@article {47992, title = {A mechanosensory circuit that mixes opponent channels to produce selectivity for complex stimulus features.}, journal = {Neuron}, volume = {92}, year = {2016}, month = {2016 Oct 27}, pages = {888-901}, abstract = {

Johnston{\textquoteright}s organ is the largest mechanosensory organ in\ Drosophila; it analyzes movements of the antenna due to sound, wind, gravity, and touch. Different Johnston{\textquoteright}s organ neurons (JONs) encode distinct stimulus features. Certain JONs respond in a sustained manner to steady displacements, and these JONs subdivide into opponent populations that prefer push or pull displacements. Here, we describe neurons in the brain (aPN3 neurons) that combine excitation and inhibition from push/pull JONs in different ratios. Consequently, different aPN3 neurons are sensitive to movement in different parts of the antenna{\textquoteright}s range, at different frequencies, or at different amplitude modulation rates. We use a model to show how the tuning of aPN3 neurons can arise from rectification and temporal filtering in JONs, followed by mixing of JON signals in different proportions. These results illustrate how several canonical neural circuit components{\textemdash}rectification, opponency, and filtering{\textemdash}can combine to produce selectivity for complex stimulus features.

}, doi = {10.1016/j.neuron.2016.09.059}, author = {Chang, Allison EB and Vaughan, Alexander G and Wilson, Rachel} } @article {47092, title = {Central neural circuitry mediating courtship song perception in male Drosophila.}, journal = {eLife}, volume = {4}, year = {2015}, month = {2015 Sep 21}, abstract = {

Animals use acoustic signals across a variety of social behaviors, particularly courtship. In Drosophila, song is detected by antennal mechanosensory neurons and further processed by second-order aPN1/aLN(al) neurons. However, little is known about the central pathways mediating courtship hearing. In this study, we identified a male-specific pathway for courtship hearing via third-order ventrolateral protocerebrum Projection Neuron 1 (vPN1) neurons and fourth-order pC1 neurons. Genetic inactivation of vPN1 or pC1 disrupts song-induced male-chaining behavior. Calcium imaging reveals that vPN1 responds preferentially to pulse song with long inter-pulse intervals (IPIs), while pC1 responses to pulse song closely match the behavioral chaining responses at different IPIs. Moreover, genetic activation of either vPN1 or pC1 induced courtship chaining, mimicking the behavioral response to song. These results outline the aPN1-vPN1-pC1 pathway as a labeled line for the processing and transformation of courtship song in males.

}, issn = {2050-084X}, doi = {10.7554/eLife.08477}, author = {Zhou, Chuan and Franconville, Romain and Vaughan, Alexander G and Robinett, Carmen C and Jayaraman, Vivek and Baker, Bruce S} } @article {45147, title = {Neural pathways for the detection and discrimination of conspecific song in D. melanogaster.}, journal = {Current Biology}, volume = {24}, year = {2014}, month = {2014 May 19}, pages = {1039-49}, abstract = {

BACKGROUND: During courtship, male Drosophila melanogaster sing a multipart courtship song to female flies. This song is of particular interest because (1) it is species specific and varies widely within the genus, (2) it is a gating stimulus for females, who are sensitive detectors of conspecific song, and (3) it is the only sexual signal that is under both neural and genetic control. This song is perceived via mechanosensory neurons in the antennal Johnston{\textquoteright}s organ, which innervate the antennal mechanosensory and motor center (AMMC) of the brain. However, AMMC outputs that are responsible for detection and discrimination of conspecific courtship song remain unknown.

RESULTS: Using a large-scale anatomical screen of AMMC interneurons, we identify seven projection neurons (aPNs) and five local interneurons (aLNs) that outline a complex architecture for the ascending mechanosensory pathway. Neuronal inactivation and hyperactivation during behavior reveal that only two classes of interneurons are necessary for song responses--the projection neuron aPN1 and GABAergic interneuron aLN(al). These neurons are necessary in both male and female flies. Physiological recordings in aPN1 reveal the integration of courtship song as a function of pulse rate and outline an intracellular transfer function that likely facilitates the response to conspecific song.

