie, M., & Vickers, J. C. (2015) · Experimental Neurology · doi:10.1016/j.expneurol.2015.09.019 · Cited by 170 · see citing works
Neuronal circuits in barrel cortex for whisker sensory perception
Staiger, J. F., & Petersen, C. C. H. (2021) · Physiological Reviews · doi:10.1152/physrev.00019.2019 · Cited by 165 · see citing works
Self-citationFavero, M., Sotuyo, N. P., Lopez, E., Kearney, J. A., & Goldberg, E. M. (2018) · The Journal of Neuroscience · doi:10.1523/jneurosci.0193-18.2018 · Cited by 163 · see citing works
Bardy, C., van den Hurk, M., Kakaradov, B., Erwin, J. A., Jaeger, B. N., Hernandez, R. V., Eames, T., Paucar, A. A., Gorris, M. A. J., Marchand, C., et al. (2016) · Molecular Psychiatry · doi:10.1038/mp.2016.158 · Cited by 160 · see citing works
Hippocampome.org: a knowledge base of neuron types in the rodent hippocampus
Wheeler, D. W., White, C. M., Rees, C. L., Komendantov, A. O., Hamilton, D. J., & Ascoli, G. A. (2015) · eLife · doi:10.7554/elife.09960 · Cited by 153 · see citing works
Self-citationNeurological Syndromes Associated with Anti-GAD Antibodies
Dade, M., Berzero, G., Izquierdo, C., Giry, M., Benazra, M., Delattre, J., Psimaras, D., & Alentorn, A. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21103701 · Cited by 158 · see citing works
Inhibition stabilization is a widespread property of cortical networks
Sanzeni, A., Akitake, B., Goldbach, H. C., Leedy, C. E., Brunel, N., & Histed, M. H. (2020) · eLife · doi:10.7554/elife.54875 · Cited by 157 · see citing works
Single-cell transcriptomic evidence for dense intracortical neuropeptide networks
Smith, S. J., Sümbül, U., Graybuck, L. T., Collman, F., Seshamani, S., Gala, R., Gliko, O., Elabbady, L., Miller, J. A., Bakken, T. E., et al. (2019) · eLife · doi:10.7554/elife.47889 · Cited by 156 · see citing works
Self-citationAdult Olfactory Bulb NeurogenesisPreprint
Lledo, P., & Valley, M. T. (2016) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a018945 · Cited by 156 · see citing works
Bayesian networks in neuroscience: a survey
Bielza, C., & Larrañaga, P. (2014) · Frontiers in Computational Neuroscience · doi:10.3389/fncom.2014.00131 · Cited by 152 · see citing works
Self-citationPre-frontal parvalbumin interneurons in schizophrenia: a meta-analysis of post-mortem studies
Kaar, S. J., Angelescu, I., Marques, T. R., & Howes, O. D. (2019) · Journal of Neural Transmission · doi:10.1007/s00702-019-02080-2 · Cited by 146 · 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
Multiple Transmitter Receptors in Regions and Layers of the Human Cerebral Cortex
Zilles, K., & Palomero‐Gallagher, N. (2017) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2017.00078 · Cited by 148 · see citing works
Molecular and Cellular Mechanisms of Rapid-Acting Antidepressants Ketamine and Scopolamine
Wohleb, E. S., Gerhard, D. M., Thomas, A., & Duman, R. S. (2016) · Current Neuropharmacology · doi:10.2174/1570159x14666160309114549 · Cited by 151 · see citing works
Big data and the industrialization of neuroscience: A safe roadmap for understanding the brain?
