The development, structure and function of glial cells in the nervous system of Drosophila melanogaster
DOI:
https://doi.org/10.33910/2687-1270-2020-1-3-202-211Keywords:
glial cells, Drosophila melanogaster, nervous system, neurons, neuropilAbstract
Glia is the most common cell type in the central nervous system. Interest in them has increased significantly over the past decades as it has become clear that glia are not just “support” cells for neurons. They also regulate important aspects of the development and functioning of the nervous system. In vertebrates, glial cells perform supporting, trophic, secretory, dividing and protective functions. Despite the fact that the nervous system of Drosophila melanogaster has a simple structure, it is similar in function to mammalian glia. The similarity of glia of Drosophila melanogaster and mammals at the molecular and morphological levels suggests that the study of invertebrate glia will provide a better understanding of the main issues in the development of glia in mammals. Using Drosophila melanogaster makes it possible to study various neuron-glia interactions in an intact organism and the use of a wide range of molecular genetic methods allows us to investigate fundamental questions about the nature of glia. The review presents the classification of glial cells in Drosophila melanogaster, describes the currently known functions of all glial cell types in insects, and compares the functions of various glia types of mammals and Drosophila glial cells.
References
Abbott, N. J. (2005) Dynamics of CNS barriers: Evolution, differentiation, and modulation. Cellular and Molecular Neurobiology, vol. 25, no. 1, pp. 5–23. PMID: 15962506. DOI: 10.1007/s10571-004-1374-y (In English)
Allen, N. J., Lyons, D. A. (2018) Glia as architects of central nervous system formation and function. Science, vol. 362, no. 6411, pp. 181–185. PMID: 30309945. DOI: 10.1126/science.aat0473 (In English)
Avet-Rochex, A., Kaul, A. K., Gatt, A. P. et al. (2012) Concerted control of gliogenesis by InR/TOR and FGF signalling in the Drosophila post-embryonic brain. Development, vol. 139, no. 15, pp. 2763–2772. PMID: 22745312. DOI: 10.1242/dev.074179 (In English)
Awasaki, T., Ito, K. (2004) Engulfing action of glial cells is required for programmed axon pruning during Drosophila metamorphosis. Current Biology, vol. 14, no. 8, pp. 668–677. PMID: 15084281. DOI: 10.1016/j.cub.2004.04.001 (In English)
Awasaki, T., Lai, S.-L., Ito, K., Lee, T. (2008) Organization and postembryonic development of glial cells in the adult central brain of Drosophila. The Journal of Neuroscience, vol. 28, no. 51, pp. 13742–13753. PMID: 19091965. DOI: 10.1523/jneurosci.4844-08.2008 (In English)
Bailey, A. P., Koster, G., Guillermier, C. et al. (2015) Antioxidant role for lipid droplets in a stem cell niche of Drosophila. Cell, vol. 163, no. 2, pp. 340–353. PMID: 26451484. DOI: 10.1016/j.cell.2015.09.020 (In English)
Bainton, R. J., Tsai, L. T.-Y., Schwabe, T. et al. (2005) Moody encodes two GPCRs that regulate cocaine behaviors and blood-brain barrier permeability in Drosophila. Cell, vol. 123, no. 1, pp. 145–156. PMID: 16213219. DOI: 10.1016/j.cell.2005.07.029 (In English)
Barres, B. A. (2008) The mystery and magic of glia: A perspective on their roles in health and disease. Neuron, vol. 60, no. 3, pp. 430–440. PMID: 18995817. DOI: 10.1016/j.neuron.2008.10.013 (In English)
Baumgartner, S., Littleton, J. T., Broadie, K. et al. (1996) A Drosophila neurexin is required for septate junction and blood-nerve barrier formation and function. Cell, vol. 87, no. 6, pp. 1059–1068. PMID: 8978610. DOI: 10.1016/s0092-8674(00)81800-0 (In English)
