The astrocyte network in the ventral nerve cord neuropil of the Drosophila third-instar larva.
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glial cells
neuron-glia interaction
Journal
The Journal of comparative neurology
ISSN: 1096-9861
Titre abrégé: J Comp Neurol
Pays: United States
ID NLM: 0406041
Informations de publication
Date de publication:
07 2020
07 2020
Historique:
received:
28
05
2019
revised:
19
12
2019
accepted:
20
12
2019
pubmed:
8
1
2020
medline:
3
11
2021
entrez:
8
1
2020
Statut:
ppublish
Résumé
Understanding neuronal function at the local and circuit level requires understanding astrocyte function. We have provided a detailed analysis of astrocyte morphology and territory in the Drosophila third-instar ventral nerve cord where there already exists considerable understanding of the neuronal network. Astrocyte shape varies more than previously reported; many have bilaterally symmetrical partners, many have a high percentage of their arborization in adjacent segments, and many have branches that follow structural features. Taken together, our data are consistent with, but not fully explained by, a model of a developmental growth process dominated by competitive or repulsive interactions between astrocytes. Our data suggest that the model should also include cell-autonomous aspects, as well as the use of structural features for growth. Variation in location of arborization territory for identified astrocytes was great enough that a standardized scheme of neuropil division among the six astrocytes that populate each hemi-segment is not possible at the third instar. The arborizations of the astrocytes can extend across neuronal functional domains. The ventral astrocyte in particular, whose territory can extend well into the proprioceptive region of the neuropil, has no obvious branching pattern that correlates with domains of particular sensory modalities, suggesting that the astrocyte would respond to neuronal activity in any of the sensory modalities, perhaps integrating across them. This study sets the stage for future studies that will generate a robust, functionally oriented connectome that includes both partners in neuronal circuits-the neurons and the glial cells, providing the foundation necessary for studies to elucidate neuron-glia interactions in this neuropil.
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Research Support, U.S. Gov't, Non-P.H.S.
Langues
eng
Sous-ensembles de citation
IM
Pagination
1683-1703Informations de copyright
© 2020 Wiley Periodicals, Inc.
Références
Allen, N. J., Bennett, M. L., Foo, L. C., Wang, G. X., Chakraborty, C., Smith, S. J., & Barres, B. A. (2012). Astrocyte glicans 4 and 6 promote formation of excitatory synapses via GluA1 AMPA receptors. Nature, 486, 410-414. https://doi.org/10.1038/nature11059
Asada, A., Ujita, S., Nakayama, R., Oba, S., Ishii, S., Matsuki, N., & Ikegaya, Y. (2015). Subtle modulation of ongoing calcium dynamics in astrocytic microdomains by sensory inputs. Physiological Reports, 3, e12454. https://doi.org/10.14814/phy2.12454
Bazargani, N., & Attwell, D. (2016). Astrocyte calcium signaling: The third wave. Nature Neuroscience, 19, 182-189. https://doi.org/10.1038/nn.4201
Boyan, G. S., & Ball, E. E. (1993). The grasshopper, Drosophila and neuronal homology (advantages of the insect nervous system for the neuroscientist). Progress in Neurobiology, 41, 657-682.
Burgos, A., Honjo, K., Ohyama, T., Qian, C. S., Shin, G. J., Gohl, D. M., … Grueber, W. B. (2018). Nociceptive interneurons control modular motor pathways to promote escape behavior in Drosophila. eLife, 7, e26016. https://doi.org/10.7554/eLife.26016
Bushong, E. A., Martone, M. E., & Ellisman, M. H. (2004). Maturation of astrocyte morphology and the establishment of astrocyte domains during postnatal hippocampal development. International Journal of Developmental Neuroscience, 22, 73-86. https://doi.org/10.1016/j.ijdevneu.2003.12.008
Bushong, E. A., Martone, M. E., Jones, Y. Z., & Ellisman, M. H. (2002). Protoplasmic astrocytes in CA1 stratum radiatum occupy separate anatomical domains. The Journal of Neuroscience, 22, 183-192.
Campos-Ortéga, J. A., & Hartenstein, V. (1997). The embryonic development of Drosophila melanogaster. Berlin, Germany: Springer.
