InteractiveFly: GeneBrief

Ionotropic receptor 84a: Biological Overview | References


Gene name - Ionotropic receptor 84a

Synonyms -

Cytological map position - 84D6-84D6

Function - channel

Keywords - chemosensory ionotropic glutamate receptor family protein, ion channel, regulation of male courtship behavior, response to aromatic odors

Symbol - Ir84a

FlyBase ID: FBgn0037501

Genetic map position - chr3R:3232504-3235106

Classification - Ligand-gated ion channel

Cellular location - surface transmembrane



NCBI links: HomoloGene | EntrezGene
BIOLOGICAL OVERVIEW

Many animals attract mating partners through the release of volatile sex pheromones, which can convey information on the species, gender and receptivity of the sender to induce innate courtship and mating behaviours by the receiver. Male Drosophila melanogaster fruitflies display stereotyped reproductive behaviours towards females, and these behaviours are controlled by the neural circuitry expressing male-specific isoforms of the transcription factor Fruitless (FRUM). However, the volatile pheromone ligands, receptors and olfactory sensory neurons (OSNs) that promote male courtship have not been identified in this important model organism. This study describes a novel courtship function of Ionotropic receptor 84a (IR84a), which is a member of the chemosensory ionotropic glutamate receptor family, in a previously uncharacterized population of FRUM-positive OSNs. IR84a-expressing neurons are activated not by fly-derived chemicals but by the aromatic odours phenylacetic acid and phenylacetaldehyde, which are widely found in fruit and other plant tissues that serve as food sources and oviposition sites for drosophilid flies. Mutation of Ir84a abolishes both odour-evoked and spontaneous electrophysiological activity in these neurons and markedly reduces male courtship behaviour. Conversely, male courtship is increased -- in an IR84a-dependent manner -- in the presence of phenylacetic acid but not in the presence of another fruit odour that does not activate IR84a. Interneurons downstream of IR84a-expressing OSNs innervate a pheromone-processing centre in the brain. Whereas IR84a orthologues and phenylacetic-acid-responsive neurons are present in diverse drosophilid species, IR84a is absent from insects that rely on long-range sex pheromones. Our results suggest a model in which IR84a couples food presence to the activation of the fruM courtship circuitry in fruit flies. These findings reveal an unusual but effective evolutionary solution to coordinate feeding and oviposition site selection with reproductive behaviours through a specific sensory pathway (Grosjean, 2012).

While mapping the projections of Ionotropic receptor (IR)-expressing OSNs to the primary olfactory centre (Silbering, 2011), the antennal lobe, it was observed that an Ir84a reporter was labelling neurons innervating the VL2a glomerulus. VL2a is one of only three glomeruli that are larger in males and whose OSN inputs and projection neuron outputs express male-specific isoforms of the behavioural sex determination gene fruitless (fruM) (Stockinger, 2005). fruM-expressing OSNs have been implicated in promoting male sexual behaviours, because inhibition of synaptic transmission in all of these neurons simultaneously reduces male courtship of female. The expression of Ir84a in fruM-expressing neurons was confirmed by visualizing the co-expression of an Ir84a reporter, as well as endogenous Ir84a transcripts, with a fruM reporter. No sexual dimorphism was observed either in the number of Ir84a-expressing cells or in their targeting to VL2a, indicating that FRUM does not have an essential role in the development of these neurons, similar to other fruM-expressing OSNs (Grosjean, 2012).

A GAL4 knock-in null allele, Ir84aGAL4 was generated. Ir84aGAL4/+ heterozygotes expressed a GAL4-responsive, membrane-targeted, green fluorescent protein (GFP) transgene (UAS-mCD8:GFP) exclusively in Ir84a-expressing OSNs. In Ir84aGAL4 homozygotes, the endogenous expression of Ir84a was lost, but the distribution and dendritic projections of these neurons, as revealed by mCD8:GFP, was unaffected. The axons of Ir84a-expressing neurons in heterozygous and homozygous Ir84aGAL4 flies projected only to VL2a. Ir84a is therefore dispensable for the specification and wiring of the neurons in which it is expressed. An amino-terminal enhanced GFP (EGFP)-tagged version of this receptor (Abuin, 2011) localized to the cell bodies and the ciliated dendritic endings of these neurons but not to their axon termini, consistent with an exclusive role for IR84a as an olfactory receptor in the fruM circuitry (Grosjean, 2012).

