scholarly journals Interplay between axonal Wnt5-Vang and dendritic Wnt5-Drl/Ryk signaling controls glomerular patterning in the Drosophila antennal lobe

2019 ◽  
Author(s):  
Huey Hing ◽  
Jennifer Snyder ◽  
Noah Reger ◽  
Lee G. Fradkin
Keyword(s):  
Antennal Lobe ◽  
Planar Cell Polarity ◽  
Neural Circuit ◽  
Projection Neuron ◽  
Olfactory Receptor Neurons ◽  
Antibody Staining ◽  
Cell Type Specific ◽  
Receptor Neurons ◽  
Signaling Components ◽  
Biphasic Responses

Despite the importance of dendritic targeting in neural circuit assembly, the mechanisms by which it is controlled still remain incompletely understood. We previously showed that in the developing Drosophila antennal lobe, the Wnt5 protein forms a gradient that directs the ~45° rotation of a cluster of projection neuron (PN) dendrites, including the adjacent DA1 and VA1d dendrites. We report here that the Van Gogh (Vang) transmembrane planar cell polarity (PCP) protein is required for the rotation of the DA1/VA1d dendritic pair. Cell type-specific rescue and mosaic analyses showed that Vang functions in the olfactory receptor neurons (ORNs), suggesting a codependence of ORN axonal and PN dendritic targeting. Loss of Vang suppressed the repulsion of the VA1d dendrites by Wnt5, indicating that Wnt5 signals through Vang to direct the rotation of the DA1 and VA1d glomeruli. We observed that the Derailed (Drl)/Ryk atypical receptor tyrosine kinase is also required for the rotation of the DA1/VA1d dendritic pair. Antibody staining showed that Drl/Ryk is much more highly expressed by the DA1 dendrites than the adjacent VA1d dendrites. Mosaic and epistatic analyses showed that Drl/Ryk specifically functions in the DA1 dendrites in which it antagonizes the Wnt5-Vang repulsion and mediates the migration of the DA1 glomerulus towards Wnt5. Thus, the nascent DA1 and VA1d glomeruli appear to exhibit Drl/Ryk-dependent biphasic responses to Wnt5. Our work shows that the final patterning of the fly olfactory map is the result of an interplay between ORN axons and PN dendrites, wherein converging pre- and postsynaptic processes contribute key Wnt5 signaling components, allowing Wnt5 to orient the rotation of nascent synapses through a PCP mechanism.

scholarly journals Transsynaptic Fish-lips signaling prevents misconnections between nonsynaptic partner olfactory neurons

2019 ◽  
Vol 116 (32) ◽  
pp. 16068-16073 ◽  
Author(s):  
Qijing Xie ◽  
Bing Wu ◽  
Jiefu Li ◽  
Chuanyun Xu ◽  
Hongjie Li ◽  
...  
Keyword(s):  
Neural Circuit ◽  
Transmembrane Protein ◽  
Small Subset ◽  
Projection Neurons ◽  
Specific Expression ◽  
Olfactory Neurons ◽  
Surface Molecules ◽  
Cell Type Specific Expression ◽  
Cell Type Specific ◽  
Receptor Neurons

Our understanding of the mechanisms of neural circuit assembly is far from complete. Identification of wiring molecules with novel mechanisms of action will provide insights into how complex and heterogeneous neural circuits assemble during development. In the Drosophila olfactory system, 50 classes of olfactory receptor neurons (ORNs) make precise synaptic connections with 50 classes of partner projection neurons (PNs). Here, we performed an RNA interference screen for cell surface molecules and identified the leucine-rich repeat–containing transmembrane protein known as Fish-lips (Fili) as a novel wiring molecule in the assembly of the Drosophila olfactory circuit. Fili contributes to the precise axon and dendrite targeting of a small subset of ORN and PN classes, respectively. Cell-type–specific expression and genetic analyses suggest that Fili sends a transsynaptic repulsive signal to neurites of nonpartner classes that prevents their targeting to inappropriate glomeruli in the antennal lobe.