Choi, J. C., Park, D., & Griffith, L. C. (2004). Electrophysiological and morphological characterization of identified motor neurons in the Drosophila third instar larva central nervous system. Journal of Neurophysiology, 91, 2353-2365. https://doi.org/10.1152/jn.01115.2003
Chung, W.-S., Clarke, L. E., Wang, G. X., Stafford, B. K., Sher, A., Chakraborty, C., … Barres, B. A. (2013). Astrocytes mediate synapse elimination through MEGF10 and MERTK pathways. Nature, 504, 394-400. https://doi.org/10.1038/nature12776
Clark, M. Q., McCumsey, S. J., Lopez-Darwin, S., Heckscher, E. S., & Doe, C. Q. (2016). Functional genetic screen to identify interneurons governing behaviorally distinct aspects of Drosophila larval motor programs. G3: Genes, Genomes, Genetics (Bethesda), 6, 2023-2031. https://doi.org/10.1534/g3.116.028472
Clark, M. Q., Zarin, A. A., Carreira-Rosario, A., & Doe, C. Q. (2018). Neural circuits driving larval locomotion in Drosophila. Neural Development, 13, 6. https://doi.org/10.1186/s13064-018-0103-z
Clarke, L. E., & Barres, B. A. (2013). Emerging roles of astrocytes in neural circuit development. Nature Reviews. Neuroscience, 14, 311-321. https://doi.org/10.1038/nrn3484
Corty, M. M., & Freeman, M. R. (2013). Architects in neural circuit design: Glia control neuron numbers and connectivity. The Journal of Cell Biology, 203, 395-405. https://doi.org/10.1083/jcb.201306099
Distler, C., Weigel, H., & Hoffman, K. P. (1993). Glia cells of the monkey retina. I. Astrocytes. The Journal of Comparative Neurology, 333, 134-147. https://doi.org/10.1002/cne.903330111
Doherty, J., Logan, M. A., Taşdemir, O. E., & Freeman, M. R. (2009). Ensheathing glia function as phagocytes in the adult Drosophila brain. The Journal of Neuroscience, 29, 4768-4781. https://doi.org/10.1523/JNEUROSCI.5951-08.2009
Enriquez, J., Rio, L. Q., Blazeski, R., Bellemin, S., Godemont, P., Mason, C., & Mann, R. S. (2018). Differing strategies despite shared lineages of motor neurons and glia to achieve robust development of an adult neuropil in Drosophila. Neuron, 97, 538-554.e5. https://doi.org/10.1016/j.neuron.2018.01.007
Eroglu, C., & Barres, B. A. (2010). Regulation of synaptic connectivity by glia. Nature, 468, 223-231. https://doi.org/10.1038/nature09612
Eroglu, C., Allen, N. J., Susman, M. W., O'Rourke, N. A., Park, C. Y., Ozkan, E., … Barres, B. A. (2009). Gabapentin receptor alpha2delta-1 is a neuronal thrombospondin receptor responsible for excitatory CNS synaptogenesis. Cell, 139, 380-392. https://doi.org/10.1016/j.cell.2009.09.025
Feng, Y., Ueda, A., & Wu, C. F. (2004). A modified minimal hemolymph-like solution, HL3.1, for physiological recordings at the neuromuscular junctions of normal and mutant Drosophila larvae. J Neurogenetics. 18(2), 377-402. PMID: 15763995
Fields, R. D., Woo, D. H., & Basser, P. J. (2015). Glial regulation of the neuronal connectome through local and long-distant communication. Neuron, 86, 374-386. https://doi.org/10.1016/j.neuron.2015.01.014
Fishiki, A., Zwart, M. F., Kohsaka, H., Fetter, R. D., Cardona, A., & Nose, A. (2016). A circuit mechanism of the propagation of waves of muscle contraction in Drosophila. eLife, 5, e13253. https://doi.org/10.7554/eLife.13253.001
Freeman, M. R. (2015). Drosophila central nervous system glia. Cold Spring Harbor Perspectives in Biology, 7(11). pii: a020552. https://doi.org/10.1101/cshperspect.a020552
Gerhard, S., Andrade, I., Fetter, R. D., Cardona, A., & Schneider-Mizell, C. M. (2017). Conserved neural circuit structure across Drosophila larval development revealed by comparative connectomics. eLife, 6, e29089. https://doi.org/10.7554/elife.29089
Giaume, C., & Liu, X. (2012). From a glial syncytium to a more restricted and specific glial networking. Journal of Physiology, Paris, 106, 34-39. https://doi.org/10.1016/j.physparis.2011.09.001
Goodman, C. S., Bastiani, M. J., Doe, C. Q., & Dulac, S. (1985). Growth cone guidance and cell recognition in insect embryos. Developmental Biology (New York, NY), 3, 283-300.
