Early warning signals regarding environmental suitability in the Drosophila antenna

HighlightsA novel geotaxis assay showed high intensity odorant exposures are harmful to fliesRepulsion at high odor intensities can be a protective mechanismOlfactory receptor neuron (ORN) excitability abruptly changes with odor intensityA linear combination of ORN activities can robustly predict intensity-dependent behavioral repulsionSummaryThe olfactory system is uniquely positioned to warn an organism of environmental threats. Whether and how it encodes such information is not understood. Here, we examined this issue in the fruit fly Drosophila melanogaster. We found that intensity-dependent repulsion to chemicals safeguarded flies from harmful, high-intensity vapor exposures. To understand how sensory input changed as the odor valence switched from innocuous to threatening, we recorded from olfactory receptor neurons (ORNs) in the fly antenna. Primarily, we observed two response non-linearities: recruitment of non-active ORNs at higher intensities, and abrupt transitions in neural excitability from regular spiking to high-firing oscillatory regime. Although non-linearities observed in any single ORN was not a good indicator, a simple linear combination of firing events from multiple neurons provided robust recognition of threating/repulsive olfactory stimuli. In sum, our results reveal how information necessary to avoid environmental threats may also be encoded in the insect antenna.

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Adaptive integrate-and-fire model reproduces the dynamics of olfactory receptor neuron responses in a moth

Journal of The Royal Society Interface ◽

10.1098/rsif.2019.0246 ◽

2019 ◽

Vol 16 (157) ◽

pp. 20190246 ◽

Cited By ~ 1

Author(s):

Marie Levakova ◽

Lubomir Kostal ◽

Christelle Monsempès ◽

Philippe Lucas ◽

Ryota Kobayashi

Keyword(s):

Olfactory Receptor ◽

Time Course ◽

Olfactory Receptor Neuron ◽

Receptor Activation ◽

Olfactory Receptor Neurons ◽

Response Dynamics ◽

Spike Threshold ◽

Olfactory Stimuli ◽

Receptor Neurons ◽

The Brain

In order to understand how olfactory stimuli are encoded and processed in the brain, it is important to build a computational model for olfactory receptor neurons (ORNs). Here, we present a simple and reliable mathematical model of a moth ORN generating spikes. The model incorporates a simplified description of the chemical kinetics leading to olfactory receptor activation and action potential generation. We show that an adaptive spike threshold regulated by prior spike history is an effective mechanism for reproducing the typical phasic–tonic time course of ORN responses. Our model reproduces the response dynamics of individual neurons to a fluctuating stimulus that approximates odorant fluctuations in nature. The parameters of the spike threshold are essential for reproducing the response heterogeneity in ORNs. The model provides a valuable tool for efficient simulations of olfactory circuits.

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Trans-synaptic Fish-lips Signaling Prevents Misconnections between Non-synaptic Partner Olfactory Neurons

10.1101/600064 ◽

2019 ◽

Author(s):

Qijing Xie ◽

Bing Wu ◽

Jiefu Li ◽

Hongjie Li ◽

David J Luginbuhl ◽

...

Keyword(s):

Olfactory Receptor ◽

Neural Circuit ◽

Transmembrane Protein ◽

Fruit Fly ◽

Projection Neuron ◽

Olfactory Receptor Neuron ◽

Projection Neurons ◽

Specific Expression ◽

Cell Type Specific Expression ◽

Circuit Assembly

AbstractOur understanding of the mechanisms of neural circuit assembly is far from complete. Identification of new wiring molecules with novel mechanisms of action will provide new insights into how complex and heterogeneous neural circuits assemble during development. Here, we performed an RNAi screen for cell-surface molecules and identified the leucine-rich-repeat containing transmembrane protein, Fish-lips (Fili), as a novel wiring molecule in the assembly of the Drosophila olfactory circuit. Fili contributes to the precise targeting of both olfactory receptor neuron (ORN) axons as well as projection neuron (PN) dendrites. Cell-type-specific expression and genetic analyses suggest that Fili sends a trans-synaptic repulsive signal to neurites of non-partner classes that prevent their targeting to inappropriate glomeruli in the antennal lobe.Significance StatementIn the fruit fly olfactory system, 50 classes of olfactory receptor neurons (ORNs) make precise synaptic connections with 50 classes of corresponding projection neurons (PNs). Identification of wiring molecules in this circuit can provide insight into understanding neural circuit assembly. This paper reports the role of a transmembrane protein, Fish-lips (Fili), in forming specific connections in this circuit. We found that some ORN axons are repelled by Fili, which is present on dendrites of non-matching PN class, preventing them from targeting inappropriate glomeruli. Similarly, some PN dendrites are repelled by Fili expressed by non-matching ORN class for their correct targeting. Together, these results suggest that Fili mediates repulsion between axons and dendrites of non-synaptic partners to ensure precise wiring patterns.

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