@article {65203, title = {Drosulfakinin signaling in fruitless circuitry antagonizes P1 neurons to regulate sexual arousal in Drosophila.}, journal = {Nature Communications}, volume = {10}, year = {2019}, month = {2019 Oct 18}, pages = {4770}, abstract = {

Animals perform or terminate particular behaviors by integrating external cues and internal states through neural circuits. Identifying neural substrates and their molecular modulators promoting or inhibiting animal behaviors are key steps to understand how neural circuits control behaviors. Here, we identify the Cholecystokinin-like peptide Drosulfakinin (DSK) that functions at single-neuron resolution to suppress male sexual behavior in Drosophila. We found that Dsk neurons physiologically interact with male-specific P1 neurons, part of a command center for male sexual behaviors, and function oppositely to regulate multiple arousal-related behaviors including sex, sleep and spontaneous walking. We further found that the DSK-2 peptide functions through its receptor CCKLR-17D3 to suppress sexual behaviors in flies. Such a neuropeptide circuit largely overlaps with the fruitless-expressing neural circuit that governs most aspects of male sexual behaviors. Thus DSK/CCKLR signaling in the sex circuitry functions antagonistically with P1 neurons to balance arousal levels and modulate sexual behaviors.

}, issn = {2041-1723}, doi = {10.1038/s41467-019-12758-6}, author = {Wu, Shunfan and Guo, Chao and Zhao, Huan and Sun, Mengshi and Chen, Jie and Han, Caihong and Peng, Qionglin and Qiao, Huanhuan and Peng, Ping and Liu, Yan and Luo, Shengzhan D and Pan, Yufeng} } @article {48698, title = {Genetic and neuronal mechanisms governing the sex-specific interaction between sleep and sexual behaviors in Drosophila.}, journal = {Nature Communications}, volume = {8}, year = {2017}, month = {2017 Jul 28}, pages = {154}, abstract = {

Animals execute one particular behavior among many others in a context-dependent manner, yet the mechanisms underlying such behavioral choice remain poorly understood. Here we studied how two fundamental behaviors, sex and sleep, interact at genetic and neuronal levels in Drosophila. We show that an increased need for sleep inhibits male sexual behavior by decreasing the activity of the male-specific P1 neurons that coexpress the sex determination genes fru (M) and dsx, but does not affect female sexual behavior. Further, we delineate a sex-specific neuronal circuit wherein the P1 neurons encoding increased courtship drive suppressed male sleep by forming mutually excitatory connections with the fru (M) -positive sleep-controlling DN1 neurons. In addition, we find that FRU(M) regulates male courtship and sleep through distinct neural substrates. These studies reveal the genetic and neuronal basis underlying the sex-specific interaction between sleep and sexual behaviors in Drosophila, and provide insights into how competing behaviors are co-regulated.Genes and circuits involved in sleep and sexual arousal have been extensively studied in Drosophila. Here the authors identify the sex determination genes fruitless and doublesex, and a sex-specific P1-DN1 neuronal feedback that governs the interaction between these competing behaviors.

}, issn = {2041-1723}, doi = {10.1038/s41467-017-00087-5}, author = {Chen, Dandan and Sitaraman, Divya and Chen, Nan and Jin, Xin and Han, Caihong and Chen, Jie and Sun, Mengshi and Baker, Bruce S and Nitabach, Michael N and Pan, Yufeng} } @article {45055, title = {Central brain neurons expressing doublesex regulate female receptivity in Drosophila.}, journal = {Neuron}, volume = {83}, year = {2014}, month = {2014 Jul 2}, pages = {149-63}, abstract = {

Drosophila melanogaster females respond to male courtship by either rejecting the male or allowing copulation. The neural mechanisms underlying these female behaviors likely involve the integration of sensory information in the brain. Because doublesex (dsx) controls other aspects of female differentiation, we asked whether dsx-expressing neurons mediate virgin female receptivity to courting males. Using intersectional techniques to manipulate the activities of defined subsets of dsx-expressing neurons, we found that activation of neurons in either the pCd or pC1 clusters promotes receptivity, while silencing these neurons makes females unreceptive. Furthermore, pCd and pC1 neurons physiologically respond to the male-specific pheromone cis-vaccenyl acetate (cVA), while pC1 neurons also respond to male courtship song. The pCd and pC1 neurons expressing dsx in females do not express transcripts from the fruitless (fru) P1 promoter. Thus, virgin female receptivity is controlled at least in part by neurons that are distinct from those governing male courtship.

}, issn = {1097-4199}, doi = {10.1016/j.neuron.2014.05.038}, author = {Zhou, Chuan and Pan, Yufeng and Robinett, Carmen C and Meissner, Geoffrey W and Baker, Bruce S} } @article {6709, title = {Genetic identification and separation of innate and experience-dependent courtship behaviors in Drosophila.}, journal = {Cell}, volume = {156}, year = {2014}, month = {2014 Jan 16}, pages = {236-48}, abstract = {

Wild-type D.\ melanogaster males innately possess the ability to perform a multistep courtship ritual to conspecific females. The potential for this behavior is specified by the male-specific products of the fruitless (fru(M)) gene; males without fru(M) do not court females when held in isolation. We show that such fru(M) null males acquire the potential for courtship when grouped with other flies; they apparently learn to court flies with which they were grouped, irrespective of sex or species and retain this behavior for at least a week. The male-specific product of the doublesex gene (dsx(M)) is necessary and sufficient for the acquisition of the potential for such experience-dependent courtship. These results reveal a process that builds, via dsx(M) and social experience, the potential for a more flexible sexual behavior, which could be evolutionarily conserved as dsx-related genes that function in sexual development are found throughout the animal kingdom.