Gordleeva, S. Y., Ermolaeva, A. V., Kastalskiy, I. A., & Kazantsev, V. B. (2019). Astrocyte as spatiotemporal integrating detector of neuronal activity. Frontiers in Physiology, 10, 294. https://doi.org/10.3389/fphys.2019.00294
Grenningloh, G., Rehm, E. J., & Goodman, C. S. (1991). Genetic analysis of growth cone guidance in Drosophila: Fasciclin II functions as a neuronal recognition molecule. Cell, 67, 45-57.
Grosjean, Y., Grillet, M., Augustin, H., Ferveur, J.-F., & Featherstone, D. E. (2008). A glial amino-acid transporter controls synaptic strength and courtship in Drosophila. Nature Neuroscience, 11, 54-61. https://doi.org/10.1038/nn2019
Grueber, W. B., Ye, B., Yang, C.-H., Younger, S., Borden, K., Jan, L. Y., & Jan, Y. N. (2007). Projections of Drosophila multidendritic neurons in the central nervous system: Links with peripheral dendrite morphology. Development, 134, 55-64. https://doi.org/10.1242/dev.02666
Halassa, M. H., Fellin, T., Takano, H., Dong, J.-H., & Haydon, P. G. (2007). Synaptic islands defined by the territory of a single astrocyte. The Journal of Neuroscience, 27, 6473-6477. https://doi.org/10.1523/JNEUROSCI.1419-07.2007
Harris, K. M., Spacek, J., Bell, M. E., Parker, P. H., Lindsey, L. F., Baden, A. D., Vogelstein, J. T., Burns, R. (2015). A resource from 3D electron microscopy of hippocampal neuropil for user training and tool development. Scientific Data, 2, 150046.
Hartenstein, V. (2011). Morphological diversity and development of glia in Drosophila. Glia, 59, 1237-1252. https://doi.org/10.1002/glia.21162
Hartenstein, V., Spindler, S., Pereanu, W., & Fung, S. (2008). The development of the Drosophila larval brain. Advances in Experimental Medicine and Biology, 628, 1-31. https://doi.org/10.1007/978-0-387-78261-4
Heckscher, E. S., Zarin, A. A., Faumont, S., Clark, M. Q., Manning, L., Fushiki, A., … Doe, C. Q. (2015). Even-skipped(+) interneurons are core components of a sensorimotor circuit that maintains left-right symmetric muscle contraction amplitude. Neuron, 88, 314-329. https://doi.org/10.1016/j.neuron.2015.09.009
Hildago, A., & Brand, A. H. (1997). Targeted neuronal ablation: The role of pioneer neurons in guidance and fasciculation in the CNS of Drosophila. Development, 124, 3253-3262.
Ito, K., Awano, W., Suzuki, K., Hiromi, Y., & Yamamoto, D. (1997). The Drosophila mushroom body is a quadruple structure of clonal units each of which contains a virtually identical set of neurons and glial cells. Development, 124, 761-771.
Kanemaru, K., Sekiya, H., Xu, M., Satoh, K., Kitajima, N., Yoshida, K., et al. (2014). In vivo visualization of subtle, transient, and local activity of astrocytes using an ultrasensitive Ca2+ indicator. Cell Reports, 8, 311-318. https://doi.org/10.1016/j.celrep.2014.05.056
Keshishian, H., & Chiba, A. (1993). Neuromuscular development in Drosophila: Insights from single neurons and single genes. Trends in Neurosciences, 16, 278-283.