Frégnac, Y. (2017) · Science · doi:10.1126/science.aan8866 · Cited by 147 · see citing works
Integrative Mechanisms of Oriented Neuronal Migration in the Developing Brain
Evsyukova, I. Y., Plestant, C., & Anton, E. S. (2013) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev-cellbio-101512-122400 · Cited by 143 · see citing works
Schmidt, M., Bakker, R., Shen, K., Bezgin, G., Diesmann, M., & van Albada, S. J. (2018) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1006359 · Cited by 145 · see citing works
Northoff, G., & Sibille, E. L. (2014) · Molecular Psychiatry · doi:10.1038/mp.2014.68 · Cited by 145 · see citing works
Hippocampal GABAergic interneurons and memory
Tzilivaki, A., Tukker, J. J., Maier, N., Poirazi, P., Sammons, R. P., & Schmitz, D. (2023) · Neuron · doi:10.1016/j.neuron.2023.06.016 · Cited by 145 · see citing works
Hamada, M., Galea, J. M., Lazzaro, V. D., Mazzone, P., Ziemann, U., & Rothwell, J. C. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.1960-14.2014 · Cited by 137 · see citing works
Tyan, L., Chamberland, S., Magnin, E., Camiré, O., Francavilla, R., David, L. S., Deisseroth, K., & Topolnik, L. (2014) · The Journal of Neuroscience · doi:10.1523/jneurosci.3813-13.2014 · Cited by 140 · see citing works
Interneuron activity leads to initiation of low‐voltage fast‐onset seizures
Shiri, Z., Manseau, F., Lévesque, M., Williams, S., & Avoli, M. (2014) · Annals of Neurology · doi:10.1002/ana.24342 · Cited by 140 · see citing works
Somatostatin and Somatostatin-Containing Neurons in Shaping Neuronal Activity and Plasticity
Liguz‐Lecznar, M., Urban‐Ciećko, J., & Kossut, M. M. (2016) · Frontiers in Neural Circuits · doi:10.3389/fncir.2016.00048 · Cited by 141 · see citing works
Inhibitory Interneurons and their Circuit Motifs in the Many Layers of the Barrel Cortex
Feldmeyer, D., Qi, G., Emmenegger, V., & Staiger, J. F. (2017) · Neuroscience · doi:10.1016/j.neuroscience.2017.05.027 · Cited by 134 · see citing works
Self-citationMiyoshi, 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
Self-citationCell-type-specific and projection-specific brain-wide reconstruction of single neurons
Lin, R., Wang, R., Yuan, J., Feng, Q., Zhou, Y., Zeng, S., Ren, M., Jiang, S., Ni, H., Zhou, C., et al. (2018) · Nature Methods · doi:10.1038/s41592-018-0184-y · Cited by 132 · see citing works
Laminar and Cellular Distribution of Monoamine Receptors in Rat Medial Prefrontal Cortex
Santana, N., & Artigas, F. (2017) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2017.00087 · Cited by 131 · see citing works
Fogaça, M. V., Wu, M., Li, C., Li, X.-Y., Picciotto, M. R., & Duman, R. S. (2021) · Molecular Psychiatry · doi:10.1038/s41380-020-00916-y · Cited by 129 · see citing works
Inhibitory Circuits in Cortical Layer 5
Naka, A., & Adesnik, H. (2016) · Frontiers in Neural Circuits · doi:10.3389/fncir.2016.00035 · Cited by 130 · see citing works
Distinct Physiological Maturation of Parvalbumin-Positive Neuron Subtypes in Mouse Prefrontal Cortex
Miyamae, T., Chen, K., Lewis, D. A., & González‐Burgos, G. (2017) · Journal of Neuroscience · doi:10.1523/jneurosci.3325-16.2017 · Cited by 129 · see citing works
Self-citationInhibitory circuits of the mammalian main olfactory bulb
Burton, S. D. (2017) · Journal of Neurophysiology · doi:10.1152/jn.00109.2017 · Cited by 124 · see citing works
Cortical inhibitory interneurons control sensory processing
Wood, K. C., Blackwell, J. M., & Geffen, M. N. (2017) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2017.08.018 · Cited by 128 · see citing works
