Axon Branching and Synaptic Bouton Phenotypes in GABAergic Nonpyramidal Cell Subtypes
Open accessAbstract
GABAergic nonpyramidal cells, cortical interneurons, consist of heterogeneous subtypes differing in their axonal field and target selectivity. It remains to be investigated how the diverse innervation patterns are generated and how these spatially complicated, but synaptically specific wirings are achieved. Here, we asked whether a particular cell type obeys a specific branching and bouton arrangement principle or differs from others only in average morphometric values of the morphological template common to nonpyramidal cells. For this purpose, we subclassified nonpyramidal cells within each physiological class by quantitative parameters of somata, dendrites, and axons and characterized axon branching and bouton distribution patterns quantitatively. Each subtype showed a characteristic set of vertical and horizontal bouton spreads around the somata. Each parameter, such as branching angles, internode or interbouton intervals, followed its own characteristic distribution pattern irrespective of subtypes, suggesting that nonpyramidal cells have the common mechanism for formation of the axon branching pattern and bouton arrangement. Fitting of internode and interbouton interval distributions to the exponential indicated their apparent random occurrence. Decay constants of the fitted exponentials varied among nonpyramidal cells, but each subtype expressed a particular set of interbouton and internode interval averages. The distinctive combination of innervation field shape and local axon phenotypes suggests a marked functional difference in the laminar and columnar integration properties of different GABAergic subtypes, as well as the subtype-specific density of inhibited targets.
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Dendrite targeting CCK-expressing interneurons are also found in the neocortex, most notably the vertically oriented bitufted double bouquet cells with ascending and descending tight radial axonal bundles targeting principal cell dendritic shafts and spines.
“Dendrite targeting CCK-expressing interneurons are also found in the neocortex, most notably the vertically oriented bitufted double bouquet cells with ascending and descending tight radial axonal bundles targeting principal cell dendritic shafts and spines (263, 355, 556, 569, 1034, 1085, 1150).”
From Hippocampal GABAergic Inhibitory Interneurons (2017) · cites this paper as [556]
Additional molecular markers commonly associated with hippocampal and neocortical CCK-expressing dendrite targeting interneurons are calbindin (CB) (hippocampus and neocortex), calretinin (CR) (neocortex), and VIP (neocortex), though none of these markers is specific for or ubiquitously expressed by CCK-expressing dendrite targeting interneurons.
“Additional molecular markers commonly associated with hippocampal and neocortical CCK-expressing dendrite targeting interneurons are calbindin (CB) (hippocampus and neocortex), calretinin (CR) (neocortex), and VIP (neocortex), though none of these markers is specific for or ubiquitously expressed by CCK-expressing dendrite targeting interneurons (224, 556, 569, 584, 611, 612).”
From Hippocampal GABAergic Inhibitory Interneurons (2017) · cites this paper as [556]
PV+ interneuron axons branch extensively and provide dense inhibition to nearby pyramidal neurons in cortical circuits.
“PV+ interneuron axons branch extensively (Karube, 2004) and provide dense inhibition to nearby pyramidal neurons in cortical circuits (Packer and Yuste, 2011).”
From Does puberty mark a transition in sensitive periods for plasticity in the associative neocortex? (2017) · cites this paper as Karube, 2004
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Cites
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
Self-citationCortex: Statistics and Geometry of Neuronal Connectivity
Braitenberg, V., & Schüz, A. (1998) · doi:10.1007/978-3-662-03733-1 · Cited by 1,178 · cited 1× · see citing works
“The overall innervation pattern depends on the manner of axonal outgrowth and branching and on the arrangement of presynaptic specializations along the axon (Hellwig et al., 1994; Braitenberg and Schütz, 1998; Anderson et al., 2002).”
