Neuronal assemblies of the Drosophila mushroom body
Abstract
The mushroom body (MB) of the insect brain has important roles in odor learning and memory and in diverse other brain functions. To elucidate the anatomical basis underlying its function, we studied how the MB of Drosophila is organized by its intrinsic and extrinsic neurons. We screened for the GAL4 enhancer‐trap strains that label specific subsets of these neurons and identified seven subtypes of Kenyon cells and three other intrinsic neuron types. Laminar organization of the Kenyon cell axons divides the pedunculus into at least five concentric strata. The α′, β′, α, and β lobes are each divided into three strata, whereas the γ lobe appears more homogeneous. The outermost stratum of the α/β lobes is specifically connected with a small, protruded subregion of the calyx, the accessory calyx, which does not receive direct olfactory input. As for the MB extrinsic neurons (MBENs), we found three types of antennal lobe projection neurons, among which two are novel. In addition, we resolved 17 other types of MBENs that arborize in the calyx, lobes, and pedunculus. Lobe‐associated MBENs arborize in only specific areas of the lobes, being restricted along their longitudinal axes, forming two to five segmented zones in each lobe. The laminar arrangement of the Kenyon cell axons and segmented organization of the MBENs together divide the lobes into smaller synaptic units, possibly facilitating characteristic interaction between intrinsic and extrinsic neurons in each unit for different functional activities along the longitudinal lobe axes and between lobes. Structural differences between lobes are also discussed. J. Comp. Neurol. 508:711–755, 2008. © 2008 Wiley‐Liss, Inc.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
The five MB lobes on the right hemisphere are further divided into 15 compartments (α1-3, α'1-3, β1-2, β'1-2, and γ1-5) by the mushroom body output neurons (MBONs) and dopaminergic neurons (DANs).
“The five MB lobes on the right hemisphere are further divided into 15 compartments (α1–3, α’1–3, β1–2, β’1–2, and γ1–5) (Tanaka et al., 2008; Aso et al., 2014) by the mushroom body output neurons (MBONs) and dopaminergic neurons (DANs).”
From A connectome and analysis of the adult Drosophila central brain (2020) · cites this paper as Tanaka et al., 2008
Cites
The organization of the chemosensory system in Drosophila melanogaster: a rewiew
Stocker, R. F. (1994) · Cell and Tissue Research · doi:10.1007/bf00305372 · Cited by 950 · see citing works
Waddell, S., Armstrong, J. D., Kitamoto, T., Kaiser, K., & Quinn, W. G. (2000) · Cell · doi:10.1016/s0092-8674(00)00183-5 · Cited by 332 · see citing works
Otsuna, H., & Ito, K. (2006) · The Journal of Comparative Neurology · doi:10.1002/cne.21015 · Cited by 224 · see citing works
Self-citation
Flagged first, then by citations
Cited by
Sorted by citations
A GAL4-Driver Line Resource for Drosophila Neurobiology
Jenett, A., Rubin, G. M., Ngo, T.-T. B., Shepherd, D., Murphy, C., Dionne, H., Pfeiffer, B. D., Cavallaro, A., Hall, D., Jeter, J., et al. (2012) · Cell Reports · doi:10.1016/j.celrep.2012.09.011 · Cited by 1,449 · see citing works
A connectome and analysis of the adult Drosophila central brain
Scheffer, L. K., Xu, C. S., Januszewski, M., Lu, Z., Takemura, S.-Y., Hayworth, K. J., Huang, G. B., Shinomiya, K., Maitlin-Shepard, J., Berg, S., et al. (2020) · eLife · doi:10.7554/elife.57443 · Cited by 1,128 · see citing works
“The mushroom body (Tanaka et al., 2008; Aso et al., 2014) and central complex (Wolff et al.”
BackgroundSelf-citationA Complete Electron Microscopy Volume of the Brain of Adult Drosophila melanogaster
Zheng, Z., Lauritzen, J. S., Perlman, E., Robinson, C. G., Nichols, M., Milkie, D., Torrens, O., Price, J., Fisher, C. B., Sharifi, N., et al. (2018) · Cell · doi:10.1016/j.cell.2018.06.019 · Cited by 1,050 · see citing works
A Systematic Nomenclature for the Insect Brain
Ito, K., Shinomiya, K., Ito, M., Armstrong, J. D., Boyan, G., Hartenstein, V., Harzsch, S., Heisenberg, M., Homberg, U., Jenett, A., et al. (2014) · Neuron · doi:10.1016/j.neuron.2013.12.017 · Cited by 611 · see citing works
Self-citationA Neural Circuit Mechanism Integrating Motivational State with Memory Expression in Drosophila
Krashes, M. J., DasGupta, S., Vreede, A., White, B., Armstrong, J. D., & Waddell, S. (2009) · Cell · doi:10.1016/j.cell.2009.08.035 · Cited by 598 · see citing works
Layered reward signalling through octopamine and dopamine in Drosophila
Burke, C. J., Huetteroth, W., Owald, D., Perisse, E., Krashes, M. J., Das, G., Gohl, D., Silies, M., Certel, S., & Waddell, S. (2012) · Nature · doi:10.1038/nature11614 · Cited by 614 · see citing works
Random convergence of olfactory inputs in the Drosophila mushroom body
Caron, S. J. C., Ruta, V., Abbott, L. F., & Axel, R. (2013) · Nature · doi:10.1038/nature12063 · Cited by 409 · see citing works
Coordinated and compartmentalized neuromodulation shapes sensory processing in Drosophila
Cohn, R., Morantte, I., & Ruta, V. (2015) · Cell · doi:10.1016/j.cell.2015.11.019 · Cited by 430 · see citing works
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
“The mushroom body contains five principal cell classes: KCs, mushroom body output neurons (MBONs), modulatory neurons (dopaminergic neurons (DANs) and octopaminergic neurons (OANs)), the dorsal paired medial (DPM) and anterior paired lateral neuron (APL) giant interneurons 48 (Fig.”
