Third-Order Neurons in the Lateral Horn Enhance Bilateral Contrast of Odor Inputs Through Contralateral Inhibition in Drosophila.

Ahmed A M Mohamed,Bill S Hansson,Silke Sachse

doi:10.3389/fphys.2019.00851

Ahmed A M Mohamed, Bill S Hansson + Show 1 more

Open Access

https://doi.org/10.3389/fphys.2019.00851

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Abstract

The survival and reproduction of Drosophila melanogaster depends heavily on its ability to determine the location of an odor source and either to move toward or away from it. Despite the very small spatial separation between the two antennae and the redundancy in sensory neuron projection to both sides of the brain, Drosophila can resolve the concentration gradient by comparing the signal strength between the two antennae. When an odor stimulates the antennae asymmetrically, ipsilateral projection neurons from the first olfactory center are more strongly excited compared to the contralateral ones. However, it remains elusive how higher-order neurons process such asymmetric or lateralized odor inputs. Here, we monitored and analyzed for the first time the activity patterns of a small cluster of third-order neurons (so-called ventrolateral protocerebrum neurons) to asymmetric olfactory stimulation using two-photon calcium imaging. Our data demonstrate that lateralized odors evoke distinct activation of these neurons in the left and right brain hemisphere as a result of contralateral inhibition. Moreover, using laser transection experiments we show that this contralateral inhibition is mediated by presynaptic neurons most likely located in the lateral horn. Finally, we propose that this inhibitory interaction between higher-order neurons facilitates odor lateralization and plays a crucial role in olfactory navigation behavior of Drosophila, a theory that needs to be experimentally addressed in future studies.

Highlights

Chemotaxis is important for the survival of many animals since chemicals that are emitted by the environment can be exploited as cues for potentially positive or negative interactions
In order to study how lateralized odors are processed by higher-order neurons, we investigated the neuronal responses of a specific cluster of LHONs, so-called ventrolateral protocerebrum (VLP) neurons, to asymmetric and symmetric odor stimulations using two-photon functional imaging
Ventrolateral protocerebrum neurons have their postsynaptic dendrites in the lateral horn (LH) and send their axonal terminals to the VLP, where they synapse onto further higher-order neurons (Figures 1A,B)

Summary

Introduction

Chemotaxis is important for the survival of many animals since chemicals that are emitted by the environment can be exploited as cues for potentially positive (e.g., food, mate, or oviposition site) or negative (toxicity, competitors, predators, or parasitoids) interactions. One of the most used strategies is to detect an odor gradient across the two antennae by comparing their signal strength, and to turn toward or away from the stronger olfactory signal, a phenomenon termed “osmotropotaxis” (Martin, 1965; Hangartner, 1967; Kennedy and Moorhouse, 1969) Confusing this strategy, by spatially reversing the antennae (i.e., by crossing and fixing them), impairs chemotaxis as shown in bees, ants, and locusts (Martin, 1965; Hangartner, 1967; Kennedy and Moorhouse, 1969). The vinegar fly Drosophila melanogaster uses the same strategy to navigate

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