scholarly journals Cholinergic calcium responses in cultured antennal lobe neurons of the migratory locust

2021 ◽  
Vol 11 (1) ◽  
Author(s):  
Gregor A. Bergmann ◽  
Gerd Bicker
Keyword(s):  
Olfactory Receptor ◽  
Intracellular Signaling ◽  
Antennal Lobe ◽  
Locusta Migratoria ◽  
Cytosolic Calcium ◽  
Olfactory Receptor Neurons ◽  
Future Research ◽  
Migratory Locust ◽  
Local Interneurons ◽  
Receptor Neurons

AbstractLocusts are advantageous organisms to elucidate mechanisms of olfactory coding at the systems level. Sensory input is provided by the olfactory receptor neurons of the antenna, which send their axons into the antennal lobe. So far, cellular properties of neurons isolated from the circuitry of the olfactory system, such as transmitter-induced calcium responses, have not been studied. Biochemical and immunocytochemical investigations have provided evidence for acetylcholine as classical transmitter of olfactory receptor neurons. Here, we characterize cell cultured projection and local interneurons of the antennal lobe by cytosolic calcium imaging to cholinergic stimulation. We bulk loaded the indicator dye Cal-520 AM in dissociated culture and recorded calcium transients after applying cholinergic agonists and antagonists. The majority of projection and local neurons respond with increases in calcium levels to activation of both nicotinic and muscarinic receptors. In local interneurons, we reveal interactions lasting over minutes between intracellular signaling pathways, mediated by muscarinic and nicotinic receptor stimulation. The present investigation is pioneer in showing that Cal-520 AM readily loads Locusta migratoria neurons, making it a valuable tool for future research in locust neurophysiology, neuropharmacology, and neurodevelopment.

scholarly journals Non-synaptic interactions between olfactory receptor neurons, a possible key feature of odor processing in insects

2020 ◽  
Author(s):  
Mario Pannunzi ◽  
Thomas Nowotny
Keyword(s):  
Lateral Inhibition ◽  
Olfactory Receptor ◽  
Olfactory System ◽  
Antennal Lobe ◽  
Olfactory Receptor Neurons ◽  
Inhibition Mechanism ◽  
Alternative Mechanism ◽  
Odor Processing ◽  
Synaptic Interactions ◽  
Receptor Neurons

AbstractWhen flies explore their environment, they encounter odors in complex, highly intermittent plumes. To navigate a plume and, for example, find food, flies must solve several tasks, including reliably identifying mixtures of odorants and discriminating odorant mixtures emanating from a single source from odorants emitted from separate sources and mixing in the air. Lateral inhibition in the antennal lobe is commonly understood to help solving these two tasks. With a computational model of the Drosophila olfactory system, we analyze the utility of an alternative mechanism for solving them: Non-synaptic (“ephaptic”) interactions (NSIs) between olfactory receptor neurons that are stereotypically co-housed in the same sensilla. For both tasks, NSIs improve the insect olfactory system and outperform the standard lateral inhibition mechanism in the antennal lobe. These results shed light, from an evolutionary perspective, on the role of NSIs, which are normally avoided between neurons, for instance by myelination.

scholarly journals Stepwise wiring of the Drosophila olfactory map requires specific Plexin B levels

eLife ◽  
2018 ◽  
Vol 7 ◽  
Author(s):  
Jiefu Li ◽  
Ricardo Guajardo ◽  
Chuanyun Xu ◽  
Bing Wu ◽  
Hongjie Li ◽  
...  
Keyword(s):  
Neural Circuit ◽  
Target Selection ◽  
Expression Patterns ◽  
Specific Distribution ◽  
The Neural Network ◽  
Regulated Expression ◽  
Cell Type Specific ◽  
Receptor Neurons ◽  
High Level ◽  
Subsequent Target