The responses of IR84a-expressing neurons to chemicals produced by male or virgin female flies was tested, both by delivering headspaces of flies from a distance (simulating the action of volatile pheromones) and by presenting extracts from fly cuticles at close range (mimicking exposure to non-volatile hydrocarbons, such as contact pheromones. These stimuli produced no or extremely small responses, as detected by extracellular recordings in ac4 sensilla, which belong to the class of olfactory hair that houses IR84a-expressing neurons, as well as OSNs that express IR75d, or IR76a and IR76b (Benton, 2009). These observations suggest that IR84a is not tuned to fly-derived pheromones. Therefore 163 structurally diverse odours were tested. Only three of these gave responses of >50 spikes s−1 above basal activity: phenylacetaldehyde [as identified previously (Yao, 2005)], phenylacetic acid and phenylethylamine. Dose response curves that revealed sensitivity to these ligands are similar in both sexes (Grosjean, 2012).

In Ir84aGAL4 homozygous mutants, the responses to phenylacetic acid and phenylacetaldehyde were completely abolished. Re-introduction of Ir84a function in these neurons, by using UAS-Ir84a or UAS-EGFP:Ir84a cDNA transgenes, rescued these phenotypes, indicating a cell-autonomous function for IR84a in mediating these odour responses. By contrast, responses to phenylethylamine were unaffected, corroborating the evidence that this chemical is detected by the neurons that express both IR76a and IR76b. Consistent with these loss-of-function data, misexpression of IR84a in Odorant receptor 35a (OR35a)-expressing neurons was sufficient to confer responsiveness to phenylacetic acid and phenylacetaldehyde. The basal activity in Ir84a mutant ac4 sensilla was also lower than that in the ac4 sensilla of wild-type and rescue genotypes, indicating that IR84a has a role in promoting spontaneous firing (Grosjean, 2012).

Phenylacetic acid and phenylacetaldehyde are aromatic compounds found in a diverse range of fruit and other plant tissues, as well as in their fermentation products, and they are used in human perfumes for their floral, honey-like, sweet smell. The presence of these chemicals in two host fruit for drosophilid flies, overripe bananas and the prickly-pear cactus Opuntia ficus-indica, as well as in laboratory Drosophila medium, was confirmed by using gas chromatography- mass spectrometry analysis. The ubiquity of phenylacetic acid in vegetal tissues may be linked with its activity as a growth-regulating auxin and/or its production by plant-associated microorganisms. Small, but reproducible, quantities of phenylacetic acid and phenylacetaldehyde were also detected in whole-body cuticular extracts of male and virgin female D. melanogaster. The similarity in the relative amounts of these chemicals in laboratory medium and fruitfly extracts suggested that these chemicals are transferred from food to flies during their culture. 'Clean' cuticular extracts from animals grown on a minimal medium containing only sucrose and agarose consistently contain no detectable phenylacetaldehyde or phenylacetic acid (Grosjean, 2012).

The expression of IR84a in fruM-expressing neurons implicates this receptor in the regulation of male courtship (Manoli, 2005; Stockinger, 2005). Indeed, in single-pair courtship assays, Ir84aGAL4 mutant males court wild-type females significantly less than do wild-type males. This phenotype was observed using both decapitated virgin females (which do not produce feedback signals) and in more natural conditions, with intact females together with food. Most individual components of the courtship ritual were affected in Ir84a mutant flies. These defects were rescued with a UAS-Ir84a transgene, confirming that they result from the absence of IR84a in OSNs. The observed reduction in male heterosexual courtship index (~50%) is highly comparable to the phenotype of flies in which all FRUM-positive OSNs are silenced (Stockinger, (2005), suggesting that IR84a-expressing neurons are the major olfactory fruM channel contributing to this behaviour. Residual courtship is presumably stimulated by other sensory modalities, such as taste. Male wild-type D. melanogaster also show a low level of courtship towards other males, and this homosexual courtship was also markedly reduced in Ir84aGAL4 mutants. By contrast, Ir84aGAL4 mutant females did not show overt defects in reproductive behaviours, including copulation latency, success or duration (Grosjean, 2012).