Kim, M. D., Wen, Y., & Jan, Y.-N. (2009). Patterning and organization of motor neuron dendrites in the Drosophila larva. Developmental Biology, 336, 213-221. https://doi.org/10.1016/j.ydbio.2009.09.041
Kohsaka, H., Guertin, P. A., & Nose, A. (2017). Neural circuits underlying fly larval locomotion. Current Pharmaceutical Design, 23, 1722-1733. https://doi.org/10.2174/1381612822666161208120835
Kohsaka, H., Takasu, E., Morimoto, T., & Nose, A. (2014). A group of segmental premotor interneurons regulates the speed of axial locomotion in Drosophila larvae. Current Biology, 24, 2632-2642. https://doi.org/10.1016/j.cub.2014.09.026
Kremer, M. C., Jung, C., Batelli, S., Rubin, G. M., & Gaul, U. (2017). The glia of the adult Drosophila nervous system. Glia, 65, 606-638. https://doi.org/10.1002/glia.23115
Landgraf, M., Jeffrey, V., Fujioka, J. B., Jaynes, J. B., & Bate, M. (2003). Embryonic origin of a motor system: Motor dendrites form a myotopic map in Drosophila. PLoS Biology, 1, e41. https://doi.org/10.1371/journal.pbio.0000041
Landgraf, M., Sánchez-Soriano, N., Technau, G. M., Urban, J., & Prokop, A. (2003). Charting the Drosophila neuropile: A strategy for the standardised characterization of genetically amenable neurites. Developmental Biology, 260, 207-225. https://doi.org/10.1016/S0012-1606(03)00215-X
Liu, H., Zhou, B., Yan, W., Lei, Z., Zhao, X., Zhang, K., & Guo, A. (2014). Astrocyte-like glial cells physiologically regulate olfactory processing through the modification of ORN-PN synaptic strength in Drosophila. The European Journal of Neuroscience, 40, 2744-2754. https://doi.org/10.1111/ejn.12646
Lopez-Hidalgo, N., & Schummers, J. (2014). Cortical maps: A role for astrocytes? Current Opinion in Neurobiology, 24, 176-189. https://doi.org/10.1016/j.conb.2013.11.001
Ma, Z., Stork, T., Bergles, D. E., & Freeman, M. R. (2016). Neuromodulators signal through astrocytes to alter neural circuit activity and behavior. Nature, 539, 428-432. https://doi.org/10.1038/nature20145
MacDonald, J. M., Beach, M. G., Porpiglia, E., Sheehan, A. E., Watts, R. J., & Freeman, M. R. (2006). The Drosophila cell corpse engulfment receptor Draper mediates glial clearance of severed axons. Neuron, 50, 869-881. https://doi.org/10.1016/j.neuron.2006.04.028
MacNamee, S. E., Liu, K. E., Gerhard, S., Tran, C. T., Fetter, R. D., Cardona, A., Tolbert, L. P., Oland, L. A. (2016). Astrocyte glutamate transport regulates a Drosophila CNS synapse that lacks astrocyte ensheathment. The Journal of Comparative Neurology, 524, 1979-1998. https://doi.org/10.1002/cne.24016
Mathew, D., Popescu, A., & Budnik, V. (2003). Drosophila amphiphysin functions during synaptic Fasciclin II membrane cycling. The Journal of Neuroscience, 23, 10710-10716.
Merritt, D. J., & Whitington, P. M. (1995). Central projections of sensory neurons in the Drosophila embryo correlate with sensory modality, some position, and proneural gene function. The Journal of Neuroscience, 15, 1755-1976.
Miller, R. H., & Raff, M. C. (1984). Fibrous and protoplasmic astrocytes are biochemically and developmentally distinct. The Journal of Neuroscience, 4, 585-592.
Molofsky, A. V., Krencik, R., Ullian, E. M., Tsai, H. H., Deneen, B., Richardson, W. D., Barres, B. A., Rowitch, D. H. (2012). Astrocytes and disease: A neurodevelopmental perspective. Genes & Development, 26, 891-907. https://doi.org/10.1101/gad.188326.112
Murphey, R. K., Poissidente, D., Pollack, G., & Merritt, D. J. (1989). Modality-specific axonal projections in the CNS of the flies Phormia and Drosophila. The Journal of Comparative Neurology, 290, 185-200. https://doi.org/10.1002/cne.902900203
Muthukumar, A. K., Stork, T., & Freeman, M. R. (2014). Activity-dependent regulation of astrocyte GAT levels during synaptogenesis. Nature Neuroscience, 17, 1340-1350. https://doi.org/10.1038/nn.3791
Nern, A., Pfeiffer, B. D., & Rubin, G. M. (2015). Optimized tools for multicolor stochastic labeling reveal diverse stereotyped cell arrangements in the fly visual system. Proceedings of the National Academy of Sciences of the United States of America, 112, e2967-e2976. https://doi.org/10.1073/pnas.1506763112
Ogata, K., & Kosaka, T. (2002). Structural and quantitative analysis of astrocytes in the mouse hippocampus. Neuroscience, 113, 221-233.