The precise assembly of a neural circuit involves many consecutive steps. The conflict between a limited number of wiring molecules and the complexity of the neural network impels each molecule to execute multiple functions at different steps. Here, we examined the cell-type specific distribution of endogenous levels of axon guidance receptor Plexin B (PlexB) in the developing antennal lobe, the first olfactory processing center in Drosophila. We found that different classes of olfactory receptor neurons (ORNs) express PlexB at different levels in two wiring steps – axonal trajectory choice and subsequent target selection. In line with its temporally distinct patterns, the proper levels of PlexB control both steps in succession. Genetic interactions further revealed that the effect of high-level PlexB is antagonized by its canonical partner Sema2b. Thus, PlexB plays a multifaceted role in instructing the assembly of the Drosophila olfactory circuit through temporally-regulated expression patterns and expression level-dependent effects.

scholarly journals Geosmin suppresses defensive behaviour and elicits unusual neural responses in honey bees.

2021 ◽  
Author(s):  
Florencia Scarano ◽  
Mukilan Deivarajan Suresh ◽  
Ettore Tiraboschi ◽  
Amélie Cabirol ◽  
Morgane Nouvian ◽  
...  
Keyword(s):  
Honey Bees ◽  
Olfactory Receptor ◽  
Antennal Lobe ◽  
Alarm Pheromone ◽  
Behavioural Change ◽  
Computational Modelling ◽  
Isoamyl Acetate ◽  
Olfactory Receptor Neurons ◽  
Defensive Behaviour ◽  
Receptor Neurons

Geosmin is an odorant produced by bacteria in moist soil. It has been found to be extraordinarily relevant to some insects, but the reasons for this are not yet fully understood. Here we report the first tests of the effect of geosmin on honey bees. A stinging assay showed that the defensive behaviour elicited by the bee's alarm pheromone is strongly suppressed by geosmin. Surprisingly, the suppression is, however, only present at very low geosmin concentrations, and completely disappears at higher concentrations. We investigated the underlying mechanisms of the behavioural change at the level of the olfactory receptor neurons by means of electroantennography and at the level of the antennal lobe output via calcium imaging. Unusual effects were observed at both levels. The responses of the olfactory receptor neurons to mixtures of geosmin and the alarm pheromone component isoamyl acetate (IAA) were lower than to pure IAA, suggesting an interaction of both compounds at the olfactory receptor level. In the antennal lobe, the neuronal representation of geosmin showed a glomerular activation that decreased with increasing concentration, correlating well with the concentration dependence of the behaviour. Computational modelling of odour transduction and odour coding in the antennal lobe suggests that a broader than usual activation of different olfactory receptor types by geosmin in combination with lateral inhibition in the antennal lobe could lead to the observed non-monotonic increasing-decreasing responses to geosmin and thus underlie the specificity of the behavioural response to low geosmin concentrations.

scholarly journals Cholinergic calcium responses in cultured antennal lobe neurons of the migratory locust

2021 ◽  
Author(s):  
Gregor A. Bergmann ◽  
Gerd Bicker
Keyword(s):  
Olfactory Receptor ◽  
Intracellular Signaling ◽  
Antennal Lobe ◽  
Locusta Migratoria ◽  
Cytosolic Calcium ◽  
Olfactory Receptor Neurons ◽  
Future Research ◽  
Migratory Locust ◽  
Local Interneurons ◽  
Receptor Neurons

AbstractLocusts are advantageous organisms to elucidate mechanisms of olfactory coding at the systems level. Sensory input is provided by the olfactory receptor neurons of the antenna, which send their axons into the antennal lobe. So far, cellular properties of neurons isolated from the circuitry of the olfactory system, such as transmitter-induced calcium responses, have not been studied. Biochemical and immunocytochemical investigations have provided evidence for acetylcholine as classical transmitter of olfactory receptor neurons. Here, we characterize cell cultured projection and local interneurons of the antennal lobe by cytosolic calcium imaging to cholinergic stimulation. We bulk loaded the indicator dye Cal-520 AM in dissociated culture and recorded calcium transients after applying cholinergic agonists and antagonists. The majority of projection and local neurons respond with increases in calcium levels to activation of both nicotinic and muscarinic receptors. In local interneurons, we reveal interactions lasting over minutes between intracellular signaling pathways, mediated by muscarinic and nicotinic receptor stimulation. The present investigation is pioneer in showing that Cal-520 AM readily loads Locusta migratoria neurons, making it a valuable tool for future research in locust neurophysiology, neuropharmacology, and neurodevelopment.