BackgroundOrganizing 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
DeFelipe, J., & Fariñas, I. (1992) · Progress in Neurobiology · doi:10.1016/0301-0082(92)90015-7 · Cited by 975 · see citing works
Somogyi, P., Tamás, G., Luján, R., & Buhl, E. H. (1998) · Brain Research Reviews · doi:10.1016/s0165-0173(97)00061-1 · Cited by 860 · see citing works
Molecular and Physiological Diversity of Cortical Nonpyramidal Cells
Cauli, B., Audinat, E., Lambolez, B., Angulo, M. C., Ropert, N., Tsuzuki, K., Hestrin, S., & Rossier, J. (1997) · Journal of Neuroscience · doi:10.1523/jneurosci.17-10-03894.1997 · Cited by 738 · see citing works
Histology Of The Nervous System
Cajal, S. R. Y., Azoulay, D. L., swanson, N., & Swanson, L. W. (1995) · doi:10.1093/oso/9780195074017.001.0001 · Cited by 634 · see citing works
The ‘module-concept’ in cerebral cortex architecture
Szentágothai, J. (1975) · Brain Research · doi:10.1016/0006-8993(75)90122-5 · Cited by 614 · see citing works
Jones, E. G. (1975) · The Journal of Comparative Neurology · doi:10.1002/cne.901600204 · Cited by 593 · see citing works
Ribak, C. E. (1978) · Journal of Neurocytology · doi:10.1007/bf01173991 · Cited by 551 · see citing works
DeFelipe, J. (1997) · Journal of Chemical Neuroanatomy · doi:10.1016/s0891-0618(97)10013-8 · Cited by 550 · see citing works
Kawaguchi, Y. (1995) · The Journal of Neuroscience · doi:10.1523/jneurosci.15-04-02638.1995 · Cited by 533 · see citing works
Self-citationA specific ‘axo-axonal’ interneuron in the visual cortex of the rat
Somogyi, P. (1977) · Brain Research · doi:10.1016/0006-8993(77)90808-3 · Cited by 530 · see citing works
Shepherd, G. M. G., & Harris, K. M. (1998) · The Journal of Neuroscience · doi:10.1523/jneurosci.18-20-08300.1998 · Cited by 502 · see citing works
Three distinct families of GABAergic neurons in rat visual cortex
Gonchar, Y. (1997) · Cerebral Cortex · doi:10.1093/cercor/7.4.347 · Cited by 481 · see citing works
Kawaguchi, Y., & Kondo, S. (2002) · Journal of Neurocytology · doi:10.1023/a:1024126110356 · Cited by 395 · see citing works
Self-citationThe axo-axonic interneuron in the cerebral cortex of the rat, cat and monkey
Somogyi, P., Freund, T. F., & Cowey, A. (1982) · Neuroscience · doi:10.1016/0306-4522(82)90086-0 · Cited by 392 · see citing works
Kawaguchi, Y. (1993) · Journal of Neurophysiology · doi:10.1152/jn.1993.69.2.416 · Cited by 390 · see citing works
Self-citationKawaguchi, Y., & Kubota, Y. (1996) · The Journal of Neuroscience · doi:10.1523/jneurosci.16-08-02701.1996 · Cited by 380 · see citing works
Self-citationWang, Y. (2002) · Cerebral Cortex · doi:10.1093/cercor/12.4.395 · Cited by 371 · see citing works
Three distinct subpopulations of GABAergic neurons in rat frontal agranular cortex
Kubota, Y., Hattori, R., & Yui, Y. (1994) · Brain Research · doi:10.1016/0006-8993(94)91060-x · Cited by 365 · see citing works
Self-citationIdentified 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
Cortical Circuits: Synaptic Organization of the Cerebral Cortex Structure, Function, and Theory
White, E. L., & Keller, A. (1989) · Cited by 333 · see citing works
Freund, T. F., Martin, K. A. C., Smith, A. D., & Somogyi, P. (1983) · Journal of Comparative Neurology · doi:10.1002/cne.902210303 · Cited by 329 · see citing works
Classification of fusiform neocortical interneurons based on unsupervised clustering
Cauli, B., Porter, J. T., Tsuzuki, K., Lambolez, B., Rossier, J., Quenet, B., & Audinat, E. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.97.11.6144 · Cited by 316 · see citing works
The forms of non‐pyramidal neurons in the visual cortex of the rat
Feldman, M. L., & Peters, A. (1978) · The Journal of Comparative Neurology · doi:10.1002/cne.901790406 · Cited by 303 · see citing works
Kawaguchi, Y., & Kubota, Y. (1998) · Neuroscience · doi:10.1016/s0306-4522(97)00685-4 · Cited by 294 · see citing works
Self-citationTamás, G., Buhl, E. H., & Somogyi, P. (1997) · The Journal of Physiology · doi:10.1113/jphysiol.1997.sp022054 · Cited by 278 · see citing works
Connectivity and Convergence of Single Corticostriatal Axons
Kincaid, A. E., Zheng, T., & Wilson, C. J. (1998) · Journal of Neuroscience · doi:10.1523/jneurosci.18-12-04722.1998 · Cited by 277 · see citing works
Thomson, A. M., West, D. C., Hahn, J. D., & Deuchars, J. (1996) · The Journal of Physiology · doi:10.1113/jphysiol.1996.sp021667 · Cited by 275 · see citing works
Houser, C. R., Hendry, S. H. C., Jones, E. G., & Vaughn, J. E. (1983) · Journal of Neurocytology · doi:10.1007/bf01181527 · Cited by 270 · see citing works
Amir, Y., Harel, M., & Malach, R. (1993) · The Journal of Comparative Neurology · doi:10.1002/cne.903340103 · Cited by 269 · see citing works
Kisvárday, Z. F., Martin, K. A. C., Whitteridge, D., & Somogyi, P. (1985) · Journal of Comparative Neurology · doi:10.1002/cne.902410202 · Cited by 200 · see citing works
Problems of the Keimbahn. New work on mammalian germ cell lineage.
