A high-throughput behavioral paradigm for Drosophila olfaction - The Flywalk

Intraspecific olfactory signals known as pheromones play important roles in insect mating systems. In the model Drosophila melanogaster, a key part of the pheromone-detecting system has remained enigmatic through many years of research in terms of both its behavioral significance and its activating ligands. Here we show that Or47b-and Or88a-expressing olfactory sensory neurons (OSNs) detect the fly-produced odorants methyl laurate (ML), methyl myristate, and methyl palmitate. Fruitless (fru M )-positive Or47b-expressing OSNs detect ML exclusively, and Or47b-and Or47b-expressing OSNs are required for optimal male copulation behavior. In addition, activation of Or47b-expressing OSNs in the male is sufficient to provide a competitive mating advantage. We further find that the vigorous male courtship displayed toward oenocyte-less flies is attributed to an oenocyte-independent sustained production of the Or47b ligand, ML. In addition, we reveal that Or88a-expressing OSNs respond to all three compounds, and that these neurons are necessary and sufficient for attraction behavior in both males and females. Beyond the OSN level, information regarding the three fly odorants is transferred from the antennal lobe to higher brain centers in two dedicated neural lines. Finally, we find that both Or47b-and Or88a-based systems and their ligands are remarkably conserved over a number of drosophilid species. Taken together, our results close a significant gap in the understanding of the olfactory background to Drosophila mating and attraction behavior; while reproductive isolation barriers between species are created mainly by species-specific signals, the mating enhancing signal in several Drosophila species is conserved. Drosophila | pheromone | mating | olfaction | olfactory circuit I n the vinegar fly Drosophila melanogaster, cuticular hydrocarbons (CHCs) act as pheremones and play important roles in courtship and aggregation behaviors. These pheremones include the female-specific aphrodisiacs (Z,Z)-7,11-heptacosadiene (7,11-HD) and (Z,Z)-7,11-nonacosadiene (7,11-ND) and the male specific antiaphrodisiacs (Z)-7-tricosene (7-T) and 11-cis-vaccenyl acetate (cVA) (1). However, several lines of evidence suggest that other unidentified pheromones likely contribute to courtship and aggregation behaviors. Previous studies have demonstrated that an unidentified volatile sex pheromone produced by female flies stimulates male courtship (2-6). Flies anosmic to cVA exhibit residual attraction to live male flies, suggesting that other attractive cues are produced by flies that are independent of cVA and its neural circuit (7). Furthermore, no specific ligands other than cVA have been identified for the potential pheromone receptors expressed in OSNs of antennal trichoid sensilla (8). Moreover, OSNs expressing olfactory receptors Or47a and Or88a housed in trichoid sensilla respond to unidentified odors in male and female body wash extracts (9).Although the CHC profile of D. melanogaster has been characterized by several analytical techniq...

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“…4A). Furthermore, pulses of ML presented in the FlyWalk assay (38,39) were attractive to both males and females (Fig. 4B).…”

Section: Vigorous Courtship Toward Oenocyte-less Flies Is Due To Sustmentioning

confidence: 99%

Pheromones mediating copulation and attraction in Drosophila

Dweck¹,

Ebrahim²,

Thoma³

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

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“…For all behavioural experiments, ethyl acetate, a known attractant odour (Steck et al, 2012), was used. Flywalk experiments were performed and raw data was pre-processed as described elsewhere (Steck et al, 2012).…”

Section: Behavioural Assaysmentioning

confidence: 99%

Intracellular regulation of the insect chemoreceptor complex impacts odor localization in flying insects

Getahun

Thoma

Lavista-Llanos

et al. 2016

Journal of Experimental Biology

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Flying insects are well known for airborne odour tracking and have evolved diverse chemoreceptors. While ionotropic receptors (IRs) are found across protostomes, insect odorant receptors (ORs) have only been identified in winged insects. We therefore hypothesized that the unique signal transduction of ORs offers an advantage for odour localization in flight. Using Drosophila, we found expression and increased activity of the intracellular signalling protein PKC in antennal sensilla following odour stimulation. Odour stimulation also enhanced phosphorylation of the OR co-receptor Orco in vitro, while site-directed mutation of Orco or mutations in PKC subtypes reduced the sensitivity and dynamic range of OR-expressing neurons in vivo, but not IR-expressing neurons. We ultimately show that these mutations reduce competence for odour localization of flies in flight. We conclude that intracellular regulation of OR sensitivity is necessary for efficient odour localization, which suggests a mechanistic advantage for the evolution of the OR complex in flying insects.

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“…In insects, assays and highthroughput methodologies can be applied for measuring odor attractiveness (Steck et al, 2012). Recently, large-scale psychophysics studies have been applied in humans (Keller et al, 2012), and it is to hope that more studies will go in a similar direction.…”

Section: Discussionmentioning

confidence: 99%

Understanding smell—The olfactory stimulus problem

Auffarth

2013

Neuroscience & Biobehavioral Reviews

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Please cite this article as: Auffarth, B., Understanding smell -the olfactory stimulus problem, Neuroscience and Biobehavioral Reviews (2013), http://dx.doi.org/10.1016/j.neubiorev.2013.06.009. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.Page 1 of 27 A c c e p t e d M a n u s c r i p t -For the olfactory system, a topographic organization is disputed. -However, work on different species suggests a topography in olfaction.-We compare other modalities such as taste and color vision.-We discuss the utility of a categorization of smell perception. *Highlights (for review)Page 2 of 27 A c c e p t e d M a n u s c r i p t 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60 61 62 63 64 65 Neuroscience and Biobehavioral Reviews The main problem with sensory processing is the difficulty in relating sensory input to physiological responses and perception. This is especially problematic at higher levels of processing, where complex cues elicit highly specific responses. In olfaction, this relationship is particularly obfuscated by the difficulty of characterizing stimulus statistics and perception. The core questions in olfaction are hence the so-called stimulus problem, which refers to the understanding of the stimulus, and the structure-activity and structure-odor relationships, which refer to the molecular basis of smell. It is widely accepted that the recognition of odorants by receptors is governed by the detection of physico-chemical properties and that the physical space is highly complex. Not surprisingly, ideas differ about how odor stimuli should be classified and about the very nature of information that the brain extracts from odors. Even though there are many measures for smell, there is none that accurately describes all aspects of it. Here, we summarize recent developments in the understanding of olfaction. We argue that an approach to olfactory function where information processing is emphasized could contribute to a high degree to our understanding of smell as a perceptual phenomenon emerging from neural computations. Further, we argue that combined analysis of the stimulus, biology, physiology, and behavior and perception can provide new insights into olfactory function. We hope that the reader can use this review as a competent guide and overview of research activities in olfactory physiology, psychophysics, computation, and psychology. We propose avenues for research, particularly in the systematic characteriza...

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A high-throughput behavioral paradigm for Drosophila olfaction - The Flywalk

Cited by 86 publications

References 26 publications

Pheromones mediating copulation and attraction in Drosophila

Pheromones mediating copulation and attraction in Drosophila

Intracellular regulation of the insect chemoreceptor complex impacts odor localization in flying insects

Understanding smell—The olfactory stimulus problem

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