Belanger, M., Allaman, I., Magistretti, P. J. (2011) Brain energy metabolism: Focus on astrocyte-neuron metabolic cooperation. Cell Metabolism, vol. 14, no. 6, pp. 724–738. PMID: 22152301. DOI: 10.1016/j.cmet.2011.08.016 (In English)
Blinkov, S. M., Glezer, I. I. (1968) The human brain in figures and tables: A quantitative handbook. New York: Plenum Publ., xxxiv + 482 p. (In English)
Boche, D., Perry, V. H., Nicoll, J. A. R. (2013) Review: Activation patterns of microglia and their identification in the human brain. Neuropathology and Applied Neurobiology, vol. 39, no. 1, pp. 3–18. PMID: 23252647. DOI: 10.1111/nan.12011 (In English)
Bossing, T., Udolph, G., Doe, C. Q., Technau, G. M. (1996) The embryonic central nervous system lineages of Drosophila melanogaster. I. Neuroblast lineages derived from the ventral half of the neuroectoderm. Developmental Biology, vol. 179, no. 1, pp. 41–64. PMID: 8873753. DOI: 10.1006/dbio.1996.0240 (In English)
Colonques, J., Ceron, J., Tejedor, F. J. (2007) Segregation of postembryonic neuronal and glial lineages inferred from a mosaic analysis of the Drosophila larval brain. Mechanisms of Development, vol. 124, no. 5, pp. 327–340. PMID: 17344035. DOI: 10.1016/j.mod.2007.01.004 (In English)
Corty, M. M., Freeman, M. R. (2013) Architects in neural circuit design: Glia control neuron numbers and connectivity. The Journal of Cell Biology, vol. 203, no. 3, pp. 395–405. PMID: 24217617. DOI: 10.1083/jcb.201306099 (In English)
Delgehyr, N., Meunier, A., Faucourt, M. et al. (2015) Ependymal cell differentiation, from monociliated to multiciliated cells. Methods in Cell Biology, vol. 127, pp. 19–35. PMID: 25837384. DOI: 10.1016/bs.mcb.2015.01.004 (In English)
Desalvo, M. K., Mayer, N., Mayer, F., Bainton, R. J. (2011) Physiologic and anatomic characterization of the brain surface glia barrier of Drosophila. Glia, vol. 59, no. 9, pp. 1322–1340. PMID: 21351158. DOI: 10.1002/glia.21147 (In English)
Dimou, L., Simons, M. (2017) Diversity of oligodendrocytes and their progenitors. Current Opinion in Neurobiology, vol. 47, pp. 73–79. PMID: 29078110. DOI: 10.1016/j.conb.2017.09.015 (In English)
Dumstrei, K., Wang, F., Hartenstein, V. (2003) Role of DE-cadherin in neuroblast proliferation, neural morphogenesis, and axon tract formation in Drosophila larval brain development. The Journal of Neuroscience, vol. 23, no. 8, pp. 3325–3335. PMID: 12716940. DOI: 10.1523/JNEUROSCI.23-08-03325.2003 (In English)
Ebens, A. J., Garren, H., Cheyette, B. N., Zipursky, S. L. (1993) The Drosophila anachronism locus: A glycoprotein secreted by glia inhibits neuroblast proliferation. Cell, vol. 74, no. 1, pp. 15–27. PMID: 7916657. DOI: 10.1016/0092-8674(93)90291-w (In English)
Edwards, J. S., Swales, L. S., Bate, M. (1993) The differentiation between neuroglia and connective tissue sheath in insect ganglia revisited: The neural lamella and perineurial sheath cells are absent in a mesodermless mutant of Drosophila. The Journal of Comparative Neurology, vol. 333, no. 2, pp. 301–308. PMID: 8345109. DOI: 10.1002/cne.903330214 (In English)
Edwards, T. N., Meinertzhagen, I. A. (2010) The functional organisation of glia in the adult brain of Drosophila and other insects. Progress in Neurobiology, vol. 90, no. 4, pp. 471–497. PMID: 20109517. DOI: 10.1016/j.pneurobio.2010.01.001 (In English)
Freeman, M. R. (2015) Drosophila central nervous system glia. Cold Spring Harbor Perspectives in Biology, vol. 7, no. 11, article a020552. PMID: 25722465. DOI: 10.1101/cshperspect.a020552 (In English)
