Postembryonic lineages of the Drosophila brain: I. Development of the lineage-associated fiber tracts
Open accessAbstract
Neurons of the Drosophila central brain fall into approximately 100 paired groups, termed lineages. Each lineage is derived from a single asymmetrically-dividing neuroblast. Embryonic neuroblasts produce 1,500 primary neurons (per hemisphere) that make up the larval CNS followed by a second mitotic period in the larva that generates approximately 10,000 secondary, adult-specific neurons. Clonal analyses based on previous works using lineage-specific Gal4 drivers have established that such lineages form highly invariant morphological units. All neurons of a lineage project as one or a few axon tracts (secondary axon tracts, SATs) with characteristic trajectories, thereby representing unique hallmarks. In the neuropil, SATs assemble into larger fiber bundles (fascicles) which interconnect different neuropil compartments. We have analyzed the SATs and fascicles formed by lineages during larval, pupal, and adult stages using antibodies against membrane molecules (Neurotactin/Neuroglian) and synaptic proteins (Bruchpilot/N-Cadherin). The use of these markers allows one to identify fiber bundles of the adult brain and associate them with SATs and fascicles of the larval brain. This work lays the foundation for assigning the lineage identity of GFP-labeled MARCM clones on the basis of their close association with specific SATs and neuropil fascicles, as described in the accompanying paper (Wong et al., 2013. Postembryonic lineages of the Drosophila brain: II. Identification of lineage projection patterns based on MARCM clones. Submitted.).
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The majority of hemilineage tracts visible in the EM dataset occur in pairs or small groups (3-5).
“the majority of hemilineage tracts visible in the EM dataset occur in pairs or small groups (3–5).”
From Whole-brain annotation and multi-connectome cell typing of Drosophila (2024) · cites this paper as [31]
The Discussion section, “Hemilineages and sub-lineages form separate tracts” (page unavailable), says that two hemilineage tracts from one lineage enter close together and remain close in the majority of lineages possessing two hemilineages. It does not establish that a majority of tracts visible in an EM dataset occur in pairs or groups of 3–5; the Methods describe confocal microscopy instead. (LLM, conf=0.83)
Experimental — accuracy not yet measuredFrom light-level data that labels a whole lineage and all of its hemilineages together, it is occasionally difficult to assess whether there is a single hemilineage or multiple if the cell body clusters do not separate sufficiently.
“From light-level data that labels a whole lineage and all of its hemilineages together,139,199,200,201 it is occasionally difficult to assess whether there is a single hemilineage or multiple, if the cell body clusters happen to not separate sufficiently.”
From Neurotransmitter classification from electron microscopy images at synaptic sites in Drosophila melanogaster (2024) · cites this paper as [199]
Our lineage-associated tracts have been mapped by light microscopy and assigned to named lineage clones.
“Our lineage-associated tracts have been mapped by light microscopy and assigned to named lineage clones.139,199,200,201,202”
From Neurotransmitter classification from electron microscopy images at synaptic sites in Drosophila melanogaster (2024) · cites this paper as [199]
The following lineages are new to the Hartenstein nomenclature: SLPal5/BLAd5, SLPav3/BLVa2a, LHl3/BLVa2b, SLPpl3/BLVa2c, PBp1/CM6, SLPpl2/CP6, SMPpd2/DPLc6, PSp1/DPMl2 and LHp3/CP5.
“New to ref. 31 (Hartenstein nomenclature) are: SLPal5/BLAd5, SLPav3/BLVa2a, LHl3/BLVa2b, SLPpl3/BLVa2c, PBp1/CM6, SLPpl2/CP6, SMPpd2/DPLc6, PSp1/DPMl2 and LHp3/CP5”
From Whole-brain annotation and multi-connectome cell typing of Drosophila (2024) · cites this paper as [31]
Previous literature expected a total of around 119 lineages in the central brain, including the gnathal ganglia (GNG).
“From previous literature, we expected a total of around 119 lineages in the central brain, including the gnathal ganglia (GNG)31–34,84.”
From Whole-brain annotation and multi-connectome cell typing of Drosophila (2024) · cites this paper as [31]
The Introduction says previous studies mapped central-brain lineages, and the Results classify individual lineages, but neither passage gives an expected total of around 119 including the gnathal ganglia. Searches for “119” and for the gnathal or subesophageal ganglion did not find that estimate in the paper’s body text. The available passages have no page numbers. (LLM, conf=0.70)
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Self-citationLineage-specific cell death in postembryonic brain development ofDrosophila
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Self-citationempty spiraclesis required for the development of olfactory projection neuron circuitry inDrosophila
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Neuroblast lineage-specific origin of the neurons of the Drosophila larval olfactory system
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Bazooka mediates secondary axon morphology in Drosophila brain lineages
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Self-citationDevelopment of neural lineages derived from the sine oculis positive eye field of Drosophila
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Modification of the Bodian technique applied to insect nerves.