In innate olfactory preference assays, Ir84aGAL4 mutant flies still show robust avoidance of acetic acid, indicating that they do not have a general impairment in sensory detection. By contrast, no obvious responses of flies to phenylacetic acid was observed, suggesting that this food-derived odour is not a volatile stimulus that attracts flies but is a salient cue at close range. Notably, phenylacetic acid has a low vapour pressure compared with other fruit volatiles (for example, ethyl butyrate). The observation that courtship is reduced in Ir84aGAL4 mutants in assays in which only small amounts of phenylacetic acid are present on fly cuticles raises the possibility that spontaneous activity of these neurons also contributes to establishing a basal courtship level, which is abolished in the absence of IR84a (Grosjean, 2012).

To test whether IR84a ligands are sufficient to promote courtship, the assay was adapted by using killed female objects (which males court at only low levels) and by replacing the base of the chamber with gauze, beneath which a filter paper treated with odour or solvent was placed. Perfuming with phenylacetic acid nearly doubled the courtship index of wild-type flies compared with a solvent control. This effect was abolished in Ir84aGAL4 mutants and could be restored, albeit not fully, by introducing a UAS-Ir84a transgene. By contrast, ethyl butyrate, which does not activate IR84a, did not increase courtship. The courtship chamber was also perfumed with Drosophila food—which contains phenylacetic acid, and this complex olfactory stimulus was observed to induced IR84a-dependent increases in male courtship behaviour (Grosjean, 2012).

The other fruM-expressing OSN populations express either OR67d, which is a receptor for the antiaphrodisiac male pheromone cis-vaccenyl acetate, or OR47b, which is activated by unidentified fly-derived odours from both sexes and may participate in mate localization. How IR84a sensory information is integrated with these pheromonal pathways was examined by visualizing the axons of projection neurons innervating the VL2a (IR84a), VA1lm (OR47b) and DA1 (OR67d) glomeruli, which carry sensory information to the mushroom body and lateral horn. Images of single-labelled projection neurons of different glomerular classes were registered onto a common reference brain. DA1 and VA1lm excitatory projection neurons target an anterior-ventral pheromone-processing region of the lateral horn, which is segregated from projection neurons that are responsive to general food odours. Importantly, it was found that VL2a projection neurons—and no other IR-expressing projection neuron class are highly interdigitated with pheromone pathways and not food pathways. Indeed, VL2a projection neuron axon terminals overlap more strongly with VA1lm projection neurons than any of the other 44 projection neuron classes, consistent with projection neurons of both of these classes transmitting courtship-promoting sensory signals. The VL2a, DA1 and VA1lm inhibitory projection neurons were observed to overlap to a similar extent. The anatomical convergence of combinations of excitatory and inhibitory inputs from VL2a, VA1lm and DA1 projection neurons may allow the integration of olfactory signals by fruM-expressing third-order neurons (Cachero, 2010; Yu, 2010) to control male courtship behaviour (Grosjean, 2012).

Many olfactory IRs are conserved in insects (Croset, 2010) and may detect odours that are important for all species. By contrast, although IR84a orthologues are present in ecologically diverse drosophilids, they are absent from other Diptera and more divergent insects. In the cactophilic species Drosophila mojavensis, coeloconic sensilla with neurons were identified that are responsive to phenylacetic acid and phenylacetaldehyde on their anterior antennal surface (similar to ac4 sensilla in D. melanogaster). Thus, IR84a may have a conserved, drosophilid-specific function (Grosjean, 2012).

Despite the widely held assumption of the existence of volatile chemicals that promote courtship in Drosophila, behavioural evidence for long-range pheromones is inconclusive, and no female-specific volatile compound that activates male OSNs has been identified. The characterization of IR84a identifies an olfactory receptor that is expressed in FRUM-positive neurons and is required to promote male courtship. Surprisingly, this receptor is not activated by fly-derived odours but rather by aromatic compounds that are present in the vegetal substrates in which fruitflies feed, breed and oviposit. Thus, the IR84a pathway may promote male courtship in the presence of food, complementing the functions of pheromone receptors in regulating mate choice. This model can account for the widespread observations that D. melanogaster and other drosophilids mate predominantly on their food substrates. Whereas many insects and other animal classes use long-range sex pheromones to attract potential mates, the evolution of IR84a in fruitflies has provided an alternative (although not necessarily exclusive) olfactory mechanism to unite males with females by integrating food-sensing neurons with the circuitry controlling sexual behaviour. Whether other animals have dedicated sensory pathways for environmental 'aphrodisiacs' remains an open question (Grosjean, 2012).

