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1.  Functional classification and central nervous projections of olfactory receptor neurons housed in antennal trichoid sensilla of female yellow fever mosquitoes, Aedes aegypti 
The European Journal of Neuroscience  2007;26(6):1611-1623.
Mosquitoes are highly dependent on their olfactory system for, e.g. host location and identification of nectar-feeding and oviposition sites. Odours are detected by olfactory receptor neurons (ORNs) housed in hair-shaped structures, sensilla, on the antennae and maxillary palps. In order to unravel the function of the olfactory system in the yellow fever vector, Aedes aegypti, we performed single-sensillum recordings from trichoid sensilla on female antennae. These sensilla are divided into four distinct morphological types. Based on the response to a set of 16 odour compounds, we identified 18 different ORN types, housed in 10 sensillum types. The ORNs responded to behaviourally relevant olfactory cues, such as oviposition attractants and sweat-borne compounds, including 4-methylcyclohexanol and indole, respectively. Two ORNs housed in these sensilla, as well as two ORNs housed in an additional sensillum type, did not respond to any of the compounds tested. The ORNs housed in individual sensilla exhibited stereotypical pairing and displayed differences in signalling mode (excitatory and inhibitory) as well as in temporal response patterns. In addition to physiological characterization, we performed anterograde neurobiotin stainings of functionally identified ORNs in order to define the functional map among olfactory glomeruli in the primary olfactory centre, the antennal lobe. The targeted glomeruli were compared with an established 3D map. Our data showed that the ORN types sent their axons to defined antennal lobe glomeruli in a stereotypic pattern.
PMCID: PMC2121139  PMID: 17880395
Aedes aegypti; antennal sensilla; olfaction; ORNs; physiology
2.  Moth Sex Pheromone Receptors and Deceitful Parapheromones 
PLoS ONE  2012;7(7):e41653.
The insect's olfactory system is so selective that male moths, for example, can discriminate female-produced sex pheromones from compounds with minimal structural modifications. Yet, there is an exception for this “lock-and-key” tight selectivity. Formate analogs can be used as replacement for less chemically stable, long-chain aldehyde pheromones, because male moths respond physiologically and behaviorally to these parapheromones. However, it remained hitherto unknown how formate analogs interact with aldehyde-sensitive odorant receptors (ORs). Neuronal responses to semiochemicals were investigated with single sensillum recordings. Odorant receptors (ORs) were cloned using degenerate primers, and tested with the Xenopus oocyte expression system. Quality, relative quantity, and purity of samples were evaluated by gas chromatography and gas chromatography-mass spectrometry. We identified olfactory receptor neurons (ORNs) housed in trichoid sensilla on the antennae of male navel orangeworm that responded equally to the main constituent of the sex pheromone, (11Z,13Z)-hexadecadienal (Z11Z13-16Ald), and its formate analog, (9Z,11Z)-tetradecen-1-yl formate (Z9Z11-14OFor). We cloned an odorant receptor co-receptor (Orco) and aldehyde-sensitive ORs from the navel orangeworm, one of which (AtraOR1) was expressed specifically in male antennae. AtraOR1•AtraOrco-expressing oocytes responded mainly to Z11Z13-16Ald, with moderate sensitivity to another component of the sex pheromone, (11Z,13Z)-hexadecadien-1-ol. Surprisingly, this receptor was more sensitive to the related formate than to the natural sex pheromone. A pheromone receptor from Heliothis virescens, HR13 ( = HvirOR13) showed a similar profile, with stronger responses elicited by a formate analog than to the natural sex pheromone, (11Z)-hexadecenal thus suggesting this might be a common feature of moth pheromone receptors.
PMCID: PMC3401280  PMID: 22911835
3.  The CCHamide 1 receptor modulates sensory perception and olfactory behavior in starved Drosophila 
Scientific Reports  2013;3:2765.
The olfactory response of the vinegar fly Drosophila melanogaster to food odor is modulated by starvation. Here we show that this modulation is not restricted to food odors and their detecting sensory neurons but rather increases the behavioral response to odors as different as food odors, repellents and pheromones. The increased behavioral responsiveness is paralleled by an increased physiological sensitivity of sensory neurons regardless whether they express olfactory or ionotropic receptors and regardless whether they are housed in basiconic, coeloconic, or trichoid sensilla. Silencing several genes that become up-regulated under starvation confirmed the involvement of the short neuropeptide f receptor in the starvation effect. In addition it revealed that the CCHamide-1 receptor is another important factor governing starvation-induced olfactory modifications.