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Flagged first, then by citations
3 of the 121 references couldn’t be matched to a known paper.
Research works printed but not linked: 4
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Cited by
Sorted by citations
Whole-brain annotation and multi-connectome cell typing of Drosophila
Schlegel, P., Yin, Y., Bates, A. S., Dorkenwald, S., Eichler, K., Brooks, P., Han, D. S., Gkantia, M., dos Santos, M., Munnelly, E. J., et al. (2024) · Nature · doi:10.1038/s41586-024-07686-5 · Cited by 413 · see citing works
“31 (Hartenstein nomenclature) are: SLPal5/BLAd5, SLPav3/BLVa2a, LHl3/BLVa2b, SLPpl3/BLVa2c, PBp1/ CM6, SLPpl2/CP6, SMPpd2/DPLc6, PSp1/DPMl2 and LHp3/CP5—we named these units according to the Hartenstein nomenclature naming scheme.”
BackgroundMethodInfluentialA genome-wide resource for the analysis of protein localisation in Drosophila
Sarov, M., Barz, C., Jambor, H. K., Hein, M. Y., Schmied, C., Suchold, D., Stender, B., Janosch, S., Vinay Vikas, K. J., Krishnan, R., et al. (2016) · eLife · doi:10.7554/elife.12068 · Cited by 361 · see citing works
Self-citationEckstein, N., Bates, A. S., Champion, A., Du, M., Yin, Y., Schlegel, P., Lu, A. K.-Y., Rymer, T., Finley-May, S., Paterson, T., et al. (2024) · Cell · doi:10.1016/j.cell.2024.03.016 · Cited by 233 · see citing works
“Cell body fiber tracts for identified hemilineages had previously been identified using TrakEM2 (Cardona et al., 2012) in a light-level atlas for a D. melanogaster brain, stained with an antibody against neurotactin (BP104) (Lovick et al., 2013).”
InfluentialSelf-citationThe Drosophila blood-brain barrier: development and function of a glial endothelium
Limmer, S., Weiler, A., Volkenhoff, A., Babatz, F., & Klämbt, C. (2014) · Frontiers in Neuroscience · doi:10.3389/fnins.2014.00365 · Cited by 214 · see citing works
Information flow, cell types and stereotypy in a full olfactory connectome
Schlegel, P., Bates, A. S., Stürner, T., Jagannathan, S. R., Drummond, N., Hsu, J., Serratosa Capdevila, L., Javier, A., Marin, E. C., Barth-Maron, A., et al. (2021) · eLife · doi:10.7554/elife.66018 · Cited by 178 · see citing works
Complete Connectomic Reconstruction of Olfactory Projection Neurons in the Fly Brain
Bates, A. S., Schlegel, P., Roberts, R. J. V., Drummond, N., Tamimi, I. F., Turnbull, R., Zhao, X., Marin, E. C., Popovici, P. D., Dhawan, S., et al. (2020) · Current Biology · doi:10.1016/j.cub.2020.06.042 · Cited by 199 · see citing works
Omoto, J. J., Keleş, M. F., Nguyen, B.-C. M., Bolanos, C., Lovick, J. K., Frye, M. A., & Hartenstein, V. (2017) · Current Biology · doi:10.1016/j.cub.2017.02.063 · Cited by 137 · see citing works
Self-citationEckstein, N., Bates, A. S., Champion, A., Du, M., Yin, Y., Schlegel, P., Lu, A. K.-Y., Rymer, T., Finley-May, S., Paterson, T., et al. (2020) · doi:10.1101/2020.06.12.148775 · Cited by 115 · see citing works
Self-citationSchlegel, P., Yin, Y., Bates, A. S., Dorkenwald, S., Eichler, K., Brooks, P., Han, D. S., Gkantia, M., dos Santos, M., Munnelly, E. J., et al. (2023) · doi:10.1101/2023.06.27.546055 · Cited by 102 · see citing works
Self-citationNériec, N., & Desplan, C. (2016) · Current topics in developmental biology/Current Topics in Developmental Biology · doi:10.1016/bs.ctdb.2015.11.032 · Cited by 101 · see citing works
Doll, C. A., & Broadie, K. S. (2014) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2014.00030 · Cited by 81 · see citing works
Neuronal constituents and putative interactions within the Drosophila Ellipsoid Body Neuropil
Omoto, J. J., Nguyen, B.-C. M., Kandimalla, P., Lovick, J. K., Donlea, J. M., & Hartenstein, V. (2018) · Frontiers in Neural Circuits · doi:10.3389/fncir.2018.00103 · Cited by 72 · see citing works
Self-citationInsect models of central nervous system energy metabolism and its links to behavior
Rittschof, C. C., & Schirmeier, S. (2017) · Glia · doi:10.1002/glia.23235 · Cited by 67 · see citing works
Control of neural stem cell self-renewal and differentiation in Drosophila
Kang, K. H., & Reichert, H. (2014) · Cell and Tissue Research · doi:10.1007/s00441-014-1914-9 · Cited by 59 · see citing works