Sturrock, R. R. (1983) · PubMed · Cited by 182 · see citing works
Morrison, J., Magistretti, P., Benoit, R., & Bloom, F. (1984) · Brain Research · doi:10.1016/0006-8993(84)90763-7 · Cited by 176 · see citing works
Heterogeneity of GABAergic cells in cat visual cortex
Demeulemeester, H. G., Vandesande, F., Orban, G. A., Brandon, C. J., & Vanderhaeghen, J. (1988) · Journal of Neuroscience · doi:10.1523/jneurosci.08-03-00988.1988 · Cited by 164 · see citing works
Dependence of GABAergic Synaptic Areas on the Interneuron Type and Target Size
Kubota, Y., & Kawaguchi, Y. (2000) · Journal of Neuroscience · doi:10.1523/jneurosci.20-01-00375.2000 · Cited by 161 · see citing works
Self-citationComputational neuroanatomy : principles and methods
Ascoli, G. A. (2002) · Humana Press eBooks · Cited by 146 · see citing works
Properties of unitary IPSPs evoked by anatomically identified basket cells in the rat hippocampus
Buhl, E., Cobb, S., Halasy, K., & Somogyi, P. (1995) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.1995.tb00721.x · Cited by 124 · see citing works
Distinct Firing Patterns of Neuronal Subtypes in Cortical Synchronized Activities
Kawaguchi, Y. (2001) · Journal of Neuroscience · doi:10.1523/jneurosci.21-18-07261.2001 · Cited by 123 · see citing works
Self-citationStereotypy in neocortical microcircuits
Silberberg, G., Gupta, A., & Markram, H. (2002) · Trends in Neurosciences · doi:10.1016/s0166-2236(02)02151-3 · Cited by 117 · see citing works
Shepherd, G. M., Raastad, M., & Andersen, P. N. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.052151299 · Cited by 108 · see citing works
Two distinct subgroups of cholecystokinin-immunoreactive cortical interneurons
Kubota, Y., & Kawaguchi, Y. (1997) · Brain Research · doi:10.1016/s0006-8993(96)01446-1 · Cited by 93 · see citing works
Self-citationIntrinsic Physiology and Morphology of Single Neurons in Neocortex
Amitai, Y., & Connors, B. W. (1995) · Cerebral cortex · doi:10.1007/978-1-4757-9616-2_7 · Cited by 84 · see citing works
Hellwig, B., Schüz, A., & Aertsen, A. (1994) · Biological Cybernetics · doi:10.1007/bf00198906 · Cited by 71 · see citing works
Chance or design? Some specific considerations concerning synaptic boutons in cat visual cortex
Anderson, J. C., Binzegger, T., Douglas, R. J., & Martin, K. A. C. (2002) · Journal of Neurocytology · doi:10.1023/a:1024113707630 · Cited by 43 · see citing works
General Organization of the Cerebral Cortex
White, E. L. (1989) · Birkhäuser Boston eBooks · doi:10.1007/978-1-4684-8721-3_1 · Cited by 38 · see citing works
Constant and variable aspects of axonal phenotype in cerebral cortex
Tettoni, L. (1998) · Cerebral Cortex · doi:10.1093/cercor/8.6.543 · Cited by 36 · see citing works
The number and distribution of Meynert cells in area 17 of the macaque monkey
Winfield, D. A., Rivera‐Dominguez, M., & Powell, T. P. S. (1981) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.1981.0051 · Cited by 31 · see citing works
Maxsim, software for the analysis of multiple axonal arbors and their simulated activation
Tettoni, L., Lehmann, P., Houzel, J., et al. (1996) · Journal of Neuroscience Methods · doi:10.1016/0165-0270(95)00095-x · Cited by 20 · see citing works
Some Approaches to Quantitative Dendritic Morphology
Burke, R. E., & Marks, W. B. (2002) · Humana Press eBooks · doi:10.1007/978-1-59259-275-3_2 · Cited by 14 · see citing works
The Digestive System in Mammals. Food, Form and Function
Carr, K. E. (1995) · Europe PMC (PubMed Central) · Cited by 13 · see citing works
Some Approaches to Quantitative Dendritic Morphology
Burke, R. E., & Marks, W. B. (2003) · Humana Press eBooks · doi:10.1385/1-59259-275-9:27 · Cited by 11 · see citing works
