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Chemical circuitry in the visual system of the fruitfly, Drosophila melanogaster
Stockholm University, Faculty of Science, Department of Zoology.
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.
Keyword [en]
Optic lobe, lamina, neurotransmitters, neuropeptides, tangential neurons
National Category
Zoology
Research subject
Functional Zoomorphology
Identifiers
URN: urn:nbn:se:su:diva-60160ISBN: 978-91-7447-331-5 (print)OAI: oai:DiVA.org:su-60160DiVA: diva2:433571
Public defence
2011-09-23, Nordenskiöldsalen, Geovetenskapens hus, Svante Arrhenius väg 12, Stockholm, 10:00 (English)
Opponent
Supervisors
Note
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
List of papers
1. Glutamate, GABA and acetylcholine signaling components in the lamina of the Drosophila visual system
Open this publication in new window or tab >>Glutamate, GABA and acetylcholine signaling components in the lamina of the Drosophila visual system
2008 (English)In: PLoS ONE, ISSN 1932-6203, E-ISSN 1932-6203, Vol. 3, no 5, e2110- p.Article in journal (Refereed) Published
Abstract [en]

Synaptic connections of neurons in the Drosophila lamina, the most peripheral synaptic region of the visual system, have been comprehensively described. Although the lamina has been used extensively as a model for the development and plasticity of synaptic connections, the neurotransmitters in these circuits are still poorly known. Thus, to unravel possible neurotransmitter circuits in the lamina of Drosophila we combined Gal4 driven green fluorescent protein in specific lamina neurons with antisera to γ-aminobutyric acid (GABA), glutamic acid decarboxylase, a GABAB type of receptor, L-glutamate, a vesicular glutamate transporter (vGluT), ionotropic and metabotropic glutamate receptors, choline acetyltransferase and a vesicular acetylcholine transporter. We suggest that acetylcholine may be used as a neurotransmitter in both L4 monopolar neurons and a previously unreported type of wide-field tangential neuron (Cha-Tan). GABA is the likely transmitter of centrifugal neurons C2 and C3 and GABAB receptor immunoreactivity is seen on these neurons as well as the Cha-Tan neurons. Based on an rdl-Gal4 line, the ionotropic GABAA receptor subunit RDL may be expressed by L4 neurons and a type of tangential neuron (rdl-Tan). Strong vGluT immunoreactivity was detected in α-processes of amacrine neurons and possibly in the large monopolar neurons L1 and L2. These neurons also express glutamate-like immunoreactivity. However, antisera to ionotropic and metabotropic glutamate receptors did not produce distinct immunosignals in the lamina. In summary, this paper describes novel features of two distinct types of tangential neurons in the Drosophila lamina and assigns putative neurotransmitters and some receptors to a few identified neuron types.

National Category
Zoology
Research subject
Functional Zoomorphology
Identifiers
urn:nbn:se:su:diva-14291 (URN)10.1371%2Fjournal.pone.0002110 (DOI)000261642400032 ()18464935 (PubMedID)
Available from: 2008-08-14 Created: 2008-08-14 Last updated: 2017-12-13Bibliographically approved
2. 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
Open this publication in new window or tab >>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
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.

Keyword
Neuropeptide, Allatostatin B, Serotonin, Biological clock, Optic lobe, Insect brain, Drososphila melanogaster (Insecta)
National Category
Zoology
Research subject
Systematic Zoology
Identifiers
urn:nbn:se:su:diva-54720 (URN)10.1007/s00441-010-1100-7 (DOI)000286829000007 ()21174124 (PubMedID)
Available from: 2011-02-14 Created: 2011-02-14 Last updated: 2017-12-11Bibliographically approved
3. Myoinhibitory peptide (MIP) immunoreactivity in the visual system of the blowfly Calliphora vomitoria in relation to putative clock neurons and serotonergic neurons
Open this publication in new window or tab >>Myoinhibitory peptide (MIP) immunoreactivity in the visual system of the blowfly Calliphora vomitoria in relation to putative clock neurons and serotonergic neurons
2011 (English)In: Cell and Tissue Research, ISSN 0302-766X, E-ISSN 1432-0878, Vol. 345, no 1, 125-135 p.Article in journal (Refereed) Published
Abstract [en]

A few types of peptidergic clock neurons have been identified in the fruitfly Drosophila, whereas in blowflies, only pigment-dispersing factor (PDF)-immunoreactive lateral ventral clock neurons (LNvs) have been described. In blowflies, but not Drosophila, a subset of these PDF-expressing neurons supplies axon branches to a region outside the synaptic layer of the lamina, the most peripheral optic lobe neuropil. In Drosophila, similar lamina processes are instead supplied by non-clock neurons (LMIo) that express myoinhibitory peptide (MIP). We have investigated the distribution of MIP-immunoreactive neurons in the visual system of the blowfly Calliphora vomitoria and found neurons resembling the three LMIos, but without processes to the lamina. In Calliphora, PDF-immunoreactive processes of LNvs in the lamina closely impinge on branching serotonin-immunoreactive axon terminations in the same region. We have also identified, in the blowfly, two types of putative clock neurons that label with an antiserum to ion-transport peptide (ITP). The presence of serotonin-immunoreactive neurons supplying processes to the lamina seems to be a conserved feature in dipteran flies. The morphology of the two types of ITP-immunoreactive clock neurons might also be conserved. However, peptidergic neurons with branches converging on the serotonin-immunoreactive neurons in the lamina are of different morphological types and express PDF in blowflies and MIP in Drosophila. The central circuitry of these PDF- and MIP-expressing neurons probably differs; consequently, whether their convergence on serotonergic neurons subserves similar functions in the two species is unclear.

Keyword
Allatostatin B, 5-Hydroxytryptamine, Pigment-dispersing factor, Ion-transport peptide, Brain, Biological clock, Optic lobe, Calliphora vomitoria (Insecta)
National Category
Zoology
Research subject
Functional Zoomorphology
Identifiers
urn:nbn:se:su:diva-60158 (URN)10.1007/s00441-011-1198-2 (DOI)000293400300007 ()
Available from: 2011-08-12 Created: 2011-08-10 Last updated: 2017-12-08Bibliographically approved
4. Distribution of serotonin receptors in the visual system of the Drosophila
Open this publication in new window or tab >>Distribution of serotonin receptors in the visual system of the Drosophila
(English)Manuscript (preprint) (Other academic)
National Category
Zoology
Research subject
Functional Zoomorphology
Identifiers
urn:nbn:se:su:diva-60157 (URN)
Available from: 2011-08-10 Created: 2011-08-10 Last updated: 2014-10-28Bibliographically approved
5. The GABAB receptor is expressed by PDF-producing clockneurons and modulates circadian locomotor activity in Drosophila
Open this publication in new window or tab >>The GABAB receptor is expressed by PDF-producing clockneurons and modulates circadian locomotor activity in Drosophila
(English)Manuscript (preprint) (Other academic)
National Category
Zoology
Research subject
Functional Zoomorphology
Identifiers
urn:nbn:se:su:diva-60153 (URN)
Available from: 2011-08-12 Created: 2011-08-10 Last updated: 2011-12-16

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