Developmental analysis of the dopamine‐containing neurons of the Drosophila brain
Hartenstein, V., Cruz, L., Lovick, J. K., & Guo, M. (2016) · The Journal of Comparative Neurology · doi:10.1002/cne.24069 · Cited by 55 · see citing works
Self-citationWong, D. C., Lovick, J. K., Ngo, K. T., Borisuthirattana, W., Omoto, J. J., & Hartenstein, V. (2013) · Developmental Biology · doi:10.1016/j.ydbio.2013.07.009 · Cited by 46 · see citing works
Self-citationNgo, K., Andrade, I. V., & Hartenstein, V. (2017) · Developmental Biology · doi:10.1016/j.ydbio.2017.05.008 · Cited by 43 · see citing works
Self-citationFarnworth, M. S., Eckermann, K. N., & Bucher, G. (2020) · PLoS Biology · doi:10.1371/journal.pbio.3000881 · Cited by 45 · see citing works
Kendroud, S., Bohra, A. A., Kuert, P. A., Nguyen, B., Guillermin, O., Sprecher, S. G., Reichert, H., VijayRaghavan, K., & Hartenstein, V. (2018) · Journal of Comparative Neurology · doi:10.1002/cne.24316 · Cited by 39 · see citing works
Self-citationKuert, P. A., Hartenstein, V., Bello, B. C., Lovick, J. K., & Reichert, H. (2014) · Developmental Biology · doi:10.1016/j.ydbio.2014.03.021 · Cited by 38 · see citing works
Self-citationShepherd, D., Harris, R. M., Williams, D. W., & Truman, J. W. (2016) · The Journal of Comparative Neurology · doi:10.1002/cne.23988 · Cited by 38 · see citing works
Kandimalla, P., Omoto, J. J., Hong, E. J., & Hartenstein, V. (2023) · Journal of Comparative Physiology A · doi:10.1007/s00359-023-01616-y · Cited by 38 · see citing works
Self-citationHartenstein, V., Omoto, J. J., Ngo, K. T., Wong, D., Kuert, P. A., Reichert, H., Lovick, J. K., & Younossi‐Hartenstein, A. (2018) · Journal of Comparative Neurology · doi:10.1002/cne.24287 · Cited by 31 · see citing works
Self-citationA conserved plan for wiring up the fan-shaped body in the grasshopper and Drosophila
Boyan, G., Liu, Y., Khalsa, S. K., & Hartenstein, V. (2017) · Development Genes and Evolution · doi:10.1007/s00427-017-0587-2 · Cited by 31 · see citing works
Self-citationA map of brain neuropils and fiber systems in the ant Cardiocondyla obscurior
Bressan, J. M. A., Benz, M., Oettler, J., Heinze, J., Hartenstein, V., & Sprecher, S. G. (2015) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2014.00166 · Cited by 28 · see citing works
Self-citationLineage-associated tracts defining the anatomy of the Drosophila first instar larval brain
Hartenstein, V., Younossi‐Hartenstein, A., Lovick, J. K., Kong, A., Omoto, J. J., Ngo, K., & Viktorin, G. (2015) · Developmental Biology · doi:10.1016/j.ydbio.2015.06.021 · Cited by 25 · see citing works
Self-citationAxon ensheathment and metabolic supply by glial cells in Drosophila
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Shaw, R. E., Kottler, B., Ludlow, Z. N., Buhl, E., Kim, D., da Silva, S. M., Miedzik, A. A., Coum, A., Hodge, J. J. L., Hirth, F., et al. (2018) · The EMBO Journal · doi:10.15252/embj.201798163 · Cited by 23 · see citing works
Farnworth, M. S., Bucher, G., & Hartenstein, V. (2022) · The Journal of Comparative Neurology · doi:10.1002/cne.25335 · Cited by 22 · see citing works
Self-citationGenetic transformation of structural and functional circuitry rewires the Drosophila brain
Sen, S., Cao, D.-S., Choudhary, R., Biagini, S., Wang, J. W., Reichert, H., & VijayRaghavan, K. (2014) · eLife · doi:10.7554/elife.04407 · Cited by 19 · see citing works
Development of the anterior visual input pathway to the Drosophila central complex
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Self-citationLovick, J. K., & Hartenstein, V. (2015) · Developmental Biology · doi:10.1016/j.ydbio.2015.03.005 · Cited by 16 · see citing works
Self-citationLovick, J. K., Kong, A., Omoto, J. J., Ngo, K., Younossi‐Hartenstein, A., & Hartenstein, V. (2015) · Developmental Neurobiology · doi:10.1002/dneu.22325 · Cited by 15 · see citing works
Self-citationSexual dimorphism in the complete Drosophila male central nervous system connectome
Berg, S., Beckett, I. R., Costa, M., Philipp, S., Januszewski, M., Marin, E. C., Nern, A., Preibisch, S., Qiu, W., Takemura, S.-Y., et al. (2026) · Cell · doi:10.1016/j.cell.2026.08.015 · Cited by 68 · see citing works