Genetic programs controlling cortical interneuron fate
Kessaris, N., Magno, L., Rubin, A. N., & Oliveira, M. G. (2014) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2013.12.012 · Cited by 122 · see citing works
Modeling Alzheimer's disease with human induced pluripotent stem (iPS) cells
Mungenast, A. E., Siegert, S., & Tsai, L. (2015) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2015.11.010 · Cited by 127 · see citing works
d-Serine and Serine Racemase are Localized to Neurons in the Adult Mouse and Human Forebrain
Balu, D. T., Takagi, S., Puhl, M. D., Benneyworth, M. A., & Coyle, J. T. (2014) · Cellular and Molecular Neurobiology · doi:10.1007/s10571-014-0027-z · Cited by 126 · see citing works
Cortical Interneurons Differentially Shape Frequency Tuning following Adaptation
Natan, R. G., Rao, W., & Geffen, M. N. (2017) · Cell Reports · doi:10.1016/j.celrep.2017.10.012 · Cited by 125 · see citing works
Target-Specific Effects of Somatostatin-Expressing Interneurons on Neocortical Visual Processing
Cottam, J. C. H., Smith, S. L., & Häusser, M. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.2624-13.2013 · Cited by 122 · see citing works
Signature morphoelectric properties of diverse GABAergic interneurons in the human neocortex
Lee, B. R., Dalley, R., Miller, J. A., Chartrand, T., Close, J., Mann, R., Mukora, A., Ng, L., Alfiler, L., Baker, K., et al. (2023) · Science · doi:10.1126/science.adf6484 · Cited by 125 · see citing works
Self-citationToward a Genetic Dissection of Cortical Circuits in the Mouse
Huang, Z. J. (2014) · Neuron · doi:10.1016/j.neuron.2014.08.041 · Cited by 123 · see citing works
- Authors
- DeFelipe, J., López-Cruz, P. L., Benavides-Piccione, R., Bielza, C., Larrañaga, P., Anderson, S., Burkhalter, A., Cauli, B., Fairén, A., Feldmeyer, D., Fishell, G., Fitzpatrick, D., Freund, T. F., González-Burgos, G., Hestrin, S., Hill, S., Hof, P. R., Huang, J., Jones, E. G., Kawaguchi, Y., Kisvárday, Z., Kubota, Y., Lewis, D. A., Marín, O., Markram, H., McBain, C. J., Meyer, H. S., Monyer, H., Nelson, S. B., Rockland, K., Rossier, J., Rubenstein, J. L. R., Rudy, B., Scanziani, M., Shepherd, G. M., Sherwood, C. C., Staiger, J. F., Tamás, G., Thomson, A., Wang, Y., Yuste, R., & Ascoli, G. A.
- Affiliations
- Universidad Politécnica de Madrid (ES)
- Children's Hospital of Philadelphia (US)
- Washington University in St. Louis (US)
- Centre National de la Recherche Scientifique (FR)
- Instituto de Neurociencias (ES)
- Forschungszentrum Jülich (DE)
- NYU Langone Health (US)
- Max Planck Florida Institute for Neuroscience (US)
- HUN-REN Institute of Experimental Medicine (HU)
- Stanford Medicine (US)
- École Polytechnique Fédérale de Lausanne (CH)
- Icahn School of Medicine at Mount Sinai (US)
- National Institute for Physiological Sciences (JP)
- University of Debrecen (HU)
- University of Pittsburgh (US)
- Eunice Kennedy Shriver National Institute of Child Health and Human Development (US)
- Technical University of Munich (DE)
- German Cancer Research Center (DE)
- Brandeis University (US)
- Boston University (US)
- Inserm (FR)
- University of California, San Francisco (US)
- New York University (US)
- Howard Hughes Medical Institute (US)
- Yale University (US)
- George Washington University (US)
- University of Göttingen (DE)
- University of Szeged (HU)
- UCL School of Pharmacy (GB)
- Wenzhou Medical University (CN)
- George Mason University (US)
- Corresponding author
- DeFelipe, Javier
- Larrañaga, Pedro
- Ascoli, Giorgio A.
