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Research ArticleNew Research, Sensory and Motor Systems

Presynaptic GABA Receptors Mediate Temporal Contrast Enhancement in Drosophila Olfactory Sensory Neurons and Modulate Odor-Driven Behavioral Kinetics

Davide Raccuglia, Li Yan McCurdy, Mahmut Demir, Srinivas Gorur-Shandilya, Michael Kunst, Thierry Emonet and Michael N. Nitabach
eNeuro 25 July 2016, 3 (4) ENEURO.0080-16.2016; DOI: https://doi.org/10.1523/ENEURO.0080-16.2016
Davide Raccuglia
1Department of Cellular and Molecular Physiology, Yale University School of Medicine, New Haven, Connecticut 06520
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Li Yan McCurdy
1Department of Cellular and Molecular Physiology, Yale University School of Medicine, New Haven, Connecticut 06520
2Interdepartmental Neuroscience Program, Yale University, New Haven, Connecticut 06520
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Mahmut Demir
3Department of Molecular, Cellular and Developmental Biology, Yale University, New Haven, Connecticut 06520
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Srinivas Gorur-Shandilya
2Interdepartmental Neuroscience Program, Yale University, New Haven, Connecticut 06520
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Michael Kunst
1Department of Cellular and Molecular Physiology, Yale University School of Medicine, New Haven, Connecticut 06520
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Thierry Emonet
3Department of Molecular, Cellular and Developmental Biology, Yale University, New Haven, Connecticut 06520
4Department of Physics, Yale University, New Haven, Connecticut 06520
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Michael N. Nitabach
1Department of Cellular and Molecular Physiology, Yale University School of Medicine, New Haven, Connecticut 06520
5Department of Genetics, Yale University School of Medicine, New Haven, Connecticut 06520
6Program in Cellular Neuroscience, Neurodegeneration and Repair, Yale University School of Medicine, New Haven, Connecticut 06520
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Abstract

Contrast enhancement mediated by lateral inhibition within the nervous system enhances the detection of salient features of visual and auditory stimuli, such as spatial and temporal edges. However, it remains unclear how mechanisms for temporal contrast enhancement in the olfactory system can enhance the detection of odor plume edges during navigation. To address this question, we delivered to Drosophila melanogaster flies pulses of high odor intensity that induce sustained peripheral responses in olfactory sensory neurons (OSNs). We use optical electrophysiology to directly measure electrical responses in presynaptic terminals and demonstrate that sustained peripheral responses are temporally sharpened by the combined activity of two types of inhibitory GABA receptors to generate contrast-enhanced voltage responses in central OSN axon terminals. Furthermore, we show how these GABA receptors modulate the time course of innate behavioral responses after odor pulse termination, demonstrating an important role for temporal contrast enhancement in odor-guided navigation.

Footnotes

  • The authors declare no competing financial interests.

  • Work in the laboratory of M.N.N. was supported in part by the National Institute of Neurological Disorders and Stroke, the National Institutes of Health (NIH; Grants R01-NS-055035, R01-NS-056443, and R01-NS-091070); the National Institute of General Medical Sciences (NIGMS), NIH (Grant R01GM098931); and the Kavli Institute for Neuroscience. L.Y.M. was supported by a Gruber Science Fellowship and NIGMS, NIH (Grant T32GM007223).

This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International, which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.

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July/August 2016
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Presynaptic GABA Receptors Mediate Temporal Contrast Enhancement in Drosophila Olfactory Sensory Neurons and Modulate Odor-Driven Behavioral Kinetics
Davide Raccuglia, Li Yan McCurdy, Mahmut Demir, Srinivas Gorur-Shandilya, Michael Kunst, Thierry Emonet, Michael N. Nitabach
eNeuro 25 July 2016, 3 (4) ENEURO.0080-16.2016; DOI: 10.1523/ENEURO.0080-16.2016

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Presynaptic GABA Receptors Mediate Temporal Contrast Enhancement in Drosophila Olfactory Sensory Neurons and Modulate Odor-Driven Behavioral Kinetics
Davide Raccuglia, Li Yan McCurdy, Mahmut Demir, Srinivas Gorur-Shandilya, Michael Kunst, Thierry Emonet, Michael N. Nitabach
eNeuro 25 July 2016, 3 (4) ENEURO.0080-16.2016; DOI: 10.1523/ENEURO.0080-16.2016
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