Abstract
Optical imaging of intracellular Ca2+ influx as a correlate of neuronal excitation represents a standard technique for visualizing spatiotemporal activity of neuronal networks. However, the information-processing properties of single neurons and neuronal circuits likewise involve inhibition of neuronal membrane potential. Here, we report spatially resolved optical imaging of odor-evoked inhibitory patterns in the olfactory circuitry of Drosophila using a genetically encoded fluorescent Cl- sensor. In combination with the excitatory component reflected by intracellular Ca2+ dynamics, we present a comprehensive functional map of both odor-evoked neuronal activation and inhibition at different levels of olfactory processing. We demonstrate that odor-evoked inhibition carried by Cl- influx is present both in sensory neurons and second-order projection neurons, and is characterized by stereotypic, odor-specific patterns. Cl- mediated inhibition features distinct dynamics in different neuronal populations. Our data support a dual role of inhibitory neurons in the olfactory system: global gain control across the neuronal circuitry and glomerulus-specific inhibition to enhance neuronal information processing.
Significance Statement Neural inhibition is evidently as important as excitation given it is present at every level of sensory processing. This study characterizes odor-evoked inhibitory patterns along different levels of olfactory processing of Drosophila using functional imaging via Clomeleon, a genetically encoded indicator for chloride ions, the main mediator of synaptic inhibition in mature neurons. In combination with the excitatory component reflected by intracellular calcium, we analyzed the interplay between odor-evoked excitation and inhibition. Our data provide both a more accurate and comprehensive characterization of the actual information content encoded by the olfactory circuitry, as well as elucidate network properties within the primary olfactory center of the fly.
Footnotes
The authors declare no competing financial interests.
This work was supported by a BMBF grant to S.S., V.G., M.S.-B., A.R. and S.T., by the Max Planck Society, and by the German Research Foundation (SPP1392 FI-3-1 and SA 909/3-1, 3-2) to A.F. and S.S.
This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license, which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.
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