BackgroundHeterosynaptic plasticity underlies aversive olfactory learning in Drosophila
Hige, T., Aso, Y., Modi, M. N., Rubin, G. M., & Turner, G. C. (2015) · Neuron · doi:10.1016/j.neuron.2015.11.003 · Cited by 354 · see citing works
A connectome of a learning and memory center in the adult Drosophila brain
Takemura, S.-Y., Aso, Y., Hige, T., Wong, A., Lu, Z., Xu, C. S., Rivlin, P. K., Hess, H., Zhao, T., Parag, T., et al. (2017) · eLife · doi:10.7554/elife.26975 · Cited by 367 · see citing works
Costa, M., Manton, J. D., Ostrovsky, A. D., Prohaska, S., & Jefferis, G. S. X. E. (2016) · Neuron · doi:10.1016/j.neuron.2016.06.012 · Cited by 294 · see citing works
Cellular diversity in the Drosophila midbrain revealed by single-cell transcriptomics
Croset, V., Treiber, C. D., & Waddell, S. (2018) · eLife · doi:10.7554/elife.34550 · Cited by 299 · see citing works
A map of octopaminergic neurons in the <i>Drosophila</i> brain
Busch, S., Selcho, M., Ito, K., & Tanimoto, H. (2009) · Journal of Comparative Neurology · doi:10.1002/cne.21966 · Cited by 255 · see citing works
Self-citationThe GABAergic anterior paired lateral neuron suppresses and is suppressed by olfactory learning
Liu, X., & Davis, R. L. (2009) · Nature Neuroscience · doi:10.1038/nn.2235 · Cited by 250 · see citing works
Tsao, C.-H., Chen, C.-C., Lin, C.-H., Yang, H.-Y., & Lin, S. (2018) · eLife · doi:10.7554/elife.35264 · Cited by 214 · see citing works
Memory-Relevant Mushroom Body Output Synapses Are Cholinergic
Barnstedt, O., Owald, D., Felsenberg, J., Brain, R., Moszynski, J.-P., Talbot, C. B., Perrat, P. N., & Waddell, S. (2016) · Neuron · doi:10.1016/j.neuron.2016.02.015 · Cited by 197 · see citing works
Direct neural pathways convey distinct visual information to Drosophila mushroom bodies
Vogt, K., Aso, Y., Hige, T., Knapek, S., Ichinose, T., Friedrich, A. B., Turner, G. C., Rubin, G. M., & Tanimoto, H. (2016) · eLife · doi:10.7554/elife.14009 · Cited by 155 · see citing works
Self-citationDolan, M.-J., Frechter, S., Bates, A. S., Dan, C., Huoviala, P., Roberts, R. J., Schlegel, P., Dhawan, S., Tabano, R., Dionne, H., et al. (2019) · eLife · doi:10.7554/elife.43079 · Cited by 169 · see citing works
Gamma‐aminobutyric acid (GABA)‐mediated neural connections in the <i>Drosophila</i> antennal lobe
Okada, R., Awasaki, T., & Ito, K. (2009) · Journal of Comparative Neurology · doi:10.1002/cne.21971 · Cited by 146 · see citing works
Self-citationAso, Y., Ray, R. P., Long, X., Bushey, D., Cichewicz, K., Ngo, T.-T., Sharp, B., Christoforou, C., Hu, A., Lemire, A. L., et al. (2019) · eLife · doi:10.7554/elife.49257 · Cited by 141 · see citing works
Nässel, D. R. (2009) · Invertebrate Neuroscience · doi:10.1007/s10158-009-0090-1 · Cited by 125 · see citing works
Spaced Training Forms Complementary Long-Term Memories of Opposite Valence in Drosophila
Jacob, P. F., & Waddell, S. (2020) · Neuron · doi:10.1016/j.neuron.2020.03.013 · Cited by 112 · see citing works
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. (2023) · doi:10.1101/2023.06.27.546055 · Cited by 102 · see citing works
Scribble Scaffolds a Signalosome for Active Forgetting
Cervantes-Sandoval, I., Chakraborty, M., MacMullen, C., & Davis, R. L. (2016) · Neuron · doi:10.1016/j.neuron.2016.05.010 · Cited by 100 · see citing works
Functional and anatomical specificity in a higher olfactory centre
Frechter, S., Bates, A. S., Tootoonian, S., Dolan, M.-J., Manton, J., Jamasb, A. R., Kohl, J., Bock, D., & Jefferis, G. (2019) · eLife · doi:10.7554/elife.44590 · Cited by 105 · see citing works