Ohyama, T., Schneider-Mizell, C. M., Fetter, R. D., Aleman, J. V., Franconville, R., Rivera-Alba, M., … Zlatic, M. (2015). A multilevel multimodal circuit enhances action selection in Drosophila. Nature, 5120, 633-639. https://doi.org/10.1038/nature14297
Panatier, A., Vallee, J., Haber, M., Murai, K. K., Lacaille, J. C., & Robataille, R. (2011). Astrocytes are endogenous regulators of basal transmission at central synapses. Cell, 146, 785-798. https://doi.org/10.1016/j.cell.2011.07.022
Peco, E., Davla, S., Camp, D., Stacey, S. M., Landgraf, M., & van Meyel, D. J. (2016). Drosophila astrocytes cover specific territories of the CNS neuropil and are instructed to differentiate by Prospero, a key effector of Notch. Development, 143, 1170-1181. https://doi.org/10.1242/dev.133165
Pereanu, W., Shy, D., & Hartenstein, V. (2005). Morphogenesis and proliferation of the larval brain glia in Drosophila. Developmental Biology, 283, 191-203. https://doi.org/10.1016/j.ydbio.2005.04.024
Peters, A., Palay, S. l., & Webster, H. d F. (1976). Fine structure of the nervous system: Neurons and their supporting cells. Oxford, UK: Oxford University Press.
Pflüger, H. J., & Watson, A. H. (1988). Structure and distribution of dorsal unpaired median (DUM) neurons in the abdominal nerve cord of male and female locusts. The Journal of Comparative Neurology, 268, 329-345. https://doi.org/10.1002/cne.902680304
Pflüger, H. J., Braunig, P., & Hustert, R. (1988). The organization of mechanosensory neuropiles in locust thoracic ganglia. Philosophical Transactions of Royal Society of London B, 321, 1-26.
Ramachandran, P. & Budnik, V. (2010) Immunocytochemical staining of Drosophila body wall muscles. Cold Spring Harb Protoc. 2010(8):pdb.prot5470. doi: PMID: 2067937
Richier, B., de Miguel Vijandi, C., Mackensen, S., & Salecker, I. (2017). Lapsyn controls branch extension and positioning of astrocyte-like glia in the Drosophila optic lobe. Nature Communications, 8, 317. https://doi.org/10.1038/s41467-017-00384-z
Rickert, C., Kunz, T., Harris, K.-L., Whitington, P., & Technau, G. M. (2011). Morphological characterization of the entire interneuron population reveals principles of neuromere organization in the ventral nerve cord of Drosophila. The Journal of Neuroscience, 31, 15870-15883. https://doi.org/10.1523/jneurosci.4009-11.2011
Rival, T., Soustelle, L., Cattaert, D., Strambi, C., Iché, M., & Birman, S. (2006). Physiological requirement for the glutamate transporter dEAAT1 at the adult Drosophila neuromuscular junction. Journal of Neurobiology, 66, 1061-1074. https://doi.org/10.1002/neu.20270
Rival, T., Soustelle, L., Strambi, C., Beeson, M.-T., Iché, M., & Birman, S. (2004). Decreasing glutamate buffering capacity triggers oxidative stress and neuropil degeneration in the Drosophila brain. Current Biology, 14, 599-605. https://doi.org/10.1016/j.cub.2004.03.039
Roux, L., Benchenane, K., Rothstein, J. D., Bonvento, G., & Giaume, C. (2011). From the cover: Plasticity of astroglial networks in olfactory glomeruli. Proceedings of the National Academy of Sciences of the United States of America, 108, 18442-18446. https://doi.org/10.1073/pnas.1107386108
Rungta, R. L., Bernier, L. P., Dissing-Olesen, L., Groten, C. J., LeDue, J. M., Ko, R., … MacVicar, B. A. (2016). Ca+2 transients in astrocyte fine processes occur via Ca+2 influx in the adult mouse hippocampus. Glia, 64, 2093-2103. https://doi.org/10.1002/glia.23042
Schneider-Mizell, C. M., Gerhard, S., Longair, M., Kazimiers, T., Li, F., Zwart, M. F., … Cardona, A. (2016). Quantitative neuroanatomy for connectomics in Drosophila. eLife, 5, e12059. https://doi.org/10.7554/eLife.12059
Schrader, S., & Merritt, D. J. (2000). Central projections of Drosophila sensory neurons in the transition from embryo to larva. The Journal of Comparative Neurology, 425, 34-44.