PMCID: PMC3783891  PMID: 24067446
4.  Reverse and Conventional Chemical Ecology Approaches for the Development of Oviposition Attractants for Culex Mosquitoes 
PLoS ONE  2008;3(8):e3045.
Synthetic mosquito oviposition attractants are sorely needed for surveillance and control programs for Culex species, which are major vectors of pathogens causing various human diseases, including filariasis, encephalitis, and West Nile encephalomyelitis. We employed novel and conventional chemical ecology approaches to identify potential attractants, which were demonstrated in field tests to be effective for monitoring populations of Cx. p. quinquefasciatus in human dwellings. Immunohistochemistry studies showed that an odorant-binding protein from this species, CquiOBP1, is expressed in trichoid sensilla on the antennae, including short, sharp-tipped trichoid sensilla type, which house an olfactory receptor neuron sensitive to a previously identified mosquito oviposition pheromone (MOP), 6-acetoxy-5-hexadecanolide. CquiOBP1 exists in monomeric and dimeric forms. Monomeric CquiOBP1 bound MOP in a pH-dependent manner, with a change in secondary structure apparently related to the loss of binding at low pH. The pheromone antipode showed higher affinity than the natural stereoisomer. By using both CquiOBP1 as a molecular target in binding assays and gas chromatography-electroantennographic detection (GC-EAD), we identified nonanal, trimethylamine (TMA), and skatole as test compounds. Extensive field evaluations in Recife, Brazil, a region with high populations of Cx. p. quinquefasciatus, showed that a combination of TMA (0.9 µg/l) and nonanal (0.15 ng/µl) is equivalent in attraction to the currently used infusion-based lure, and superior in that the offensive smell of infusions was eliminated in the newly developed synthetic mixture.
PMCID: PMC2516325  PMID: 18725946
5.  The Blunt Trichoid Sensillum of Female Mosquitoes, Anopheles gambiae: Odorant Binding Protein and Receptor Types 
In order to find a blood host and to select appropriate oviposition sites female Anopheles gambiae mosquitoes rely on olfactory cues which are sensed by olfactory sensory neurons (OSNs) located within morphologically different sensilla hairs. While the sharp type trichoid sensilla are most abundant and intensely studied, the striking blunt type trichoid sensilla exist only in small numbers and their specific function is unknown. It has been suggested that they may play a role in the detection of chemical cues indicating oviposition sites. With the aim of identifying molecular elements in blunt type trichoid sensilla, which may be relevant for chemosensory function of this sensillum type, experiments were performed which include whole mount fluorescence in situ hybridization (WM-FISH) and fluorescence immunohistochemistry (WM-FIHC). The studies were concentrated on odorant binding proteins (AgOBPs) and odorant receptors (AgORs). WM-FISH approaches using a probe for the plus-C class AgOBP47 led to the labeling of cells, which resembled in number and antennal distribution pattern the blunt type trichoid sensilla. Moreover, WM-FIHC with an antiserum for AgOBP47 allowed to assign the AgOBP47-expressing cells to blunt type trichoid sensilla and to allocate the protein within the sensillum hair shafts. The result of double WM-FISH-experiments and combined WM-FIHC/FISH approaches indicated that the AgOBP47-expressing cells are co-localized with cells, which express AgOR11, AgOR13 and AgOR55. In addition, it turned out that the two receptor types AgOR13 and AgOR55 are co-expressed in the same cells. Together, the results indicate that the blunt type trichoid sensilla contain a characteristic binding protein, plus-C AgOBP47, in the sensillum lymph and two sensory neurons, one cell which express the odorant receptor AgOR11 and a second cell which express the receptor types AgOR13 and AgOR55. The expression of characteristic chemosensory elements in blunt type trichoid sensilla supports the notion that this sensillum type is involved in sensing distinct odorous compounds.
PMCID: PMC3979995  PMID: 24719560
olfaction; odorant receptor proteins; odorant binding proteins; mRNA expression.
6.  Olfactory Processing and Behavior Downstream from Highly Selective Receptor Neurons 
Nature neuroscience  2007;10(5):623-630.
In either the vertebrate nose or the insect antenna, most olfactory receptor neurons (ORNs) respond to multiple odors. However, some ORNs respond to just a single odor, or at most to a few highly related odors. It has been hypothesized that narrowly-tuned ORNs project to narrowly-tuned neurons in the brain, and that these dedicated circuits mediate innate behavioral responses to a particular ligand. Here we have investigated neural activity and behavior downstream from two narrowly-tuned ORN types in Drosophila. We found that genetically ablating either of these ORN types impairs innate behavioral attraction to their cognate ligand. Neurons in the antennal lobe postsynaptic to one of these ORN types are, like their presynaptic ORNs, narrowly tuned to a pheromone. However, neurons postsynaptic to the second ORN type are broadly tuned. These results demonstrate that some narrowly-tuned ORNs project to dedicated central circuits, ensuring a tight connection between stimulus and behavior, whereas others project to central neurons which participate in the ensemble representations of many odors.
