High Precision of Spike Timing across Olfactory Receptor Neurons Allows Rapid Odor Coding in  Drosophila

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Summary

In recent years, it has become evident that olfaction is a fast sense, and millisecond short differences in stimulus onsets are used by animals to analyze their olfactory environment. In contrast, olfactory receptor neurons are thought to be relatively slow and temporally imprecise. These observations have led to a conundrum: how, then, can an animal resolve fast stimulus dynamics and smell with high temporal acuity? Using parallel recordings from olfactory receptor neurons in Drosophila, we found hitherto unknown fast and temporally precise odorant-evoked spike responses, with first spike latencies (relative to odorant arrival) down to 3 ms and with a SD below 1 ms. These data provide new upper bounds for the speed of olfactory processing and suggest that the insect olfactory system could use the precise spike timing for olfactory coding and computation, which can explain insects' rapid processing of temporal stimuli when encountering turbulent odor plumes.

Graphical Abstract

Highlights

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Olfactory receptor neuron responses are fast and temporally precise
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Odor-evoked spikes can occur 3 ms after odorant arrival and jitter less than 1 ms
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First-spike timing varies over a wider concentration range than spike rate
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Neural network model demonstrates the plausibility of a spike-timing code for odors

Abstract

Cellular Physiology; Neuroscience; Sensory Neuroscience

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Most cited references 52

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Insect olfactory receptors are heteromeric ligand-gated ion channels.

Koji Sato, Maurizio Pellegrino, Takao Nakagawa … (2008)

In insects, each olfactory sensory neuron expresses between one and three ligand-binding members of the olfactory receptor (OR) gene family, along with the highly conserved and broadly expressed Or83b co-receptor. The functional insect OR consists of a heteromeric complex of unknown stoichiometry but comprising at least one variable odorant-binding subunit and one constant Or83b family subunit. Insect ORs lack homology to G-protein-coupled chemosensory receptors in vertebrates and possess a distinct seven-transmembrane topology with the amino terminus located intracellularly. Here we provide evidence that heteromeric insect ORs comprise a new class of ligand-activated non-selective cation channels. Heterologous cells expressing silkmoth, fruitfly or mosquito heteromeric OR complexes showed extracellular Ca2+ influx and cation-non-selective ion conductance on stimulation with odorant. Odour-evoked OR currents are independent of known G-protein-coupled second messenger pathways. The fast response kinetics and OR-subunit-dependent K+ ion selectivity of the insect OR complex support the hypothesis that the complex between OR and Or83b itself confers channel activity. Direct evidence for odorant-gated channels was obtained by outside-out patch-clamp recording of Xenopus oocyte and HEK293T cell membranes expressing insect OR complexes. The ligand-gated ion channel formed by an insect OR complex seems to be the basis for a unique strategy that insects have acquired to respond to the olfactory environment.

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Drosophila odorant receptors are both ligand-gated and cyclic-nucleotide-activated cation channels.

Dieter Wicher, Ronny Schäfer, René Bauernfeind … (2008)

From worm to man, many odorant signals are perceived by the binding of volatile ligands to odorant receptors that belong to the G-protein-coupled receptor (GPCR) family. They couple to heterotrimeric G-proteins, most of which induce cAMP production. This second messenger then activates cyclic-nucleotide-gated ion channels to depolarize the olfactory receptor neuron, thus providing a signal for further neuronal processing. Recent findings, however, have challenged this concept of odorant signal transduction in insects, because their odorant receptors, which lack any sequence similarity to other GPCRs, are composed of conventional odorant receptors (for example, Or22a), dimerized with a ubiquitously expressed chaperone protein, such as Or83b in Drosophila. Or83b has a structure akin to GPCRs, but has an inverted orientation in the plasma membrane. However, G proteins are expressed in insect olfactory receptor neurons, and olfactory perception is modified by mutations affecting the cAMP transduction pathway. Here we show that application of odorants to mammalian cells co-expressing Or22a and Or83b results in non-selective cation currents activated by means of an ionotropic and a metabotropic pathway, and a subsequent increase in the intracellular Ca(2+) concentration. Expression of Or83b alone leads to functional ion channels not directly responding to odorants, but being directly activated by intracellular cAMP or cGMP. Insect odorant receptors thus form ligand-gated channels as well as complexes of odorant-sensing units and cyclic-nucleotide-activated non-selective cation channels. Thereby, they provide rapid and transient as well as sensitive and prolonged odorant signalling.

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Odor coding in the Drosophila antenna.

M. de Bruyne, K Foster, J Carlson (2001)

Odor coding in the Drosophila antenna is examined by a functional analysis of individual olfactory receptor neurons (ORNs) in vivo. Sixteen distinct classes of ORNs, each with a unique response spectrum to a panel of 47 diverse odors, are identified by extracellular recordings. ORNs exhibit multiple modes of response dynamics: an individual neuron can show either excitatory or inhibitory responses, and can exhibit different modes of termination kinetics, when stimulated with different odors. The 16 ORN classes are combined in stereotyped configurations within seven functional types of basiconic sensilla. One sensillum type contains four ORNs and the others contain two neurons, combined according to a strict pairing rule. We provide a functional map of ORNs, showing that each ORN class is restricted to a particular spatial domain on the antennal surface.

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Author and article information

Contributors

Paul Szyszka

Journal

Journal ID (nlm-ta): iScience

Journal ID (iso-abbrev): iScience

Title: iScience

Publisher: Elsevier

ISSN (Electronic): 2589-0042

Publication date PMC-release: 17 May 2018

Publication date Collection: 29 June 2018

Publication date (Electronic): 17 May 2018

Volume: 4

Pages: 76-83

Affiliations

[1 ]University of Konstanz, Department of Biology, Neurobiology, Konstanz 78457, Germany

[2 ]Institute of Neuroinformatics, University of Zurich and ETH Zurich, Zürich 8057, Switzerland

Author notes

[∗ ]Corresponding author paul.szyszka@ 123456uni-konstanz.de

[3]

These authors contributed equally

[4]

Lead Contact

Article

Publisher ID: S2589-0042(18)30064-6

DOI: 10.1016/j.isci.2018.05.009

PMC ID: 6147046

PubMed ID: 30240755

SO-VID: 2ac462f9-c0b2-4564-a70d-4d0212c0fe45

License:

This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).

History

Date received : 7 March 2018

Date revision received : 19 April 2018

Date accepted : 14 May 2018

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High Precision of Spike Timing across Olfactory Receptor Neurons Allows Rapid Odor Coding in Drosophila

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