Semyanov, A. (2019). Spatiotemporal pattern of calcium activity in astrocytic network. Cell Calcium, 78, 15-25. https://doi.org/10.1016/j.ceca.2018.12.007
Shigetomi, E., Bushong, E. A., Haustein, M. D., Tong, X., Jackson-Weaver, O., Kracun, S., … Khakh, B. S. (2013). Imaging calcium microdomains within entire astrocyte territories and endfeet with GCaMPs expressed using adeno-associated viruses. The Journal of General Physiology, 141, 633-647. https://doi.org/10.1085/jgp.201210949
Southern, J. A., Young, D. F., Heaney, F., Baumgartner, W., & Randall, R. E. (1991). Identification of an epitope on the P and V proteins of simian virus 5 that distinguishes between two isolates with different biological characteristics. The Journal of General Virology, 72, 1551-1557. https://doi.org/10.1099/0022-1317-72-7-1551
Stacey, S. M., Muraro, N. I., Peco, E., Labbé, A., Thomas, G. B., Baines, R. A., & van Meyel, D. J. (2010). Drosophila glial glutamate transporter Eaat1 is regulated by fringe-mediated notch signaling and is essential for larval locomotion. The Journal of Neuroscience, 30, 14446-14457. https://doi.org/10.1523/JNEUROSCI.1021-10.2010
Stobart, J. L., Ferrari, K. D., Barrett, M. J. P., Stobart, M. J., Looser, Z. J., Saab, A. S., & Weber, B. (2018). Long-term in vivo calcium imaging of astrocytes reveals distinct cellular compartment responses to sensory stimulation. Cerebral Cortex, 28, 184-198. https://doi.org/10.1093/cercor/bhw366
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, 83, 388-403. https://doi.org/10.1016/j.neuron.2014.06.026
Strausfeld, N. J. (1976). Atlas of an insect brain. New York, NY: Springer-Verlag.
Tastekin, I., Khandelwal, A., Tadres, D., Fessner, N. D., Truman, J. W., Zlatic, M., … Louis, M. (2018). Sensorimotor pathway controlling stopping behavior during chemotaxis in the Drosophila melanogaster larva. eLife, 7, e38740. https://doi.org/10.7554/eLife.38740
Tessier, C. R., & Broadie, K. (2009). Activity-dependent modulation of neural circuit synaptic connectivity. Frontiers in Molecular Neuroscience, 2, 8. https://doi.org/10.3389/neuro.02.008.2009
Theodosis, D. T., Poulain, D. A., & Oliet, S. H. R. (2008). Activity-dependent structural and functional plasticity of astrocyte-neuron interactions. Physiological Reviews, 88, 983-1008. https://doi.org/10.1152/physrev.00036.2007
Verkhratsky, A., & Nedergaard, M. (2018). Physiology of astroglia. Physiological Reviews, 98, 239-389. https://doi.org/10.1152/physrev.00042.2016
Viswanathan, S., Williams, M. E., Bloss, E. B., Stasevich, T. J., Speer, C. M., Nern, A., … Looger, L. I. (2015). High-performance probes for light and electron microscopy. Nature Methods, 12, 568-576. https://doi.org/10.1038/nmeth.3365
Vonhoff, F., & Duch, C. (2010). Tiling among stereotyped dendritic branches in an identified Drosophila motoneuron. The Journal of Comparative Neurology, 518, 2169-2185. https://doi.org/10.1002/cne.22380
Wagh, D. A., Rasse, T. M., Asan, E., Hofbauer, A., Schwenkert, I., Dürrbeck, H., … Buchner, E. (2006). Bruchpilot, a protein with homology to ELKS/DAST, is required for structural integrity and function of synaptic active zones in Drosophila. Neuron, 49, 833-844. https://doi.org/10.1016/j.neuron.2006.02.008
Worrell, J. W., & Levine, R. B. (2008). Characterization of voltage-dependent Ca2+ currents in identified Drosophila motoneurons in situ. Neurophysiology, 100, 868-878. https://doi.org/10.1152/jn.90464.2008
Yildirim, K., Petri, J., Kottmeier, R., & Klämbt, C. (2019). Drosophila glia: Few cell types and many conserved functions. Glia, 67, 5-26. https://doi.org/10.1002/glia.23459
Zhang, Y. V., Ormerod, K. G., & Littleton, J. T. (2017). Astrocyte Ca2+ influx negatively regulates neuronal activity. eNeuro, 4, e0340. https://doi.org/10.1523/eneuro.0340-16.2017
Zlatic, M., Landgraf, M., & Bate, M. (2003). Genetic specification of axonal arbors: Atonal regulates robo3 to position terminal branches in the Drosophila nervous system. Neuron, 37, 41-51.
Zlatic, M., Li, F., Strigini, M., Grueber, W., & Bate, M. (2009). Positional cues in the Drosophila nerve cord: Semaphorins pattern the dorso-ventral axis. PLoS Biology, 7, e1000135. https://doi.org/10.1371/journal.pbio.1000135