Sen, S., Biagini, S., Reichert, H., & VijayRaghavan, K. (2014) · Biology Open · doi:10.1242/bio.20148524 · Cited by 12 · see citing works
Beyond Host Defense: Deregulation of Drosophila Immunity and Age-Dependent Neurodegeneration
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Pioneer interneurons instruct bilaterality in the Drosophila olfactory sensory map
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Minocha, S., Boll, W., & Noll, M. (2017) · PLoS ONE · doi:10.1371/journal.pone.0176002 · Cited by 10 · see citing works
Development of the Nervous System of Invertebrates
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Self-citationLineage-specific determination of ring neuron circuitry in the central complex of Drosophila
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Differential neuronal survival defines a novel axis of sexual dimorphism in the Drosophila brain
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Transcription factor codes patterning neuronal groundplans of the cerebrum
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Organization of descending neurons in the brain of the desert locust
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A Role for Exaptation in Sculpting Sexually Dimorphic Brains from Shared Neural LineagesPreprint
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Hierarchical diversification of neurons regulating motivated behaviorsPreprint
Elkahlah, N. A., Lin, Y., Pan, Y., Carter, J. A., Shirangi, T. R., & Clowney, E. J. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.06.03.657692 · Cited by 3 · see citing works
Rewiring the Drosophila Brain With Genetic Manipulations in Neural Lineages
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Neurogenesis in the Insect Central Nervous System and Its Peculiarities in the Brain Mushroom Bodies
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Sarcoplasmic reticulum Ca2+ dynamics in aging Drosophila and correlation with sarcopenia
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Mushroom Bodies of Stick and Leaf Insects (Phasmatodea: Insecta): Structure and Sources of Formation
Панов, А. А. (2021) · Biology Bulletin · doi:10.1134/s106235902101009x
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Self-citationStructural changes shaping the Drosophila ellipsoid body ER-neurons during development and aging
Koch, S., Kandimalla, P., Padilla, E. T., Kaur, S., Kaur, R., Nguyen, M., Nelson, A., Khalsa, S. K., Younossi‐Hartenstein, A., & Hartenstein, V. (2024) · Developmental Biology · doi:10.1016/j.ydbio.2024.07.018
Self-citation
- Authors
- Lovick, J. K., Ngo, K. T., Omoto, J. J., Wong, D. C., Nguyen, J. D., & Hartenstein, V.
- Affiliations
- University of California, Los Angeles (US)
- Corresponding author
- Hartenstein, Volker
- Venue
- Developmental Biology
- Publisher
- Elsevier BV
- Published
- 2013-12
- Volume
- 384
- Issue
- 2
- Pages
- 228-257
- ISSN
- 0012-1606 (ISSN-L)
- PMC
- PMC3886848
- OpenAlex
- W2008227188
- Cited by
- 48
- References
- 121
- Citations by year
- 2026: 3 · 2024: 3 · 2023: 2 · 2022: 2 · 2021: 3 · 2020: 5 · 2019: 3 · 2018: 3 · 2017: 8 · 2016: 4 · 2015: 5 · 2014: 6 · 2013: 1
- FWCI
- 2.15
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Developmental Biology (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- NIH (R01 NS29357-15)
- NSF Graduate Research Fellowship Program (DGE-0707424)
- Ruth L. Kirschstein National Research Service Award (GM007185)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Axon Guidance and Neuronal Signaling
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurobiology and Insect Physiology Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Keywords
- Drosophila brain, neuronal lineage, fascicles, neuroblasts, adult brain, synaptic proteins, lineage identity
- MeSH terms
- Animals, Brain, Drosophila, Humans, Metamorphosis, Biological, Body Patterning
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
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