PMCID: PMC2838507  PMID: 17417635
7.  Activation of the T1 Neuronal Circuit is Necessary and Sufficient to Induce Sexually Dimorphic Mating Behavior in Drosophila 
The molecular and cellular events mediating complex behaviors in animals are largely unknown. Elucidating the circuits underlying behaviors in simple model systems may shed light on how these circuits function. In Drosophila, courtship behavior provides a tractable model for studying the underlying basis of innate behavior. The male-specific pheromone 11-cis-vaccenyl acetate (cVA) modulates courtship behavior and is detected by T1 neurons, located on the antenna of male and female flies. The T1 neurons express the odorant receptor Or67d, and are exquisitely tuned to cVA pheromone. However, cVA-induced changes in mating behavior have also been reported upon manipulation of olfactory neurons expressing odorant receptor Or65a. These findings raise the issue of whether multiple olfactory-driven circuits underlie cVA-induced behavioral responses, and what role these circuits play in behavior. Here, we engineered flies in which the Or67d circuit is specifically activated in the absence of cVA in order to determine the role of this circuit in behavior. We created transgenic flies that express a dominant-active, pheromone-independent variant of the extracellular pheromone receptor, LUSH. We found that, similar to the behaviors elicited by cVA, engineered male flies have dramatically reduced courtship, while engineered females showed enhanced courtship. Furthermore, cVA exposure did not enhance the dominant LUSH-triggered effects on behavior in the engineered flies. Finally, we show the effects of both cVA and dominant LUSH on courtship are reversed by genetically removing Or67d. These findings demonstrate that the T1/Or67d circuit is necessary and sufficient to mediate sexually dimorphic courtship behaviors.
PMCID: PMC3426441  PMID: 20164344
lush; Or67d; cVA; courtship; pheromone; olfaction
8.  Spike amplitude of single unit responses in antennal sensillae is controlled by the Drosophila circadian clock 
Current biology : CB  2008;18(11):803-807.
Oscillators in olfactory sensory neurons (OSNs) are both necessary and sufficient to sustain rhythms in electroanntenogram (EAG) responses, which suggests that odorant receptors (ORs) and/or OR-dependent processes are under clock control. Since EAGs have limited spatial resolution and do not necessarily reflect firing of action potentials, we measured single unit responses in different antennal sensillae from wild-type, clock mutant, odorant receptor mutant, and G-protein coupled receptor kinase 2 (Gprk2) mutant flies to examine the cellular and molecular mechanisms that drive rhythms in olfaction. Spontaneous spike amplitude, but not spontaneous or odor induced firing frequency, is under clock control in ab1 and ab3 basiconic sensillae and T2 trichoid sensillae. Mutants lacking odorant receptors in dendrites display constant low spike amplitudes, and reducing or increasing levels of GPRK2 in OSNs results in constant low or high spontaneous spike amplitudes, respectively, in ab1, ab3 and T2 sensillae. We conclude that spike amplitude is controlled by circadian clocks in basiconic and trichoid sensillae, and requires GPRK2 expression and the presence of functional ORs in dendrites. These results argue that rhythms in GPRK2 levels control OR localization and OR-dependent ion channel activity/composition to mediate rhythms in spontaneous spike amplitude.
PMCID: PMC2474768  PMID: 18499459
9.  The smell of love in Drosophila 
Odors are key sensory signals for social communication and food search in animals including insects. Drosophila melanogaster, is a powerful neurogenetic model commonly used to reveal molecular and cellular mechanisms involved in odorant detection. Males use olfaction together with other sensory modalities to find their mates. Here, we review known olfactory signals, their related olfactory receptors, and the corresponding neuronal architecture impacting courtship. OR67d receptor detects 11-cis-Vaccenyl Acetate (cVA), a male specific pheromone transferred to the female during copulation. Transferred cVA is able to reduce female attractiveness for other males after mating, and is also suspected to decrease male-male courtship. cVA can also serve as an aggregation signal, maybe through another OR. OR47b was shown to be activated by fly odors, and to enhance courtship depending on taste pheromones. IR84a detects phenylacetic acid (PAA) and phenylacetaldehyde (PA). These two odors are not pheromones produced by flies, but are present in various fly food sources. PAA enhances male courtship, acting as a food aphrodisiac. Drosophila males have thus developed complementary olfactory strategies to help them to select their mates.
