Chemical neuroanatomy of the Drosophila central complex: Distribution of multiple neuropeptides in relation to neurotransmitters
Abstract
The central complex of the insect brain is an integration center, receiving inputs from many parts of the brain. In Drosophila it has been associated with the control of both locomotor and visually correlated behaviors. The central complex can be divided into several substructures and is comprised of a large number of neuronal types. These neurons produce classical neurotransmitters, biogenic amines, and different neuropeptides. However, the distribution of neurotransmitters and neuromodulators in central‐complex circuits of Drosophila is poorly known. By immunolabeling and GAL4‐directed expression of marker proteins, we analyzed the distribution of acetylcholine, glutamate, GABA, monoamines, and eight different neuropeptides; Drosophila tachykinin, short neuropeptide F, myoinhibitory peptide, allatostatin A, proctolin, SIFamide, neuropeptide F, and FMRFamide. All eight neuropeptides were localized to the fan‐shaped body, the largest substructure of the central complex, and were mapped to different layers within this structure. Several populations of peptide‐immunoreactive tangential and columnar neurons were identified, of which some colocalized acetylcholine. Fewer peptides were found to be expressed in the other substructures: the ellipsoid body, the protocerebral bridge, and the noduli. The ellipsoid body and the protocerebral bridge were innervated by extrinsic peptide expressing neurons. Our findings reveal that numerous neuropeptides are expressed in the central complex and that each peptide has a distinct distribution pattern, suggesting important roles for neuropeptides as neuromediators and cotransmitters in this brain area. J. Comp. Neurol. 519:290‐315, 2011. © 2010 Wiley‐Liss, Inc.
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The fan-shaped body is known to express leucokinin, allatostatin A, short neuropeptide F, Drosophila neuropeptide F, tachykinin, proctolin, dFMRFa, SIFamide and myoinhibitory peptide in a highly specific and layer-wise manner.
“The fan-shaped body is known to express leucokinin, allatostatin A, short neuropeptide F, Drosophila neuropeptide F, tachykinin, proctolin, dFMRFa, SIFamide and myoinhibitory peptide in a highly specific and layer-wise manner.106,175,177,184”
From Neurotransmitter classification from electron microscopy images at synaptic sites in Drosophila melanogaster (2024) · cites this paper as [175]
The hDeltaK misprediction is because their presynapses lie in layer 6, an unusual layer known to express allatostatin A, short neuropeptide F and innexin 6.
“because their presynapses lie in layer 6 of the fan-shaped body (Figure 5G, arrows), an unusual layer that is known to express allatostatin A, short neuropeptide F and innexin 6.175,184,185”
From Neurotransmitter classification from electron microscopy images at synaptic sites in Drosophila melanogaster (2024) · cites this paper as [175]
dFMRFa is expressed in layer 4, and SIFamide and proctolin are expressed in layer 5.
“but we note that dFMRFa is expressed in layer 4, and SIFamide and proctolin are expressed in layer 5.175,186”
From Neurotransmitter classification from electron microscopy images at synaptic sites in Drosophila melanogaster (2024) · cites this paper as [175]
Short neuropeptide F has been shown to co-localise in 5-6 neurons with cholinergic transmission specifically in layers 5-6.
“In addition, short neuropeptide F has been shown to co-localise in 5-6 neurons with cholinergic transmission specifically in layers 5-6,175”
From Neurotransmitter classification from electron microscopy images at synaptic sites in Drosophila melanogaster (2024) · cites this paper as [175]
Serotonin is used in layers 3, 6 and more ventral layers of the fan-shaped body.
“serotonin immunolabeling revealed that serotonin is used in layers 3, 6 and more ventral layers.150,175”
From Neurotransmitter classification from electron microscopy images at synaptic sites in Drosophila melanogaster (2024) · cites this paper as [175]
Cites
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
Multiple neuropeptides in the <i>Drosophila</i> antennal lobe suggest complex modulatory circuits
Carlsson, M. A., Diesner, M., Schachtner, J., & Nässel, D. R. (2010) · Journal of Comparative Neurology · doi:10.1002/cne.22405 · Cited by 146 · see citing works
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Hulse, B. K., Haberkern, H., Franconville, R., Turner-Evans, D., Takemura, S.-Y., Wolff, T., Noorman, M., Dreher, M., Dan, C., Parekh, R., et al. (2021) · eLife · doi:10.7554/elife.66039 · Cited by 392 · see citing works
Organization and Functional Roles of the Central Complex in the Insect Brain
Pfeiffer, K., & Homberg, U. (2014) · Annual Review of Entomology · doi:10.1146/annurev-ento-011613-162031 · Cited by 392 · see citing works
An Anatomically Constrained Model for Path Integration in the Bee Brain
Stone, T., Webb, B., Adden, A., Weddig, N. B., Honkanen, A., Templin, R., Wcislo, W., Scimeca, L., Warrant, E., & Heinze, S. (2017) · Current Biology · doi:10.1016/j.cub.2017.08.052 · Cited by 377 · see citing works
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Ring Attractor Dynamics Emerge from a Spiking Model of the Entire Protocerebral Bridge
Kakaria, K. S., & de Bivort, B. L. (2017) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2017.00008 · Cited by 89 · see citing works
Kahsai, L., Carlsson, M. A., Winther, Å. M. E., & Nässel, D. R. (2012) · Neuroscience · doi:10.1016/j.neuroscience.2012.02.007 · Cited by 65 · see citing works
Self-citationHulse, B. K., Haberkern, H., Franconville, R., Turner-Evans, D. B., Takemura, S., Wolff, T., Noorman, M., Dreher, M., Dan, C., Parekh, R., et al. (2020) · doi:10.1101/2020.12.08.413955 · Cited by 392 · see citing works
“The CX is innervated by a large number of modulatory and peptidergic neurons (Kahsai et al., 2012; Kahsai et al., 2010; Kahsai and Winther, 2011), many unidentified and almost all of unknown function.”
Background
- Authors
- Kahsai, L., & Winther, Å. M. E.
- Affiliations
- Stockholm University (SE)
- Corresponding author
- Winther, Åsa M.E.
- Venue
- Journal of Comparative Neurology
- Publisher
- Wiley
- Published
- 2010-12-16
- Volume
- 519
- Issue
- 2
- Pages
- 290-315
- ISSN
- 0021-9967 (ISSN-L)
- 1096-9861
- OpenAlex
- W1985282761
- Cited by
- 115
- References
- 2
- Citations by year
- 2026: 7 · 2025: 12 · 2024: 5 · 2023: 8 · 2022: 10 · 2021: 9 · 2020: 3 · 2019: 5 · 2018: 4 · 2017: 10 · 2016: 5 · 2015: 4 · 2014: 7 · 2013: 11 · 2012: 7
- FWCI
- 3.36
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- The Journal of Comparative Neurology (publishedVersion)
- PubMed (publishedVersion)
- Funders
- University of Oxford
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurobiology and Insect Physiology Research
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuropeptides and Animal Physiology
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Keywords
- neuropeptides, neurotransmitters, neuromodulators, acetylcholine, glutamate, GABA, monoamines, tachykinins, short neuropeptide F, myoinhibitory peptides, allatostatin A, proctolin, SIFamide, neuropeptide F, FMRFamide, fan-shaped body, ellipsoid body, protocerebral bridge, co-transmission, insect brain
- MeSH terms
- Animals, Drosophila melanogaster, Immunohistochemistry, Neurons, Neuropeptides, Biomarkers, Neurotransmitter Agents, Drosophila Proteins
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