Freeman, M. R., Delrow, J., Kim, J. et al. (2003) Unwrapping glial biology: Gcm target genes regulating glial development, diversification, and function. Neuron, vol. 38, no. 4, pp. 567–580. PMID: 12765609. DOI: 10.1016/s0896-6273(03)00289-7 (In English)
Freeman, M. R., Doherty, J. (2006) Glial cell biology in Drosophila and vertebrates. Trends in Neurosciences, vol. 29, no. 2, pp. 82–90. PMID: 16377000. DOI: 10.1016/j.tins.2005.12.002 (In English)
Gilmour, D. T., Maischein, H.-M., Nusslein-Volhard, C. (2002) Migration and function of a glial subtype in the vertebrate peripheral nervous system. Neuron, vol. 34, no. 4, pp. 577–588. PMID: 12062041. DOI: 10.1016/s0896-6273(02)00683-9 (In English)
Gilyarov, M. S. (ed.). (1986) Biologicheskij entsiklopedicheskij slovar’ [Biological encyclopedic dictionary]. Moscow: Sovetskaya Entsiklopediya Publ., 831 p. (In Russian)
Hartenstein, V. (2011) Morphological diversity and development of glia in Drosophila. Glia, vol. 59, no. 9, pp. 1237–1252. PMID: 21438012. DOI: 10.1002/glia.21162 (In English)
Holcroft, C. E., Jackson, W. D., Lin, W.-H. et al. (2013) Innexins Ogre and Inx2 are required in glial cells for normal postembryonic development of the Drosophila central nervous system. Journal of Cell Science, vol. 126, no. 17, pp. 3823–3834. PMID: 23813964. DOI: 10.1242/jcs.117994 (In English)
Hoyle, G. (1986) Glial cells of an insect ganglion. Journal of Comparative Neurology, vol. 246, no. 1, pp. 85–103. DOI: 10.1002/cne.902460106 (In English)
Huang, Y., Ng, F. S., Jackson, F. R. (2015) Comparison of larval and adult Drosophila astrocytes reveals stage-specific gene expression profiles. G3: Genes, Genomes, Genetics, vol. 5, no. 4, pp. 551–558. PMID: 25653313. DOI: 10.1534/g3.114.016162 (In English)
Ito, K., Urban, J., Technau, G. M. (1995) Distribution, classification, and development of Drosophila glial cells in the late embryonic and early larval ventral nerve cord. Roux’s Archives of Developmental Biology, vol. 204, no. 5, pp. 284–307. PMID: 28306125. DOI: 10.1007/BF02179499 (In English)
Juang, J. L., Carlson, S. D. (1992) A blood-brain barrier without tight junctions in the fly central nervous system in the early postembryonic stage. Cell & Tissue Research, vol. 270, no. 1, pp. 95–103. (In English)
Kanai, M. I., Kim, M. J., Akiyama, T. et al. (2018) Regulation of neuroblast proliferation by surface glia in the Drosophila larval brain. Scientific Reports, vol. 8, no. 1, article 3730. PMID: 29487331. DOI: 10.1038/s41598-018-22028-y (In English)
Kidd, G. J., Ohno, N., Trapp, B. D. (2013) Biology of Schwann cells. Handbook of Clinical Neurology, vol. 115, no. 1, pp. 55–79. PMID: 23931775. DOI: 10.1016/B978-0-444-52902-2.00005-9 (In English)
Kim, S. N., Jeibmann, A., Halama, K. et al. (2014) ECM stiffness regulates glial migration in Drosophila and mammalian glioma models. Development, vol. 141, no. 16, pp. 3233–3242. PMID: 25063458. DOI: 10.1242/dev.106039 (In English)
Kis, V., Barti, B., Lippai, M., Sass, M. (2015) Specialized cortex glial cells accumulate lipid droplets in Drosophila melanogaster. PLoS One, vol. 10, no. 7, article e0131250. PMID: 26148013. DOI: 10.1371/journal.pone.0131250 (In English)
Klambt, C., Jacobs, J. R., Goodman, C. S. (1991) The midline of the Drosophila central nervous system: A model for the genetic analysis of cell fate, cell migration, and growth cone guidance. Cell, vol. 64, no. 4, pp. 801–815. PMID: 1997208. DOI: 10.1016/0092-8674(91)90509-w (In English)