PMCID: PMC3617446  PMID: 23576993
courtship; Drosophila; olfaction; receptor; nervous system
10.  Morphological characterization of the antennal sensilla of t he earwig Anisolabis maritima (Dermaptera: Carcinophoridae) with reference to their probable functions 
The earwig, Anisolabis maritima (Dermaptera: Carcinophoridae), is one of the most significant insects in KSA because, it was recorded in Saudi Arabia as a beneficial predator on eggs and newly hatched larvae of the red palm weevil, Rhyncophorus ferrugineus. We examined the external morphology of the antennal sensilla of males and females of A. maritima using scanning electron microscopy (SEM). The filiform antennae of A. maritima were of the conventional type comprising a basal scape, pedicle and a long, thread-like flagellum, which was composed of 12 flagellomeres of males and 16 flagellomeres of females. Six morphologically unique sensillar types were found and described on the antennae of males and females of A. maritima. Of those identified, there were three types of porous trichoid sensilla (long, curved and arcuate), and two types of basiconic sensilla (short and curved), and one type of aporous trichoid sensilla. The shape, external morphology and array of sensilla on the antennae of males and females of A. maritima were similar.
PMCID: PMC3730710  PMID: 23961038
Earwig; Anisolabis maritima; Sensilla; Antennae; Scanning electron microscopy
11.  A carboxylesterase, Esterase-6, modulates sensory physiological and behavioral response dynamics to pheromone in Drosophila 
BMC Biology  2012;10:56.
Insects respond to the spatial and temporal dynamics of a pheromone plume, which implies not only a strong response to 'odor on', but also to 'odor off'. This requires mechanisms geared toward a fast signal termination. Several mechanisms may contribute to signal termination, among which odorant-degrading enzymes. These enzymes putatively play a role in signal dynamics by a rapid inactivation of odorants in the vicinity of the sensory receptors, although direct in vivo experimental evidences are lacking. Here we verified the role of an extracellular carboxylesterase, esterase-6 (Est-6), in the sensory physiological and behavioral dynamics of Drosophila melanogaster response to its pheromone, cis-vaccenyl acetate (cVA). Est-6 was previously linked to post-mating effects in the reproductive system of females. As Est-6 is also known to hydrolyze cVA in vitro and is expressed in the main olfactory organ, the antenna, we tested here its role in olfaction as a putative odorant-degrading enzyme.
We first confirm that Est-6 is highly expressed in olfactory sensilla, including cVA-sensitive sensilla, and we show that expression is likely associated with non-neuronal cells. Our electrophysiological approaches show that the dynamics of olfactory receptor neuron (ORN) responses is strongly influenced by Est-6, as in Est-6° null mutants (lacking the Est-6 gene) cVA-sensitive ORN showed increased firing rate and prolonged activity in response to cVA. Est-6° mutant males had a lower threshold of behavioral response to cVA, as revealed by the analysis of two cVA-induced behaviors. In particular, mutant males exhibited a strong decrease of male-male courtship, in association with a delay in courtship initiation.
Our study presents evidence that Est-6 plays a role in the physiological and behavioral dynamics of sex pheromone response in Drosophila males and supports a role of Est-6 as an odorant-degrading enzyme (ODE) in male antennae. Our results also expand the role of Est-6 in Drosophila biology, from reproduction to olfaction, and highlight the role of ODEs in insect olfaction.
PMCID: PMC3414785  PMID: 22715942
carboxylesterase; esterase 6; olfaction; pheromone; signal termination
12.  Asymmetric neurotransmitter release enables rapid odor lateralization in Drosophila 
Nature  2012;493(7432):424-428.
In Drosophila, most individual olfactory receptor neurons (ORNs) project bilaterally to both sides of the brain1,2. Having bilateral rather than unilateral projections may represent a useful redundancy. However, bilateral ORN projections to the brain should also compromise the ability to lateralize odors. Nevertheless, walking or flying Drosophila reportedly turn toward their more strongly stimulated antenna3-5. Here we show that each ORN spike releases ~40% more neurotransmitter from the axon branch ipsilateral to the soma, as compared to the contralateral branch. As a result, when an odor activates the antennae asymmetrically, ipsilateral central neurons begin to spike a few milliseconds before contralateral neurons, and ipsilateral central neurons also fire at a 30-50% higher rate. We show that a walking fly can detect a 5% asymmetry in total ORN input to its left and right antennal lobes, and can turn toward the odor in less time than it requires the fly to complete a stride. These results demonstrate that neurotransmitter release properties can be tuned independently at output synapses formed by a single axon onto two target cells with identical functions and morphologies. Our data also show that small differences in spike timing and spike rate can produce reliable differences in olfactory behavior.