Role for VGLUT2 in selective vulnerability of midbrain dopamine neurons
Steinkellner, T., Zell, V., Farino, Z. J., Sonders, M. S., Villeneuve, M., Freyberg, R. J., Przedborski, S., Lu, W., Freyberg, Z., & Hnasko, T. S. (2018) · Journal of Clinical Investigation · doi:10.1172/jci95795 · Cited by 102 · see citing works
Developmental origins and architecture of <i>Drosophila</i> leg motoneurons
Brierley, D. J., Rathore, K., VijayRaghavan, K., & Williams, D. W. (2012) · Journal of Comparative Neurology · doi:10.1002/cne.23003 · Cited by 73 · see citing works
The Drosophila Split Gal4 System for Neural Circuit Mapping
Luan, H., Diao, F., Scott, R. L., & White, B. H. (2020) · Frontiers in Neural Circuits · doi:10.3389/fncir.2020.603397 · Cited by 73 · see citing works
Structured sampling of olfactory input by the fly mushroom body
Zheng, Z., Li, F., Fisher, C., Ali, I. J., Sharifi, N., Calle-Schuler, S., Hsu, J., Masoodpanah, N., Kmecova, L., Kazimiers, T., et al. (2022) · Current Biology · doi:10.1016/j.cub.2022.06.031 · Cited by 75 · see citing works
Mitochondrial origins of the pressure to sleep
Sarnataro, R., Velasco, C. D., Monaco, N., Kempf, A., & Miesenböck, G. (2025) · Nature · doi:10.1038/s41586-025-09261-y · Cited by 62 · see citing works
Trace conditioning in insects—keep the trace!
Dylla, K. V., Galili, D. S., Szyszka, P., & Lüdke, A. (2013) · Frontiers in Physiology · doi:10.3389/fphys.2013.00067 · Cited by 57 · see citing works
Evolving the olfactory system with machine learning
Wang, P. Y., Sun, Y., Axel, R., Abbott, L. F., & Yang, G. R. (2021) · Neuron · doi:10.1016/j.neuron.2021.09.010 · Cited by 54 · see citing works
Second-order conditioning in <i>Drosophila</i>
Tabone, C. J., & de Belle, J. S. (2011) · Learning & Memory · doi:10.1101/lm.2035411 · Cited by 51 · see citing works
Feed-Forward versus Feedback Inhibition in a Basic Olfactory Circuit
Kee, T., Sanda, P., Gupta, N., Stopfer, M., & Bazhenov, M. (2015) · PLOS Computational Biology · doi:10.1371/journal.pcbi.1004531 · Cited by 40 · see citing works
Behavioral dissection of hunger states in Drosophila
Weaver, K. J., Raju, S., Rucker, R. A., Chakraborty, T., Holt, R. A., & Pletcher, S. D. (2023) · eLife · doi:10.7554/elife.84537.3 · Cited by 13 · see citing works
- Authors
- Tanaka, N. K., Tanimoto, H., & Ito, K.
- Affiliations
- National Institute for Basic Biology (JP)
- University of Würzburg (DE)
- Corresponding author
- Ito, Kei
- Venue
- Journal of Comparative Neurology
- Publisher
- Wiley
- Published
- 2008-04-07
- Volume
- 508
- Issue
- 5
- Pages
- 711-755
- ISSN
- 0021-9967 (ISSN-L)
- 1096-9861
- OpenAlex
- W1980949515
- Cited by
- 470
- References
- 3
- Citations by year
- 2026: 11 · 2025: 20 · 2024: 40 · 2023: 37 · 2022: 27 · 2021: 18 · 2020: 22 · 2019: 30 · 2018: 30 · 2017: 23 · 2016: 23 · 2015: 30 · 2014: 20 · 2013: 35 · 2012: 35
- FWCI
- 9.93
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- The Journal of Comparative Neurology (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurobiology and Insect Physiology Research
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Keywords
- mushroom body, Drosophila, Kenyon cells, intrinsic neurons, neuronal cell types, laminar organization, olfactory lobe, olfactory learning, memory, neuronal arborization
- MeSH terms
- Animals, Drosophila, Neural Pathways, Neurons, Mushroom Bodies
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.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