Kremer, M. C., Jung, C., Batelli, S. et al. (2017) The glia of the adult Drosophila nervous system. Glia, vol. 65, no. 4, pp. 606–638. PMID: 28133822. DOI: 10.1002/glia.23115 (In English)
Kretzschmar, D., Hasan, G., Sharma, S. et al. (1997) The swiss cheese mutant causes glial hyperwrapping and brain 22 degeneration in Drosophila. The Journal of Neuroscience, vol. 17, no. 19, pp. 7425–7432. PMID: 9295388. DOI: 10.1523/JNEUROSCI.17-19-07425.1997 (In English)
Leiserson, W. M., Harkins, E. W., Keshishian, H. (2000) Fray, a Drosophila serine/threonine kinase homologous to mammalian PASK, is required for axonal ensheathment. Neuron, vol. 28, no. 3, pp. 793–806. PMID: 11163267. DOI: 10.1016/s0896-6273(00)00154-9 (In English)
Matzat, T., Sieglitz, F., Kottmeier, R. et al. (2015) Axonal wrapping in the Drosophila PNS is controlled by gliaderived neuregulin homolog Vein. Development, vol. 142, no. 7, pp. 1336–1345. PMID: 25758464. DOI: 10.1242/dev.116616 (In English)
Mayer, F., Mayer, N., Chinn, L. et al. (2009) Evolutionary conservation of vertebrate blood-brain barrier chemoprotective mechanisms in Drosophila. The Journal of Neuroscience, vol. 29, no. 11, pp. 3538–3550. PMID: 19295159. DOI: 10.1523/JNEUROSCI.5564-08.2009 (In English)
Melom, J. E., Littleton, J. T. (2013) Mutation of a NCKX eliminates glial microdomain calcium oscillations and enhances seizure susceptibility. The Journal of Neuroscience, vol. 33, no. 3, pp. 1169–1178. PMID: 23325253. DOI: 10.1523/JNEUROSCI.3920-12.2013 (In English)
Meyer, S., Schmidt, I., Klambt, C. (2014) Glia ECM interactions are required to shape the Drosophila nervous system. Mechanisms of Development, vol. 133, no. 23, pp. 105–116. PMID: 24859129. DOI: 10.1016/j.mod.2014.05.003 (In English)
Nave, K.-A., Trapp, B. D. (2008) Axon-glial signaling and the glial support of axon function. Annual Review of Neuroscience, vol. 31, pp. 535–561. PMID: 18558866. DOI: 10.1146/annurev.neuro.30.051606.094309 (In English)
Nave, K.-A., Werner, H. B. (2014) Myelination of the nervous system: Mechanisms and functions. Annual Review of Cell and Developmental Biology, vol. 30, pp. 503–533. PMID: 25288117. DOI: 10.1146/annurevcellbio-100913-013101 (In English)
Ng, F. S., Sengupta, S., Huang, Y. et al. (2016) TRAP-seq profiling and RNAi-based genetic screens identify conserved glial genes required for adult Drosophila behavior. Frontiers in Molecular Neuroscience, vol. 9, article 146. PMID: 28066175. DOI: 10.3389/fnmol.2016.00146 (In English)
Obermeier, B., Verma, A., Ransohoff, R. M. (2016) The blood-brain barrier. In: S. J. Pittock, A. Vincent (eds.). Autoimmune neurology. S. l.: Elsevier Science, pp. 39–59. (Handbook of Clinical Neurology. Vol. 133). PMID: 27112670. DOI: 10.1016/B978-0-444-63432-0.00003-7 (In English)
Omoto, J. J., Lovick, J. K., Hartenstein, V. (2016) Origins of glial cell populations in the insect nervous system. Current Opinion in Insect Science, vol. 18, pp. 96–104. PMID: 27939718. DOI: 10.1016/j.cois.2016.09.003 (In English)
Omoto, J. J., Yogi, P., Hartenstein, V. (2015) Origin and development of neuropil glia of the Drosophila larval and adult brain: Two distinct glial populations derived from separate progenitors. Developmental Biology, vol. 404, no. 2, pp. 2–20. PMID: 25779704. DOI: 10.1016/j.ydbio.2015.03.004 (In English)
Pandey, R., Blanco, J., Udolph, G. (2011) The glucuronyltransferase GlcAT-P is required for stretch growth of peripheral nerves in Drosophila. PLoS One, vol. 6, no. 11, article e28106. PMID: 22132223. DOI: 10.1371/journal.pone.0028106 (In English)