PMCID: PMC3590906  PMID: 23263180
13.  A Presynaptic Gain Control Mechanism Fine-Tunes Olfactory Behavior 
Neuron  2008;59(2):311-321.
Early sensory processing can play a critical role in sensing environmental cues. We have investigated the physiological and behavioral function of gain control at the first synapse of olfactory processing in Drosophila. We report that olfactory receptor neurons (ORNs) express the GABAB receptor (GABABR) and its expression expands the dynamic range of ORN synaptic transmission that is preserved in projection neuron responses. Strikingly, we find that different ORN channels have unique baseline levels of GABABR expression. ORNs that sense the aversive odorant CO2 do not express GABABRs nor exhibit any presynaptic inhibition. In contrast, pheromone-sensing ORNs express a high level of GABABRs and exhibit strong presynaptic inhibition. Furthermore, a behavioral significance of presynaptic inhibition was revealed by a courtship behavior in which pheromone-dependent mate localization is impaired in flies that lack GABABRs in specific ORNs. Together, these findings indicate that different olfactory receptor channels may employ heterogeneous presynaptic gain control as a mechanism to allow an animal’s innate behavioral responses to match its ecological needs.
PMCID: PMC2539065  PMID: 18667158
Drosophila; olfaction; GABAB; presynaptic inhibition; gain control; dynamic range; two-photon imaging
14.  Degradation of Pheromone and Plant Volatile Components by a Same Odorant-Degrading Enzyme in the Cotton Leafworm, Spodoptera littoralis 
PLoS ONE  2011;6(12):e29147.
Odorant-Degrading Enzymes (ODEs) are supposed to be involved in the signal inactivation step within the olfactory sensilla of insects by quickly removing odorant molecules from the vicinity of the olfactory receptors. Only three ODEs have been both identified at the molecular level and functionally characterized: two were specialized in the degradation of pheromone compounds and the last one was shown to degrade a plant odorant.
Previous work has shown that the antennae of the cotton leafworm Spodoptera littoralis, a worldwide pest of agricultural crops, express numerous candidate ODEs. We focused on an esterase overexpressed in males antennae, namely SlCXE7. We studied its expression patterns and tested its catalytic properties towards three odorants, i.e. the two female sex pheromone components and a green leaf volatile emitted by host plants.
SlCXE7 expression was concomitant during development with male responsiveness to odorants and during adult scotophase with the period of male most active sexual behaviour. Furthermore, SlCXE7 transcription could be induced by male exposure to the main pheromone component, suggesting a role of Pheromone-Degrading Enzyme. Interestingly, recombinant SlCXE7 was able to efficiently hydrolyze the pheromone compounds but also the plant volatile, with a higher affinity for the pheromone than for the plant compound. In male antennae, SlCXE7 expression was associated with both long and short sensilla, tuned to sex pheromones or plant odours, respectively. Our results thus suggested that a same ODE could have a dual function depending of it sensillar localisation. Within the pheromone-sensitive sensilla, SlCXE7 may play a role in pheromone signal termination and in reduction of odorant background noise, whereas it could be involved in plant odorant inactivation within the short sensilla.
PMCID: PMC3246455  PMID: 22216190
15.  Intensity invariant dynamics and odor-specific latencies in olfactory receptor neuron response 
Odors elicit spatio-temporal patterns of activity in the brain. Spatial patterns arise from the specificity of the interaction between odorants and odorant receptors expressed in different olfactory receptor neurons (ORNs). But the origin of temporal patterns of activity and their role in odor coding remain unclear. We investigate how physiological aspects of ORN response and physical aspects of odor stimuli give rise to diverse responses in Drosophila ORNs. We show that odor stimuli have intrinsic dynamics that depend on odor type and strongly affect ORN response. Using linear-nonlinear modeling to remove the contribution of the stimulus dynamics from the ORN dynamics we study the physiological properties of the response to different odorants and concentrations. For several odorants and receptor types the ORN response dynamics normalized by the peak response are independent of stimulus intensity for a large portion of the neuron’s dynamic range. Adaptation to a background odor changes the gain and dynamic range of the response but does not affect normalized response dynamics. Stimulating ORNs with various odorants reveals significant odor-dependent delays in the ORN response functions. These differences however can be dominated by differences in stimulus dynamics. In one case the response of one ORN to two odorants is predicted solely from measurements of the odor signals. Within a large portion of their dynamic range ORNs can capture information about stimulus dynamics independently from intensity while introducing odor-dependent delays. How insects might use odor-specific stimulus dynamics and ORN dynamics in discrimination and navigation tasks remains an open question.
