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Distribution and modulatory roles of neuropeptides and neurotransmitters in the Drosophila brain 
Stockholm University, Faculty of Science, Department of Zoology.
2010 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

The central complex is a prominent neuropil found in the middle of the insect brain. It is considered as a higher center for motor control and information processing. Multiple neuropeptides and neurotransmitters are produced in neurons of the central complex, however, distribution patterns and functional roles of signaling substances in this brain region are poorly known. Thus, this thesis focuses on the distribution of signaling substances and on modulatory roles of neuropeptides in the central complex of Drosophila.

Immunocytochemistry in combination with GAL4/UAS technique was used to visualize various signaling substances in the central complex. We revealed different central-complex neurons expressing the neuropeptides; Drosophila tachykinin (DTK), short neuropeptide F (sNPF), myoinhibitory peptide (MIP), allatostatin A, proctolin, SIFamide, neuropeptide F and FMRFamide. Subpopulations of DTK, sNPF and MIP-expressing neurons were found to co-localize a marker for acetylcholine. In addition, five metabotropic neurotransmitter receptors were found to be expressed in distinct patterns. Comparison of receptor/ligand distributions revealed a close match in most of the structures studied.

By using a video-tracking assay, peptidergic modulation of locomotor behavior was studied. Different DTK and sNPF-expressing neurons innervating the central complex were revealed to modulate spatial distribution, number of activity-rest phases and activity levels, suggesting circuit dependent modulation.

Furthermore, neurosecretory cells in the Drosophila brain that co-express three types of neuropeptides were shown to modulate stress responses to desiccation and starvation.

In summary, we have studied two different neuropeptides (DTK and sNPF) expressed in interneuronal circuits and neurosecretory cells of the Drosophila brain in more detail. We found that these neuropeptides display multiple actions as neuromodulators and circulating hormones, and that their actions depend on where they are released.

Place, publisher, year, edition, pages
Stockholm: Department of Zoology, Stockholm University , 2010. , 44 p.
Keyword [en]
central complex, locomotor behavior, co-transmitter, metabotropic receptor, metabolic stress
National Category
Neurosciences
Research subject
Zoology
Identifiers
URN: urn:nbn:se:su:diva-42947ISBN: 978-91-7447-150-2 (print)OAI: oai:DiVA.org:su-42947DiVA: diva2:352353
Public defence
2010-10-29, Nordenskiöldsalen, Geovetenskapenshus, 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 2: In press. Paper 3: Manuscript.Available from: 2010-10-07 Created: 2010-09-20 Last updated: 2012-01-20Bibliographically approved
List of papers
1. Neuropeptides in the Drosophila central complex in modulation of locomotor behavior
Open this publication in new window or tab >>Neuropeptides in the Drosophila central complex in modulation of locomotor behavior
2010 (English)In: Journal of Experimental Biology, ISSN 0022-0949, E-ISSN 1477-9145, Vol. 213, 2256-2265 p.Article in journal (Refereed) Published
Abstract [en]

The central complex is one of the most prominent neuropils in the insect brain. It has been implicated in the control of locomotor activity and is considered as a pre-motor center. Several neuropeptides are expressed in circuits of the central complex, and thus may be modulators of locomotor behavior. Here we have investigated the roles of two different neuropeptides, Drosophila tachykinin (DTK) and short neuropeptide F (sNPF), in aspects of locomotor behavior. In the Drosophila brain, DTK and sNPF are expressed in interneurons innervating the central complex. We have directed RNA interference (RNAi) towards DTK and sNPF specifically in different central complex neurons. We also expressed a temperature-sensitive dominant negative allele of the fly ortholog of dynamin called shibire(ts1), essential in membrane vesicle recycling and endocytosis, to disrupt synaptic transmission in central complex neurons. The spontaneous walking activity of the RNAi- or shibire(ts1)-expressing flies was quantified by video tracking. DTK-deficient flies displayed drastically increased center zone avoidance, suggesting that DTK is involved in the regulation of spatial orientation. In addition, DTK deficiency in other central complex neurons resulted in flies with an increased number of activity-rest bouts. Perturbations in the sNPF circuit indicated that this peptide is involved in the fine regulation of locomotor activity levels. Our findings suggest that the contribution of DTK and sNPF to locomotor behavior is circuit dependent and associated with particular neuronal substrates. Thus, peptidergic pathways in the central complex have specific roles in the fine tuning of locomotor activity of adult Drosophila.