- ORCID
- DeFelipe, Javier
- Bielza, Concha
- Larrañaga, Pedro
- Anderson, Stewart
- Burkhalter, Andreas
- Cauli, Bruno
- Feldmeyer, Dirk
- Fishell, Gord
- Freund, Tamás F.
- Hill, Sean
- Hof, Patrick R.
- Jones, Edward G.
- Kawaguchi, Yasuo
- Kisvárday, Zoltán
- Kubota, Yoshiyuki
- Lewis, David A.
- Markram, Henry
- McBain, Chris J.
- Meyer, Hanno S.
- Monyer, Hannah
- Nelson, Sacha B.
- Rockland, Kathleen
- Rossier, Jean
- Rubenstein, John L. R.
- Rudy, Bernardo
- Scanziani, Massimo
- Shepherd, Gordon M.
- Sherwood, Chet C.
- Staiger, Jochen F.
- Tamás, Gábor
- Yuste, Rafael
- Ascoli, Giorgio A.
- Venue
- Nature Reviews Neuroscience
- Published
- 2013-02-06
- Volume
- 14
- Issue
- 3
- Pages
- 202-216
- ISSN
- 1471-003X (ISSN-L)
- 1471-0048
- PMC
- PMC3619199
- OpenAlex
- W1995031373
- Cited by
- 833
- References
- 40
- Citations by year
- 2026: 23 · 2025: 44 · 2024: 48 · 2023: 57 · 2022: 62 · 2021: 56 · 2020: 72 · 2019: 71 · 2018: 63 · 2017: 72 · 2016: 67 · 2015: 86 · 2014: 79 · 2013: 33
- FWCI
- 8.99
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Nature reviews. Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- JuSER (Forschungszentrum Jülich) (publishedVersion)
- Repository of the Academy's Library (Library of the Hungarian Academy of Sciences) (acceptedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Cold Spring Harbor Laboratory Institutional Repository (Cold Spring Harbor Laboratory) (acceptedVersion)
- HAL (submittedVersion)
- DIGITAL.CSIC (Spanish National Research Council (CSIC)) (submittedVersion)
- UCL Discovery (University College London) (submittedVersion)
- eScholarship (California Digital Library) (submittedVersion)
- University of Debrecen Electronic Archive (University of Debrecen) (submittedVersion, other-oa)
- Infoscience (Ecole Polytechnique Fédérale de Lausanne) (submittedVersion)
- mediaTUM (Technical University of Munich) (submittedVersion)
- Archivo Digital UPM (Universidad Politécnica de Madrid) (submittedVersion, cc-by-nc-nd)
- GRO (submittedVersion)
- RWTH Publications (RWTH Aachen) (submittedVersion)
- Funders
- École Polytechnique Fédérale de Lausanne
- Ministerio de Economía y Competitividad (C04-04, TIN2010-20900-C04-04)
- National Institutes of Health (5r01ns030989-22)
- U.S. Public Health Service (R01-39600)
- Japan Society for the Promotion of Science (21240030)
- National Institute of Mental Health (R01MH043784)
- National Eye Institute (R01EY012114, R01EY011787)
- National Institute on Deafness and Other Communication Disorders (R01DC009977, P01DC004732)
- National Institute of Diabetes and Digestive and Kidney Diseases (P30DK063720)
- National Institute of Neurological Disorders and Stroke (R01-NS030989, R01NS039600, R01NS075007)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Biophysics › Cell Image Analysis Techniques
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Keywords
- GABAergic interneurons, cortical interneurons, neuron classification, cerebral cortex, neuronal morphology, Bayesian analysis, clustering algorithms, supervised classification, community consensus, taxonomy
- MeSH terms
- Algorithms, Animals, Bayes Theorem, Cerebral Cortex, gamma-Aminobutyric Acid, Humans, Interneurons, Terminology as Topic, Cluster Analysis
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