PMCID: PMC3678969  PMID: 23575828
16.  Excitatory Interactions Between Olfactory Processing Channels in the Drosophila Antennal Lobe 
Neuron  2007;54(1):89-103.
Each odorant receptor gene defines a unique type of olfactory receptor neuron (ORN) and a corresponding type of second-order neuron. Because each odor can activate multiple ORN types, information must ultimately be integrated across these processing channels to form a unified percept. Here we show that, in Drosophila, integration begins at the level of second-order projection neurons (PNs). We genetically silence all the ORNs that normally express a particular odorant receptor, and find that PNs postsynaptic to the silent glomerulus receive substantial lateral excitatory input from other glomeruli. Genetically confining odor-evoked ORN input to just one glomerulus reveals that most PNs postsynaptic to other glomeruli receive indirect excitatory input from the single ORN type that is active. Lateral connections between identified glomeruli vary in strength, and this pattern of connections is stereotyped across flies. Thus, a dense network of lateral connections distributes odor-evoked excitation between channels in the first brain region of the olfactory processing stream.
PMCID: PMC2048819  PMID: 17408580
17.  Engrailed expression in subsets of adult Drosophila sensory neurons 
Invertebrate neuroscience : IN  2008;8(3):133-146.
Engrailed (En) has an important role in neuronal development in vertebrates and invertebrates. In adult Drosophila, although En expression persists throughout adulthood, a detailed description of its expression in sensory neurons has not been made. In this study, en-GAL4 was used to drive UAS-CD8::GFP expression and the projections of sensory neurons were examined with confocal microscopy. En protein expression was confirmed using immunocytochemistry. In the antenna, En is present in subsets of Johnston’s organ neurons and of olfactory neurons. En-driven GFP is expressed in axons projecting to 18 identifed olfactory glomeruli, originating from basiconic, trichoid and coeloconic sensilla. In most cases both neurons of a sensillum express En. En expression overlaps with that of Acj6, another transcription factor. En-driven GFP is also expressed in a subset of maxillary palp olfactory neurons and in all mechanosensory and gustatory sensilla in the posterior compartment of the labial palps. In the legs and halteres, en-driven GFP is expressed in only a subset of the sensory neurons of different modalities that arise in the posterior compartment. Finally, en-driven GFP is expressed in a single multidendritic sensory neuron in each abdominal segment.
PMCID: PMC2557442  PMID: 18597129
Transcription factor; homeodomain; Drosophila melanogaster; sense organs
18.  Odorant Receptor from the Southern House Mosquito Narrowly Tuned to the Oviposition Attractant Skatole 
Journal of Chemical Ecology  2010;36(8):797-800.
Oviposition attractants are environmental cues that allow Culex gravid female mosquitoes to locate suitable sites for egg-laying and, therefore, may be exploited for environmentally friendly strategies for controlling mosquito populations. Naturally occurring skatole has been identified as an oviposition attractant for the Southern House mosquito, Culex quinquefasciatus. Previously, we identified in Cx. quinquefasciatus female antennae an olfactory receptor neuron (ORN) highly sensitive to skatole and an odorant-binding protein involved in the detection of this semiochemical. Here, we describe the characterization of an odorant receptor (OR), CquiOR10, which is narrowly tuned to skatole when expressed in the Xenopus oocyte system. Odorant-induced response profiles generated by heterologously expressed CquiOR10 suggest that this OR is expressed in the mosquito ORN sensitive to skatole. However, geranylacetone, which stimulates the antennal ORN, was not detected by CquiOR10-expressing oocytes, thus raising interesting questions about reception of oviposition attractants in mosquitoes.
PMCID: PMC2908433  PMID: 20623327
Odorant receptor; CquiOR10; Culex quinquefasciatus; Xenopus oocyte expression system; 3-Methylindole; 2-Methylphenol
19.  Generalization of courtship learning in Drosophila is mediated by cis-vaccenyl acetate 
Current biology : CB  2007;17(7):599-605.
