Shaping Sensory Perception in Time: A Mechanism for Temporal Contrast Enhancement of Olfactory Information

Material below summarizes the article, Presynaptic GABA Receptors Mediate Temporal Contrast Enhancement in Drosophila Olfactory Sensory Neurons and Modulate Odor-Driven Behavioral Kinetics, published on July 25, 2016, in eNeuro and authored by Davide Raccuglia, Li Yan McCurdy, Mahmut Demir, Srinivas Gorur-Shandilya, Michael Kunst, Thierry Emonet, and Michael N. Nitabach.

The way we perceive the world around us depends on the proper balance and integration of excitatory and inhibitory inputs in neuronal networks that process specific sensory stimuli.

In the visual system, lateral inhibition improves environmental perception by enhancing contrast vision. Besides shaping our perception in the spatial dimensions, contrast enhancement also occurs in the temporal dimension. Temporal edge detection in the auditory system, for example, improves sound localization.

In our paper, we address whether temporal contrast enhancement that improves the temporal perception of fluctuating olfactory information exists in the olfactory system.

The antennal lobe in insects is remarkably similar to the olfactory bulb in mammals. Lateral inhibition in these structures has been studied in mammals and in various insects, including locusts, honey bees, hawkmoths, and fruit flies. In the fruit fly Drosophila melanogaster, it has been shown that presynaptic GABA receptors of olfactory sensory neurons (OSNs) play a crucial role in mediating lateral inhibition and modulating odor-guided behavior.

By combining classical and optical electrophysiology, we find that high-intensity odor pulses induce sustained peripheral activity in dendrites and cell bodies of OSNs. Using ArcLight to measure electrical responses in the presynaptic terminals, we find that the sustained peripheral responses undergo temporal contrast enhancement by presynaptic GABA receptors to generate sharper responses in OSN presynaptic axon terminals in the antennal lobe. Using pharmacological blockage of GABA receptors and cell-specific RNAi-mediated knockdown of GABA receptor expression, we demonstrate that the temporal sharpening of odor-induced neuronal activity in OSN presynaptic terminals is mediated by the combined activity of inhibitory ionotropic and metabotropic GABA receptors.

Although it was previously shown that presynaptic inhibition in Drosophila OSNs is mediated by ionotropic (GABAA) and metabotropic (GABAB) GABA receptors, a role for odor-guided behavior has only been shown for GABAB receptors. Fruit flies can display innate behavior to different odors: They are attracted by some odors and repelled by others.

To test the flies’ behavior when confronted with different intensities of the fruity odor ethyl butyrate, we tracked locomotor responses of walking flies. We find that RNAi-mediated knockdown of GABAA receptors and to an even stronger degree the simultaneous knockdown of GABAA and GABAB receptors in OSNs expressing the olfactory receptor OR22a increases avoidance to ethyl butyrate. This demonstrates that the combined activity of GABAA and GABAB receptors in OSNs modulates odor-driven innate behavioral responses.

To test whether the combined activity of presynaptic GABA receptors in OSNs affects the temporal perception of a transient odor stimulus, we delivered 1 s odor pulses and focused on behavioral responses after the odor pulse. We find that the combined RNAi-mediated knockdown of GABAA and GABAB receptors in OSNs expressing the olfactory receptor OR22a prolongs avoidance after the termination of the odor pulse. Thus, the combined activity of GABAA and GABAB receptors in OSNs can mediate temporal contrast enhancement and improve temporal edge detection of olfactory stimuli.

Drosophila melanogaster live, feed, and reproduce on fermenting fruits. To locate fermenting fruit, Drosophila navigate via plumes of odors. In this paper, we demonstrate a mechanism that enhances the temporal contrast within the antennal lobe to improve the detection of the temporal dynamics of odor plumes. The combined role of GABAA and GABAB receptors which mediate both gain control and temporal contrast enhancement in OSNs could be an advantage for animals that encounter a very wide dynamic range of odor stimuli. Future studies are required to probe the role of this mechanism in actual plume-guided navigation. 

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Presynaptic GABA Receptors Mediate Temporal Contrast Enhancement in Drosophila Olfactory Sensory Neurons and Modulate Odor-Driven Behavioral Kinetics, published on July 25, 2016, in eNeuro and authored by Davide Raccuglia, Li Yan McCurdy, Mahmut Demir, Srinivas Gorur-Shandilya, Michael Kunst, Thierry Emonet, Michael N. Nitabach.

About the Contributor

Davide Raccuglia, PhD

Davide Raccuglia conducted the work for this paper while in the department of cellular and molecular physiology at Yale University School of Medicine. He is currently a research scientist at the Institute of Neurophysiology at the Charité in Berlin, Germany.