Amplification of Drosophila olfactory responses by a DEG/ENaC Channel

Insect olfactory receptors operate as ligand-gated ion channels that directly transduce odor stimuli into electrical signals. However, in the absence of any known intermediate transduction steps, it remains unclear whether and how these ionotropic inputs are amplified in olfactory receptor neurons (ORNs). This study finds that amplification occurs in the Drosophila courtship-promoting ORNs through Pickpocket (PPK25), a member of the degenerin/epithelial sodium channel family (DEG/ENaC). Pharmacological and genetic manipulations indicate that, in Or47b and Ir84a ORNs, PPK mediates Ca(2+)-dependent signal amplification via an intracellular calmodulin-binding motif. Additionally, hormonal signaling upregulates PPK expression to determine the degree of amplification, with striking effects on male courtship. Together, these findings advance understanding of sensory neurobiology by identifying an amplification mechanism compatible with ionotropic signaling. Moreover, this study offers new insights into DEG/ENaC activation by highlighting a novel means of regulation that is likely conserved across species (Ng, 2019).

Vertebrates detect odorants with G-protein-coupled receptors (GPCRs), the activation of which triggers subsequent metabotropic signaling cascades in the olfactory receptor neurons (ORNs) to transduce chemical stimuli into electrical signals. These series of transduction events also provide opportunities to amplify input signals. In contrast, insect olfaction is initiated by ligand-gated receptor channels that lack canonical G protein interacting domains. Although various G proteins and effectors have been implicated in the function of insect ORNs, it remains an open question whether those molecules play a specific role in olfactory transduction or a regulatory role in neuronal development, maintenance, and neuromodulation. Given that ligand-gated receptor channels can directly convert sensory stimuli to neuronal depolarization, it is unclear whether and how ionotropic inputs can be amplified in the absence of any known intermediate transduction steps (Ng, 2019).

In earlier work, it was found that the responses of Or47b ORNs, which detect aphrodisiac fly odors in D. melanogaster, increase with age in male flies (Lin, 2016), pointing to the possibility of signal amplification downstream of insect olfactory receptors. This age-dependent plasticity therefore presents an opportunity to investigate the mechanisms by which ionotropic sensory inputs can be amplified. Intriguingly, Or47b ORNs express a degenerin/epithelial sodium channel (DEG/ENaC) subunit named Pickpocket (PPK25). Within invertebrate genomes, DEG/ENaCs constitute one of the largest ion channel families. In mechanosensory and gustatory neurons, PPK subunits are involved in touch, proprioception, nociception, salt taste, water sensation, and recognition of contact pheromones. However, the functional role of PPK in olfaction remains unknown (Ng, 2019).

If PPK amplifies olfactory signals, how then is its activity regulated? Can it function as a transduction channel activated by intracellular second messengers downstream of receptor activation? Members of the DEG/ENaC superfamily, including the mammalian nonvoltage-gated sodium channels (SCNNs) and acid-sensing sodium ion channels (ASICs), are known to open in response to mechanical stimuli, extracellular ligands, or are otherwise constitutively active. In cultured cell lines, various intracellular signaling mechanisms can influence DEG/ENaC currents by regulating channel transcription, endocytosis, degradation, or translocation. Post-translational modification is also known to modulate DEG/ENaC function; for example, constitutive channel activity can be regulated by CaMKII-mediated phosphorylation or by protease-mediated cleavage of the extracellular domain. However, the possibility of DEG/ENaC activation by direct interaction with an intracellular ligand has not been explored (Ng, 2019).

This study shows that signal amplification can occur downstream of ligand-gated receptor channels. The age-dependent response plasticity of Or47b ORNs arises through PPK25-mediated amplification. Additionally, this mechanism is employed in another type of courtship-promoting ORN expressing the Ir84a receptor. Interestingly, the degree of amplification is determined by PPK expression levels, which are in turn upregulated by a reproductive hormone. Thus, a common hormone regulates these two parallel olfactory pathways to coordinate courtship behavior. Mechanistically, PPK operates as a transduction channel: its activation requires odor-induced Ca2+ influx and a calmodulin binding motif (CBM) in the N-terminal intracellular domain. This result therefore highlights a novel mechanism whereby DEG/ENaCs can be activated by second messengers, a critical feature common to all transduction channels. Moreover, similar intracellular CBMs are predicted in multiple DEG/ENaCs across animal species, suggesting an evolutionarily conserved regulatory mechanism for channels in this superfamily (Ng, 2019).