CONCLUSIONS: These results reveal a critical pathway for courtship hearing in male and female flies, in which both aLN(al) and aPN1 mediate the detection of conspecific song. The pathways arising from these neurons likely serve as a critical neural substrate for behavioral reproductive isolation in D. melanogaster.

}, issn = {1879-0445}, doi = {10.1016/j.cub.2014.03.048}, author = {Vaughan, Alexander G and Zhou, Chuan and Manoli, Devanand S and Baker, Bruce S} } @article {1032, title = {Sex and the single cell. II. There is a time and place for sex.}, journal = {PLoS Biology}, volume = {8}, year = {2010}, month = {2010 May}, pages = {e1000365}, abstract = {

The Drosophila melanogaster sex hierarchy controls sexual differentiation of somatic cells via the activities of the terminal genes in the hierarchy, doublesex (dsx) and fruitless (fru). We have targeted an insertion of GAL4 into the dsx gene, allowing us to visualize dsx-expressing cells in both sexes. Developmentally and as adults, we find that both XX and XY individuals are fine mosaics of cells and tissues that express dsx and/or fruitless (fru(M)), and hence have the potential to sexually differentiate, and those that don{\textquoteright}t. Evolutionary considerations suggest such a mosaic expression of sexuality is likely to be a property of other animal species having two sexes. These results have also led to a major revision of our view of how sex-specific functions are regulated by the sex hierarchy in flies. Rather than there being a single regulatory event that governs the activities of all downstream sex determination regulatory genes-turning on Sex lethal (Sxl) RNA splicing activity in females while leaving it turned off in males-there are, in addition, elaborate temporal and spatial transcriptional controls on the expression of the terminal regulatory genes, dsx and fru. Thus tissue-specific aspects of sexual development are jointly specified by post-transcriptional control by Sxl and by the transcriptional controls of dsx and fru expression.

}, keywords = {Animals, Developmental, DNA-Binding Proteins, Drosophila melanogaster, Drosophila Proteins, Female, Gene Expression Regulation, Male, Nerve Tissue Proteins, Organ Specificity, RNA-Binding Proteins, Sex Characteristics, Sex Differentiation, Transcription Factors}, issn = {1545-7885}, doi = {10.1371/journal.pbio.1000365}, author = {Robinett, Carmen C and Vaughan, Alexander G and Knapp, Jon-Michael and Baker, Bruce S} } @article {1205, title = {Manipulation of an innate escape response in Drosophila: photoexcitation of acj6 neurons induces the escape response.}, journal = {PLoS One}, volume = {4}, year = {2009}, month = {2009 Apr 2}, pages = {e5100}, abstract = {

BACKGROUND: The genetic analysis of behavior in Drosophila melanogaster has linked genes controlling neuronal connectivity and physiology to specific neuronal circuits underlying a variety of innate behaviors. We investigated the circuitry underlying the adult startle response, using photoexcitation of neurons that produce the abnormal chemosensory jump 6 (acj6) transcription factor. This transcription factor has previously been shown to play a role in neuronal pathfinding and neurotransmitter modality, but the role of acj6 neurons in the adult startle response was largely unknown. PRINCIPAL FINDINGS: We show that the activity of these neurons is necessary for a wild-type startle response and that excitation is sufficient to generate a synthetic escape response. Further, we show that this synthetic response is still sensitive to the dose of acj6 suggesting that that acj6 mutation alters neuronal activity as well as connectivity and neurotransmitter production. RESULTS/SIGNIFICANCE: These results extend the understanding of the role of acj6 and of the adult startle response in general. They also demonstrate the usefulness of activity-dependent characterization of neuronal circuits underlying innate behaviors in Drosophila, and the utility of integrating genetic analysis into modern circuit analysis techniques.

}, keywords = {Animal, Animals, Base Sequence, Behavior, DNA Primers, Drosophila melanogaster, Genetically Modified, Neurons, Startle Reaction}, issn = {1932-6203}, doi = {10.1371/journal.pone.0005100}, author = {Zimmermann, Gregor and Wang, Li-Ping and Vaughan, Alexander G and Manoli, Devanand S and Zhang, Feng and Deisseroth, Karl and Baker, Bruce S and Scott, Matthew P} }