Reproductive behavior in Drosophila has both stereotyped and plastic components that are driven by age- and sex-specific chemical cues. Males who unsuccessfully court virgin females subsequently avoid females that are of the same age as the trainer. In contrast, males trained with mature mated females associate volatile appetitive and aversive pheromonal cues and learn to suppress courtship of all females. Here we show that the volatile aversive pheromone that leads to generalized learning with mated females is (Z)-11-octadecenyl acetate (cis-vaccenyl acetate, cVA). cVA is a major component of the male cuticular hydrocarbon profile, but it is not found on virgin females. During copulation, cVA is transferred to the female in ejaculate along with sperm and peptides that decrease her sexual receptivity. When males sense cVA (either synthetic or from mated female or male extracts) in the context of female pheromone, they develop a generalized suppression of courtship. The effects of cVA on initial courtship of virgin females can be blocked by expression of tetanus toxin in Or65a, but not Or67d neurons, demonstrating that the aversive effects of this pheromone are mediated by a specific class of olfactory neuron. These findings suggest that transfer of cVA to females during mating may be part of the male’s strategy to suppress reproduction by competing males.
PMCID: PMC1913718  PMID: 17363250
Learning and memory; olfaction; Drosophila; pheromones; cis-vaccenyl acetate
20.  Distinct functions of acj6 splice forms in odor receptor gene choice 
Individual olfactory receptor neurons (ORNs) selectively express one or a small number of odor receptors from among a large receptor repertoire. The expression of an odor receptor dictates the odor response spectrum of the ORN. The process of receptor gene choice relies in part on a combinatorial code of transcription factors. In Drosophila, the POU domain transcription factor Acj6 is one element of the transcription factor code. In acj6 null mutants, many ORNs do not express an appropriate odor receptor gene and thus are not correctly specified. We find that acj6 is alternatively spliced to yield many structurally distinct transcripts in the olfactory organs. We generate flies that express single splice forms of acj6 in an acj6− background. We find that different splice forms are functionally distinct; they differ in their abilities to specify ORN identities. Some individual splice forms can fully rescue the specification of some ORNs. Individual splice forms can function both positively and negatively in receptor gene regulation. ORNs differ in their requirements for splice forms; some are not fully rescued by any single splice form tested, suggesting that some ORNs may require the combinatorial action of multiple splice forms. Late expression of some acj6 splice forms is sufficient to rescue some ORN classes, consistent with a direct role for Acj6 isoforms in receptor gene expression. The results indicate that alternative splicing may add another level of richness to the regulatory code that underlies the process of odor receptor gene choice.
PMCID: PMC2858447  PMID: 20371823
olfaction; Drosophila; Acj6; POU-domain; odor receptor; splicing
21.  Non-synaptic inhibition between grouped neurons in an olfactory circuit 
Nature  2012;492(7427):66-71.
Diverse sensory organs, including mammalian taste buds and insect chemosensory sensilla, show a striking compartmentalization of receptor cells. However, the functional impact of this organization remains unclear. Here we show that compartmentalized Drosophila olfactory receptor neurons (ORNs) communicate with each other directly. The sustained response of one ORN is inhibited by the transient activation of a neighboring ORN. Mechanistically, such lateral inhibition does not depend on synapses and is likely mediated by ephaptic coupling. Moreover, lateral inhibition in the periphery can modulate olfactory behavior. Together, the results show that integration of olfactory information can occur via lateral interactions between ORNs. Inhibition of a sustained response by a transient response may provide a means of encoding salience. Finally, a CO2-sensitive ORN in the malaria mosquito Anopheles can also be inhibited by excitation of an adjacent ORN, suggesting a broad occurrence of lateral inhibition in insects and possible applications in insect control.
PMCID: PMC3518700  PMID: 23172146
22.  A Regulatory Code for Neuron-Specific Odor Receptor Expression 
PLoS Biology  2008;6(5):e125.
Olfactory receptor neurons (ORNs) must select—from a large repertoire—which odor receptors to express. In Drosophila, most ORNs express one of 60 Or genes, and most Or genes are expressed in a single ORN class in a process that produces a stereotyped receptor-to-neuron map. The construction of this map poses a problem of receptor gene regulation that is remarkable in its dimension and about which little is known. By using a phylogenetic approach and the genome sequences of 12 Drosophila species, we systematically identified regulatory elements that are evolutionarily conserved and specific for individual Or genes of the maxillary palp. Genetic analysis of these elements supports a model in which each receptor gene contains a zip code, consisting of elements that act positively to promote expression in a subset of ORN classes, and elements that restrict expression to a single ORN class. We identified a transcription factor, Scalloped, that mediates repression. Some elements are used in other chemosensory organs, and some are conserved upstream of axon-guidance genes. Surprisingly, the odor response spectra and organization of maxillary palp ORNs have been extremely well-conserved for tens of millions of years, even though the amino acid sequences of the receptors are not highly conserved. These results, taken together, define the logic by which individual ORNs in the maxillary palp select which odor receptors to express.