scholarly journals Non-synaptic interactions between olfactory receptor neurons, a possible key feature of odor processing in flies

2021 ◽  
Vol 17 (12) ◽  
pp. e1009583
Author(s):  
Mario Pannunzi ◽  
Thomas Nowotny
Keyword(s):  
Lateral Inhibition ◽  
Olfactory Receptor ◽  
Antennal Lobe ◽  
Dynamic Range ◽  
Olfactory Receptor Neurons ◽  
Alternative Mechanism ◽  
Mixture Ratio ◽  
Odor Processing ◽  
Functional Perspective ◽  
Receptor Neurons

When flies explore their environment, they encounter odors in complex, highly intermittent plumes. To navigate a plume and, for example, find food, they must solve several challenges, including reliably identifying mixtures of odorants and their intensities, and discriminating odorant mixtures emanating from a single source from odorants emitted from separate sources and just mixing in the air. Lateral inhibition in the antennal lobe is commonly understood to help solving these challenges. With a computational model of the Drosophila olfactory system, we analyze the utility of an alternative mechanism for solving them: Non-synaptic (“ephaptic”) interactions (NSIs) between olfactory receptor neurons that are stereotypically co-housed in the same sensilla. We find that NSIs improve mixture ratio detection and plume structure sensing and do so more efficiently than the traditionally considered mechanism of lateral inhibition in the antennal lobe. The best performance is achieved when both mechanisms work in synergy. However, we also found that NSIs decrease the dynamic range of co-housed ORNs, especially when they have similar sensitivity to an odorant. These results shed light, from a functional perspective, on the role of NSIs, which are normally avoided between neurons, for instance by myelination.

scholarly journals Combinations of DIPs and Dprs control organization of olfactory receptor neuron terminals in Drosophila

2018 ◽  
Author(s):  
Scott Barish ◽  
Sarah Nuss ◽  
Ilya Strunilin ◽  
Suyang Bao ◽  
Sayan Mukherjee ◽  
...  
Keyword(s):  
Axon Guidance ◽  
Olfactory Receptor ◽  
Antennal Lobe ◽  
Olfactory Receptor Neuron ◽  
Olfactory Receptor Neurons ◽  
Surface Receptors ◽  
Differential Adhesion ◽  
Receptor Neurons ◽  
Neuron Terminals ◽  
Cell Adhesion Proteins

SummaryIn Drosophila, 50 classes of olfactory receptor neurons (ORNs) connect to 50 class-specific and uniquely positioned glomeruli in the antennal lobe. Despite the identification of cell surface receptors regulating axon guidance, how ORN axons sort to form 50 stereotypical glomeruli remains unclear. Here we show that the heterophilic cell adhesion proteins, DIPs and Dprs, are expressed in ORNs during glomerular formation. Each ORN class expresses a unique combination of DIPs/dprs, with neurons of the same class expressing interacting partners, suggesting a role in class-specific self-adhesion ORN axons. Analysis of DIP/Dpr expression revealed that ORNS that target neighboring glomeruli have different combinations, and ORNs with very similar DIP/Dpr combinations can project to distant glomeruli in the antennal lobe. Perturbations of DIP/dpr gene function result in local projection defects of ORN axons and glomerular positioning, without altering correct matching of ORNs with their target neurons. Our results suggest that context-dependent differential adhesion through DIP/Dpr combinations regulate self-adhesion and sort ORN axons into uniquely positioned glomeruli.

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