This study has demonstrated that ionotropic sensory inputs can be amplified in select Drosophila ORNs whose receptors are ligand-gated cation channels. Pharmacological and genetic experiments reveal a simple and elegant mechanism for this amplification. Upon odor stimulation, receptor excitation allows for direct influx of Ca2+, which serves as a second messenger to activate a DEG/ENaC channel, PPK25, and thereby amplify ORN responses (Ng, 2019).

Ionotropic signal amplification, as described, affords remarkable versatility in sensory signaling when compared against G-protein-mediated metabotropic mechanisms. In vertebrate olfaction, separate families of metabotropic receptors typically couple to different G proteins, each engaging a unique downstream signaling cascade. In contrast, activation of specific G proteins is not required for Ca2+-mediated amplification, making it compatible with a wide variety of ionotropic receptor channels, so long as these receptors are permeable to Ca2+. As evidenced in this study, PPK can function downstream of Or47b, Ir84a, and ChR2, despite their low sequence similarity and distinct topologies because these receptors can flux Ca2+ (Ng, 2019).

These findings highlight striking differences and commonalities between insect and vertebrate olfactory transduction. This study observed surprising heterogeneity within insect olfactory transduction: PPK is neither expressed nor functional in another ORN type expressing Or22a, which belongs to the same receptor family as Or47b. It is unclear whether input signals in Or22a ORNs are amplified. If so, it is likely through a different mechanism. This finding indicates that insect ORNs expressing the same family of receptors do not necessarily employ the same mechanism for amplification, in contrast with vertebrate olfaction where receptors from the same family share a common signaling pathway. Despite this difference, the activation mechanism and function of PPK are remarkably similar to those of Anoctamin (ANO2), a key transduction channel in vertebrate ORNs. Specifically, both PPK and ANO are activated by calcium to amplify olfactory inputs. Although the sources of Ca2+may differ-ligand-gated ion channels in insects or cyclic nucleotide-gated cation channels in vertebrates-Ca2+-mediated amplification may represent a shared signaling motif between the two olfactory systems (Ng, 2019).

Interestingly, the impact of signal amplification on spike output differs between insect and vertebrate ORNs. Consistent with its role as a transduction channel, Ano mutation markedly reduces odor-evoked currents. However, the spike output of Ano knockout ORNs is higher than that of wild-type neurons. Vertebrate ORN spike number peaks when the transduction current is largely carried by ANO at intermediate odor concentrations, suggesting a strong depolarization block whereby amplification provides negative feedback to clamp total spike output. In contrast, the local field potential and spike responses of insect ORNs both peak at saturating odor concentrations. As such, blocking PPK25-mediated amplification not only reduces LFP response but also total spike number. Therefore, signal amplification in insect ORNs may predominantly serve to modulate the gain of neuronal output (Ng, 2019).

What is the functional significance of PPK in the Or47b and Ir84a ORNs? Notably, these are the only ORN types known to promote courtship in D. melanogaster males, whose fertility and courtship drive increase and peak at about days of age. Male mating drive is highly influenced by external olfactory cues, including the availability of mates and food signaled by Or47b and Ir84a ORNs, respectively. Remarkably, the responses of both ORN types exhibit age-dependent plasticity, which is coordinated by the same reproductive hormone-juvenile hormone-through upregulation of PPK expression in older males. The expression level of PPK in turn determines the ORN response magnitude, with striking impacts on courtship. Therefore, flexibility over this biologically salient behavior is afforded by the dynamic regulation of PPK expression, which heightens males' sensitivity to food and mate odors at their age of peak fertility. This upregulation of PPK provides a molecular mechanism for how sex-specific refinements of olfactory circuits are achieved via hormonal signaling (Ng, 2019).

The critical role of the intracellular CBM in PPK function argues that Ca2+/CaM activates the channel by directly interacting with this motif. Such regulation contrasts sharply with previously reported mechanisms, in which Ca2+/CaM indirectly modulates ENaC activity through intermediate proteins. For example, in cultured Xenopus cells, Ca2+/CaM can inhibit ENaC currents by interacting with MARCKS (myristoylated alanine-rich C kinase substrate) to modulate channel open probability and also by activating CaMKII to regulate ENaC apical trafficking. Together, these findings highlight the complexity of interactions between Ca2+/CaM and neuronal DEG/ENaC (Ng, 2019).