Local Circuit Neurons in the Frontal Cortico-Striatal System
Kawaguchi, Y. (2003) · Springer eBooks · doi:10.1007/978-1-4615-0039-1_9 · Cited by 7 · see citing works
Self-citationAhmed-Jackson, R., & Magazine, T. T. P. (1998) · The Philosophers Magazine · doi:10.5840/tpm1998277 · Cited by 5 · see citing works
Flagged first, then by citations
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GABAergic Interneurons in the Neocortex: From Cellular Properties to Circuits
Tremblay, R., Lee, S., & Rudy, B. (2016) · Neuron · doi:10.1016/j.neuron.2016.06.033 · Cited by 2,033 · see citing works
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
Hu, H., Gan, J., & Jonas, P. (2014) · Science · doi:10.1126/science.1255263 · Cited by 1,197 · 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
Packer, A. M., & Yuste, R. (2011) · The Journal of Neuroscience · doi:10.1523/jneurosci.3131-11.2011 · Cited by 506 · see citing works
Murakami, S., & Okada, Y. (2006) · The Journal of Physiology · doi:10.1113/jphysiol.2006.105379 · Cited by 395 · see citing works
Regulation of cortical microcircuits by unitary GABA-mediated volume transmission
Oláh, S., Füle, M., Komlósi, G., Varga, C., Báldi, R., Barzó, P., & Tamás, G. (2009) · Nature · doi:10.1038/nature08503 · Cited by 386 · see citing works
Neuronal activity is required for the development of specific cortical interneuron subtypes
De Marco García, N. V., Karayannis, T., & Fishell, G. (2011) · Nature · doi:10.1038/nature09865 · Cited by 294 · 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
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
Self-citationUematsu, 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
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Excitatory signal flow and connectivity in a cortical column: focus on barrel cortex.
Lübke, J., & Feldmeyer, D. (2007) · Brain Structure and Function · doi:10.1007/s00429-007-0144-2 · Cited by 233 · see citing works
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Yavorska, I., & Wehr, M. (2016) · Frontiers in Neural Circuits · doi:10.3389/fncir.2016.00076 · Cited by 185 · see citing works
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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
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
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- Authors
- Karube, F., Kubota, Y., & Kawaguchi, Y.
- Affiliations
- National Institute for Physiological Sciences (JP)
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2004-03-24
- Volume
- 24
- Issue
- 12
- Pages
- 2853-2865
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC6729850
- OpenAlex
- W2071097942
- Cited by
- 203
- References
- 55
- Citations by year
- 2026: 6 · 2025: 6 · 2024: 5 · 2023: 7 · 2022: 13 · 2021: 8 · 2020: 11 · 2019: 7 · 2018: 7 · 2017: 11 · 2016: 12 · 2015: 10 · 2014: 7 · 2013: 16 · 2012: 8
- FWCI
- 3.52
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Daiko Foundation
- Ministry of Education, Culture, Sports, Science and Technology
- Toyota Physical and Chemical Research Institute
- Japan Epilepsy Research Foundation
- Epilepsiatutkimussäätiö
- Japan Society for the Promotion of Science
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Axon Guidance and Neuronal Signaling
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Keywords
- cortical interneurons, axon branching, innervation pattern, branch angle, neuronal morphology
- MeSH terms
- Analysis of Variance, Animals, Axons, Cell Separation, gamma-Aminobutyric Acid, Neurons, Phenotype, Regression Analysis, Cluster Analysis, Rats, Wistar, Presynaptic Terminals, Patch-Clamp Techniques, Rats, In Vitro Techniques
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