National Category
Natural Sciences
Identifiers
urn:nbn:se:su:diva-40757 (URN)10.1242/jeb.043190 (DOI)000278671900018 ()
Available from: 2010-06-22 Created: 2010-06-22 Last updated: 2017-12-12Bibliographically approved
2. Chemical Neuroanatomy of the Drosophila Central Complex: Distribution of Multiple Neuropeptides in Relation to Neurotransmitters 
Open this publication in new window or tab >>Chemical Neuroanatomy of the Drosophila Central Complex: Distribution of Multiple Neuropeptides in Relation to Neurotransmitters 
2011 (English)In: Journal of Comparative Neurology, ISSN 0021-9967, E-ISSN 1096-9861, Vol. 519, no 2, 290-315 p.Article in journal (Refereed) Published
Abstract [en]

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.

Keyword
brain, interneurons, cotransmitter, neuromodulator, immunocytochemistry
National Category
Biological Sciences
Identifiers
urn:nbn:se:su:diva-42946 (URN)10.1002/cne.22520 (DOI)000285425700007 ()
Available from: 2010-09-20 Created: 2010-09-20 Last updated: 2017-12-12Bibliographically approved
3. Distribution of metabotropic receptors of serotonin, dopamine, GABA andglutamate in the central complex of Drosophila
Open this publication in new window or tab >>Distribution of metabotropic receptors of serotonin, dopamine, GABA andglutamate in the central complex of Drosophila
(English)Manuscript (preprint) (Other academic)
National Category
Microbiology
Identifiers
urn:nbn:se:su:diva-42930 (URN)
Available from: 2010-09-20 Created: 2010-09-20 Last updated: 2014-10-28Bibliographically approved
4. Metabolic stress responses in Drosophila are modulated by brain neurosecretory cells that produce multiple neuropeptides
Open this publication in new window or tab >>Metabolic stress responses in Drosophila are modulated by brain neurosecretory cells that produce multiple neuropeptides
Show others...
2010 (English)In: PLoS ONE, ISSN 1932-6203, E-ISSN 1932-6203, Vol. 5, no 7, e11480- p.Article in journal (Refereed) Published
Abstract [en]

In Drosophila, neurosecretory cells that release peptide hormones play a prominent role in the regulation of development, growth, metabolism, and reproduction. Several types of peptidergic neurosecretory cells have been identified in the brain of Drosophila with release sites in the corpora cardiaca and anterior aorta. We show here that in adult flies the products of three neuropeptide precursors are colocalized in five pairs of large protocerebral neurosecretory cells in two clusters (designated ipc-1 and ipc-2a): Drosophila tachykinin (DTK), short neuropeptide F (sNPF) and ion transport peptide (ITP). These peptides were detected by immunocytochemistry in combination with GFP expression driven by the enhancer trap Gal4 lines c929 and Kurs-6, both of which are expressed in ipc-1 and 2a cells. This mix of colocalized peptides with seemingly unrelated functions is intriguing and prompted us to initiate analysis of the function of the ten neurosecretory cells. We investigated the role of peptide signaling from large ipc-1 and 2a cells in stress responses by monitoring the effect of starvation and desiccation in flies with levels of DTK or sNPF diminished by RNA interference. Using the Gal4-UAS system we targeted the peptide knockdown specifically to ipc-1 and 2a cells with the c929 and Kurs-6 drivers. Flies with reduced DTK or sNPF levels in these cells displayed decreased survival time at desiccation and starvation, as well as increased water loss at desiccation. Our data suggest that homeostasis during metabolic stress requires intact peptide signaling by ipc-1 and 2a neurosecretory cells.

National Category
Biological Sciences
Identifiers
urn:nbn:se:su:diva-41306 (URN)10.1371/journal.pone.0011480 (DOI)000279637100010 ()
Available from: 2010-07-10 Created: 2010-07-10 Last updated: 2017-12-12Bibliographically approved

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