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A novel wide-field neuron with branches in the lamina of the Drosophila visual system expresses myoinhibitory peptide and may be associated with the clock
Stockholm University, Faculty of Science, Department of Zoology.
Stockholm University, Faculty of Science, Department of Zoology.ORCID iD: 0000-0002-1147-7766
2011 (English)In: Cell and Tissue Research, ISSN 0302-766X, E-ISSN 1432-0878, Vol. 343, no 2, 357-369 p.Article in journal (Refereed) Published
Abstract [en]

Although neuropeptides are widespread throughout the central nervous system of the fruifly Drosophila, no records exist of peptidergic neurons in the first synaptic region of the visual system, the lamina. Here, we describe a novel type of neuron that has wide-field tangential arborizations just distal to the lamina neuropil and that expresses myoinhibitory peptide (MIP). The cell bodies of these neurons, designated lateral MIP-immunoreactive optic lobe (LMIo) neurons, lie anteriorly at the base of the medulla of the optic lobe. The LMIo neurons also arborize in several layers of the medulla and in the dorso-lateral and lateral protocerebrum. Since the LMIo resemble LN(v) clock neurons, we have investigated the relationships between these two sets of neurons by combining MIP-immunolabeling with markers for two of the clock genes, viz., Cryptochrome and Timeless, or with antisera to two peptides expressed in clock neurons, viz., pigment-dispersing factor and ion transport peptide. LMIo neurons do not co-express any of these clock neuron markers. However, branches of LMIo and clock neurons overlap in several regions. Furthermore, the varicose lamina branches of LMIo neurons superimpose those of two large bilateral serotonergic neurons. The close apposition of the terminations of MIP- and serotonin-producing neurons distal to the lamina suggests that they have the same peripheral targets. Our data indicate that the LMIo neurons are not bona fide clock neurons, but they may be associated with the clock system and regulate signaling peripherally in the visual system.

Place, publisher, year, edition, pages
2011. Vol. 343, no 2, 357-369 p.
Keyword [en]
Neuropeptide, Allatostatin B, Serotonin, Biological clock, Optic lobe, Insect brain, Drososphila melanogaster (Insecta)
National Category
Research subject
Systematic Zoology
URN: urn:nbn:se:su:diva-54720DOI: 10.1007/s00441-010-1100-7ISI: 000286829000007PubMedID: 21174124OAI: diva2:397229
Available from: 2011-02-14 Created: 2011-02-14 Last updated: 2014-10-28Bibliographically approved
In thesis
1. Chemical circuitry in the visual system of the fruitfly, Drosophila melanogaster
Open this publication in new window or tab >>Chemical circuitry in the visual system of the fruitfly, Drosophila melanogaster
2011 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Signal processing in the visual system is mediated by classic neurotransmission and neuropeptidergic modulatory pathways. In Dipteran insects, especially in the fruitfly Drosophila melanogaster, the morphology of the visual system is very well described. However neurotransmitter and neuropeptidergic circuits within the optic lobe neuropil are only partially known.

Using several transgenic fly lines and antibodies we determined the localization of the classical neurotransmitters GABA, acetylcholine and glutamate in the visual system, and their putative targets via detecting several neurotransmitter receptors. We paid particular attention to the peripheral neuropil layer called the lamina, where the light signals are filtered, channeled and amplified (Paper I).

We discovered four new types of efferent tangential neurons branching distally to the lamina. Among them was the first neuropeptidergic neuron (LMIo) in this region of Drosophila. The LMIo expresses myoinhibitory peptide (MIP) and has its cell body located close to the main lateral clock neurons that express the neuropeptide pigment-dispersing factor (PDF)(Paper II).

Since in other Dipteran species PDF is expressed in processes distally to the lamina, we performed comparative anatomical studies of the MIP, PDF, Ion Transport Peptide (ITP) and serotonin (5-HT) distribution in the visual system of the flies Drosophila and Calliphora. Our data suggest that PDF signaling distal to the lamina of the blowfly might be replaced by MIP signaling in the fruitfly, while ITP and 5-HT expression is conserved in the two species (Paper III).

Serotonin is crucial in light adaptation during the daily light-dark cycles. We analyzed putative serotonergic circuits in the lamina. We found that LMIo neurons express the inhibitory receptor 5-HT1A, while 5-HT1B and 5-HT2 are both expressed in the epithelial glia of the lamina. Another novel wide-field neuron with lamina branches expresses the excitatory serotonin receptor 5-HT7. Our studies have identified a fairly complex neuronal circuitry in the tangential plexus above the lamina. (Paper IV).

Finally we tested circadian locomotor activity rhythms in flies with the GABAB receptor knocked down on the lateral PDF-expressing clock neurons. We observed significant changes in the activity periods and diminished strength of rhythmicity during DD suggesting a modulatory role of GABA in clock function (Paper V).

Place, publisher, year, edition, pages
Stockholm: Department of Zoology, Stockholm University, 2011. 43 p.
Optic lobe, lamina, neurotransmitters, neuropeptides, tangential neurons
National Category
Research subject
Functional Zoomorphology
urn:nbn:se:su:diva-60160 (URN)978-91-7447-331-5 (ISBN)
Public defence
2011-09-23, Nordenskiöldsalen, Geovetenskapens hus, Svante Arrhenius väg 12, Stockholm, 10:00 (English)
At the time of the doctoral defense, the following papers were unpublished and had a status as follows: Paper 4: Manuscript. Paper 5: Manuscript.Available from: 2011-09-01 Created: 2011-08-10 Last updated: 2011-08-12Bibliographically approved

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