Peco, E., Davla, S., Camp, D. et al. (2016) Drosophila astrocytes cover specific territories of the CNS neuropil and are instructed to differentiate by Prospero, a key effector of Notch. Development, vol. 143, no. 7, pp. 1170–1181. PMID: 26893340. DOI: 10.1242/dev.133165 (In English)
Pennetta, G., Welte, M. A. (2018) Emerging links between lipid droplets and motor neuron diseases. Developmental Cell, vol. 45, no. 4, pp. 427–432. PMID: 29787708. DOI: 10.1016/j.devcel.2018.05.002 (In English)
Pereanu, W., Shy, D., Hartenstein, V. (2005) Morphogenesis and proliferation of the larval brain glia in Drosophila. Developmental Biology, vol. 283, no. 1, pp. 191–203. PMID: 15907832. DOI: 10.1016/j.ydbio.2005.04.024 (In English)
Pereanu, W., Spindler, S., Cruz, L., Hartenstein, V. (2007) Tracheal development in the Drosophila brain is constrained by glial cells. Developmental Biology, vol. 302, no. 1, pp. 169–180. PMID: 17046740. DOI: 10.1016/j.ydbio.2006.09.022 (In English)
Petley-Ragan, L. M., Ardiel, E. L., Rankin, C. H., Auld, V. J. (2016) Accumulation of laminin monomers in Drosophila glia leads to glial endoplasmic reticulum stress and disrupted larval locomotion. The Journal of Neuroscience, vol. 36, no. 4, pp. 1151–1164. PMID: 26818504. DOI: 10.1523/JNEUROSCI.1797-15.2016 (In English)
Schmid, A., Chiba, A., Doe, C. Q. (1999) Clonal analysis of Drosophila embryonic neuroblasts: Neural cell types, axon projections and muscle targets. Development, vol. 126, no. 21, pp. 4653–4689. PMID: 10518486. (In English)
Schwabe, T., Bainton, R. J., Fetter, R. D. et al. (2005) GPCR signaling is required for blood-brain barrier formation in Drosophila. Cell, vol. 123, no. 1, pp. 133–144. PMID: 16213218. DOI: 10.1016/j.cell.2005.08.037 (In English)
Sepp, K. J., Schulte, J., Auld, V. J. (2001) Peripheral glia direct axon guidance across the CNS/PNS transition zone. Developmental Biology, vol. 238, no. 1, pp. 47–63. PMID: 11783993. DOI: 10.1006/dbio.2001.041 (In English)
Skeath, J. B., Wilson, B. A., Romero, S. E. et al. (2017) The extracellular metalloprotease AdamTS-A anchors neural lineages in place within and preserves the architecture of the central nervous system. Development, vol. 144, no. 17, pp. 3102–3113. PMID: 28760813. DOI: 10.1242/dev.145854 (In English)
Sousa-Nunes, R., Yee, L. L., Gould, A. P. (2011) Fat cells reactivate quiescent neuroblasts via TOR and glial insulin relays in Drosophila. Nature, vol. 471, no. 7339, pp. 508–512. PMID: 21346761. DOI: 10.1038/nature09867 (In English)
Speder, P., Brand, A. H. (2014) Gap junction proteins in the blood-brain barrier control nutrient-dependent reactivation of Drosophila neural stem cells. Developmental Cell, vol. 30, no. 3, pp. 309–321. PMID: 25065772. DOI: 10. 1016/j.devcel.2014.05.0219867 (In English)
Speder, P., Brand, A. H. (2018) Systemic and local cues drive neural stem cell niche remodelling during neurogenesis in Drosophila. eLife, vol. 7, article e30413. PMID: 29299997. DOI: 10.7554/eLife.30413 (In English)
Spindler, S. R., Ortiz, I., Fung, S. et al. (2009) Drosophila cortex and neuropile glia influence secondary axon tract growth, pathfinding, and fasciculation in the developing larval brain. Developmental Biology, vol. 334, no. 2, pp. 355–368. PMID: 19646433. DOI: 10.1016/j.ydbio.2009.07.035 (In English)
Stacey, S. M., Muraro, N. I., Peco, E. et al. (2010) Drosophila glial glutamate transporter Eaat1 is regulated by fringemediated notch signaling and is essential for larval locomotion. The Journal of Neuroscience, vol. 30, no. 43, pp. 14446–14457. PMID: 20980602. DOI: 10.1523/JNEUROSCI.1021-10.2010 (In English)