Author Summary
Odors are detected by olfactory receptor neurons (ORNs). Which odor an individual neuron detects is dictated by the odor receptors it expresses. Odor receptors are encoded by large families of genes, and an individual neuron must thus select the gene it expresses from among many possibilities. The mechanism underlying this choice is largely unknown. We have examined the problem of receptor gene choice in the fruit fly Drosophila, whose maxillary palp contains six functional classes of ORNs, each expressing different odor receptor genes. By comparing the DNA sequences flanking these genes in 12 different species of Drosophila, we have identified regulatory elements that are evolutionarily conserved and specific to each odor receptor. Genetic analysis of these elements showed that some act positively to dictate expression in a subset of ORNs, while others act negatively to restrict the expression of a receptor gene to a particular ORN class. We identified a transcription factor, Scalloped, that mediates repression. We were surprised to find that the odor response spectra of these neurons have been well-conserved for tens of millions of years, even though the amino acid sequences of their receptors have diverged considerably.
How does an olfactory receptor neuron select which odor receptor to express? A computational analysis of 12Drosophila genomes combined with mutational analysis identifies conservedcis elements and defines a regulatory code.
PMCID: PMC2430909  PMID: 18846726
23.  Excitatory Local Circuits and Their Implications for Olfactory Processing in the Fly Antennal Lobe 
Cell  2007;128(3):601-612.
Conflicting views exist of how circuits of the antennal lobe, the insect equivalent of the olfactory bulb, translate input from olfactory receptor neurons (ORNs) into projection neuron (PN) output. Synaptic connections between ORNs and PNs are one-to-one, yet PNs are more broadly tuned to odors than ORNs. The basis for this difference in receptive range remains unknown. Analyzing a Drosophila mutant lacking ORN input to one glomerulus, we show that some of the apparent complexity in the antennal lobe’s output arises from lateral, interglomerular excitation of PNs. We describe a previously unidentified population of cholinergic local neurons (LNs) with multiglomerular processes. These excitatory LNs respond broadly to odors but exhibit little glomerular specificity in their synaptic output, suggesting that PNs are driven by a combination of glomerulus-specific ORN afferents and diffuse LN excitation. Lateral excitation may boost PN signals and enhance their transmission to third-order neurons in a mechanism akin to stochastic resonance.
PMCID: PMC2866183  PMID: 17289577
24.  Sex-biased expression of odorant receptors in antennae and palps of the African malaria vector Anopheles gambiae 
At the heart of the odor recognition process in all animals are G-protein-coupled receptors, which are seven-transmembrane domain proteins that initiate G-protein-mediated signaling cascades when activated by their ligands. Odorant receptors (ORs) are a large, diverse family of proteins with some 80 members in the mosquito Anopheles gambiae. With the assumption that more sensilla on female antennae are tuned to human odors than on male antennae, comparison of specific OR mRNA levels in male and female antennae can provide an indication as to which receptors may be stimulated by host odors. We have used RT PCR and quantitative real-time PCR (qRT PCR) to investigate sex-biased expression levels of 80 A. gambiae ORs in male and female antennae and maxillary palps. On the basis of prevalence of expression in female antennae and on a strong female relative to male expression bias we identified a short list of ORs that are likely involved in host odor recognition by female mosquitoes.
PMCID: PMC2247438  PMID: 18207086
Mosquito; Olfaction; Odorant binding protein (OBP); OR; Olfactory sensillum; Trichoid sensillum; mRNA expression; Olfactory organs
25.  Disruption of Olfactory Receptor Neuron Patterning in Scutoid mutant Drosophila 
Olfactory neurons show an extreme diversity of cell types with each cell usually expressing one member from a large family of 60 Odorant receptor (Or)genes in Drosophila. Little is known about the developmental processes and transcription factors that generate this stereotyped pattern of cellular diversity. Here we investigate the molecular and cellular basis of defects in olfactory system function in an unusual dominant mutant, Scutoid. We show that the defects map to olfactory neurons innervating a specific morphological class of sensilla on the antenna, large basiconics. Molecular analysis indicates defects in neurons expressing specific classes of receptor genes that map to large basiconic sensilla. Previous studies have shown that in Scutoid mutants the coding region of the transcriptional repressor snail is translocated near the no-ocelli promoter, leading to misexpression of snail in the developing eye-antenna disc. We show that ectopic expression of snail in developing olfactory neurons leads to severe defects in neurons of the antennal large basiconics supporting the model that the dominant olfactory phenotype in Scutoid is caused by misexpression of snail.
PMCID: PMC3019251  PMID: 20875862

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