The results described in this study further advance understanding of DEG/ENaC activation. The gating mechanisms for this family of sodium channels are known to be highly diverse: some open in response to mechanical stimuli; others to extracellular ligands; and still others are constitutively active. In light of these findings, it is possible that other members of the DEG/ENaC superfamily may also be directly activated by intracellular second messengers, allowing them to function as transduction channels to amplify sensory inputs. In support of this notion, similar N-terminal intracellular CBMs were bioinformatically identified in multiple members of the DEG/ENaC superfamily across species-including worm, fruit fly, mosquito, mouse, and human-suggesting that those channels have the potential to function as Ca2+-activated transduction channels (Ng, 2019).


REFERENCES

Search PubMed for articles about Drosophila Ir84a

Abuin, L., Bargeton, B., Ulbrich, M. H., Isacoff, E. Y., Kellenberger, S. and Benton, R. (2011). Functional architecture of olfactory ionotropic glutamate receptors. Neuron 69: 44-60. PubMed ID: 21220098

Benton, R., Vannice, K. S., Gomez-Diaz, C. and Vosshall, L. B. (2009). Variant ionotropic glutamate receptors as chemosensory receptors in Drosophila. Cell 136: 149-162. PubMed ID: 19135896

Cachero, S., Ostrovsky, A. D., Yu, J. Y., Dickson, B. J. and Jefferis, G. S. (2010). Sexual dimorphism in the fly brain. Curr Biol 20: 1589-1601. PubMed ID: 20832311

Croset, V., Rytz, R., Cummins, S. F., Budd, A., Brawand, D., Kaessmann, H., Gibson, T. J. and Benton, R. (2010). Ancient protostome origin of chemosensory ionotropic glutamate receptors and the evolution of insect taste and olfaction. PLoS Genet 6: e1001064. PubMed ID: 20808886

Grosjean, Y., Rytz, R., Farine, J. P., Abuin, L., Cortot, J., Jefferis, G. S. and Benton, R. (2011). An olfactory receptor for food-derived odours promotes male courtship in Drosophila. Nature 478: 236-240. PubMed ID: 21964331

Lin, H. H., Cao, D. S., Sethi, S., Zeng, Z., Chin, J. S. R., Chakraborty, T. S., Shepherd, A. K., Nguyen, C. A., Yew, J. Y., Su, C. Y. and Wang, J. W. (2016). Hormonal modulation of pheromone detection enhances male courtship success. Neuron 90(6): 1272-1285. PubMed ID: 27263969

Manoli, D. S., Foss, M., Villella, A., Taylor, B. J., Hall, J. C. and Baker, B. S. (2005). Male-specific fruitless specifies the neural substrates of Drosophila courtship behaviour. Nature 436: 395-400. PubMed ID: 15959468

Ng, R., Salem, S. S., Wu, S. T., Wu, M., Lin, H. H., Shepherd, A. K., Joiner, W. J., Wang, J. W. and Su, C. Y. (2019). Amplification of Drosophila olfactory responses by a DEG/ENaC Channel. Neuron 104(5): 947-959. PubMed ID: 31629603

Silbering, A. F., Rytz, R., Grosjean, Y., Abuin, L., Ramdya, P., Jefferis, G. S. and Benton, R. (2011). Complementary function and integrated wiring of the evolutionarily distinct Drosophila olfactory subsystems. J Neurosci 31: 13357-13375. PubMed ID: 21940430

Stockinger, P., Kvitsiani, D., Rotkopf, S., Tirian, L. and Dickson, B. J. (2005). Neural circuitry that governs Drosophila male courtship behavior. Cell 121: 795-807. PubMed ID: 15935765

Yao, C. A., Ignell, R. and Carlson, J. R. (2005). Chemosensory coding by neurons in the coeloconic sensilla of the Drosophila antenna. J Neurosci 25: 8359-8367. PubMed ID: 16162917

Yu, J. Y., Kanai, M. I., Demir, E., Jefferis, G. S. and Dickson, B. J. (2010). Cellular organization of the neural circuit that drives Drosophila courtship behavior. Curr Biol 20: 1602-1614. PubMed ID: 20832315


Biological Overview

date revised: 15 April 2020

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