Stork, T., Bernardos, R., Freeman, M. R. (2012) Analysis of glial cell development and function in Drosophila. Cold Spring Harbor Protocols, vol. 2012, no. 1, pp. 1–17. PMID: 22194269. DOI: 10.1101/pdb.top067587 (In English)
Stork, T., Engelen, D., Krudewig, A. et al. (2008) Organization and function of the blood-brain barrier in Drosophila. The Journal of Neuroscience, vol. 28, no. 3, pp. 587–597. PMID: 18199760. DOI: 10.1523/JNEUROSCI.4367-07.2008 (In English)
Stork, T., Sheehan, A., Tasdemir-Yilmaz, O. E., Freeman, M. R. (2014) Neuron-glia interactions through the Heartless FGF receptor signaling pathway mediate morphogenesis of Drosophila astrocytes. Neuron, vol. 83, no. 2, pp. 388–403. PMID: 25033182. DOI: 10.1016/j.neuron.2014.06.026 (In English)
Subramanian, A., Siefert, M., Banerjee, S. et al. (2017) Remodeling of peripheral nerve ensheathment during the larval-to-adult transition in Drosophila. Developmental Neurobiology, vol. 77, no. 10, pp. 1144–1160. PMID: 28388016. DOI: 10.1002/dneu.22502 (In English)
Tasdemir-Yilmaz, O. E., Freeman, M. R. (2014) Astrocytes engage unique molecular programs to engulf pruned neuronal debris from distinct subsets of neurons. Genes & Development, vol. 28, no. 1, pp. 20–33. PMID: 24361692. DOI: 10.1101/gad.229518.113 (In English)
Tavares, L., Pereira, E., Correia, A. et al. (2015) Drosophila PS2 and PS3 integrins play distinct roles in retinal photoreceptors-glia interactions. Glia, vol. 63, no. 7, pp. 1155–1165. DOI: 10.1002/glia.22806 (In English)
Unhavaithaya, Y., Orr-Weaver, T. L. (2012) Polyploidization of glia in neural development links tissue growth to blood-brain barrier integrity. Genes & Development, vol. 26, no. 1, pp. 31–36. PMID: 22215808. DOI: 10.1101/gad.177436.111 (In English)
Vasile, F., Dossi, E., Rouach, N. (2017) Human astrocytes: Structure and functions in the healthy brain. Brain Structure & Function, vol. 222, no. 5, pp. 2017–2029. PMID: 28280934. DOI: 10.1007/s00429-017-1383-5 (In English)
Volkenhoff, A., Weiler, A., Letzel, M. et al. (2015) Glial glycolysis is essential for neuronal survival in Drosophila. Cell Metabolism, vol. 22, no. 3, pp. 437–447. PMID: 26235423. DOI: 10.1016/j.cmet.2015.07.006 (In English)
Watts, R. J., Schuldiner, O., Perrino, J. et al. (2004) Glia engulf degenerating axons during developmental axon pruning. Current Biology, vol. 14, no. 8, pp. 678–684. PMID: 15084282. DOI: 10.1016/j.cub.2004.03.035 (In English)
Xiong, W. C., Montell, C. (1995) Defective glia induce neuronal apoptosis in the repo visual system of Drosophila. Neuron, vol. 14, no. 3, pp. 581–590. PMID: 7695904. DOI: 10.1016/0896-6273(95)90314-3 (In English)
Yildirim, K., Petri, J., Kottmeier, R., Klambt, C. (2019) Drosophila glia: Few cell types and many conserved functions. Glia, vol. 67, no. 1, pp. 5–26. PMID: 30443934. DOI: 10.1002/glia.23459 (In English)
Zavarzin, A. A.; Stroeva, O. E. (ed.). (2000) Sravnitel’naya gistologiya [Comparative histology]. Saint Petersburg: Saint Petersburg University Publ., 517 p. (In Russian)
Zhang, S. L., Yue, Z., Arnold, D. M. et al. (2018) A circadian clock in the blood-brain barrier regulates xenobiotic efflux. Cell, vol. 173, no. 1, pp. 130–139. PMID: 29526461. DOI: 10.1016/j.cell.2018.02.017 (In English)
Zhang, Y., Chen, K., Sloan, S. A. et al. (2014) An RNA-sequencing transcriptome and splicing database of glia, neurons, and vascular cells of the cerebral cortex. The Journal of Neuroscience, vol. 34, no. 36, pp. 11929–11947. PMID: 25186741. DOI: 10.1523/JNEUROSCI.1860-14.2014 (In English)
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