}, issn = {1097-4172}, doi = {10.1016/j.cell.2013.11.041}, author = {Pan, Yufeng and Baker, Bruce S} } @article {4886, title = {Joint control of Drosophila male courtship behavior by motion cues and activation of male-specific P1 neurons.}, journal = {Proceedings of the National Academy of Sciences of the United States of America}, volume = {109}, year = {2012}, month = {2012 May 29}, pages = {10065-70}, abstract = {

Sexual behaviors in animals are governed by inputs from multiple external sensory modalities. However, how these inputs are integrated to jointly control animal behavior is still poorly understood. Whereas visual information alone is not sufficient to induce courtship behavior in Drosophila melanogaster males, when a subset of male-specific fruitless (fru)- and doublesex (dsx)-expressing neurons that respond to chemosensory cues (P1 neurons) were artificially activated via a temperature-sensitive cation channel (dTRPA1), males followed and extended their wing toward moving objects (even a moving piece of rubber band) intensively. When stationary, these objects were not courted. Our results indicate that motion input and activation of P1 neurons are individually necessary, and under our assay conditions, jointly sufficient to elicit early courtship behaviors, and provide insights into how courtship decisions are made via sensory integration.

}, issn = {1091-6490}, doi = {10.1073/pnas.1207107109}, author = {Pan, Yufeng and Meissner, Geoffrey W and Baker, Bruce S} } @article {3357, title = {Turning males on: activation of male courtship behavior in Drosophila melanogaster.}, journal = {PLoS One}, volume = {6}, year = {2011}, month = {2011}, pages = {e21144}, abstract = {

The innate sexual behaviors of Drosophila melanogaster males are an attractive system for elucidating how complex behavior patterns are generated. The potential for male sexual behavior in D. melanogaster is specified by the fruitless (fru) and doublesex (dsx) sex regulatory genes. We used the temperature-sensitive activator dTRPA1 to probe the roles of fru(M)- and dsx-expressing neurons in male courtship behaviors. Almost all steps of courtship, from courtship song to ejaculation, can be induced at very high levels through activation of either all fru(M) or all dsx neurons in solitary males. Detailed characterizations reveal different roles for fru(M) and dsx in male courtship. Surprisingly, the system for mate discrimination still works well when all dsx neurons are activated, but is impaired when all fru(M) neurons are activated. Most strikingly, we provide evidence for a fru(M)-independent courtship pathway that is primarily vision dependent.

}, issn = {1932-6203}, doi = {10.1371/journal.pone.0021144}, author = {Pan, Yufeng and Robinett, Carmen C and Baker, Bruce S} } @article {1225, title = {Differential roles of the fan-shaped body and the ellipsoid body in Drosophila visual pattern memory.}, journal = {Learning \& Memory}, volume = {16}, year = {2009}, month = {2009 Apr 23}, pages = {289-95}, abstract = {

The central complex is a prominent structure in the Drosophila brain. Visual learning experiments in the flight simulator, with flies with genetically altered brains, revealed that two groups of horizontal neurons in one of its substructures, the fan-shaped body, were required for Drosophila visual pattern memory. However, little is known about the role of other components of the central complex for visual pattern memory. Here we show that a small set of neurons in the ellipsoid body, which is another substructure of the central complex and connected to the fan-shaped body, is also required for visual pattern memory. Localized expression of rutabaga adenylyl cyclase in either the fan-shaped body or the ellipsoid body is sufficient to rescue the memory defect of the rut(2080) mutant. We then performed RNA interference of rutabaga in either structure and found that they both were required for visual pattern memory. Additionally, we tested the above rescued flies under several visual pattern parameters, such as size, contour orientation, and vertical compactness, and revealed differential roles of the fan-shaped body and the ellipsoid body for visual pattern memory. Our study defines a complex neural circuit in the central complex for Drosophila visual pattern memory.

}, keywords = {Adenylate Cyclase, Animal, Animals, Behavior, Brain, Classical, Conditioning, Discrimination (Psychology), Drosophila, Drosophila Proteins, Gene Expression, Genetically Modified, Memory, Mutation, Neurons, Orientation, Pattern Recognition, Photic Stimulation, RNA Interference, Visual, Visual Pathways, Visual Perception}, issn = {1549-5485}, doi = {10.1101/lm.1331809}, author = {Pan, Yufeng and Zhou, Yanqiong and Guo, Chao and Gong, Haiyun and Gong, Zhefeng and Liu, Li} } @article {1226, title = {Morphological characterization of single fan-shaped body neurons in Drosophila melanogaster.}, journal = {Cell and Tissue Research}, volume = {336}, year = {2009}, month = {2009 Jun}, pages = {509-19}, abstract = {

The fan-shaped body is the largest substructure of the central complex in Drosophila melanogaster. Two groups of large-field neurons that innervate the fan-shaped body, viz., F1 and F5 neurons, have recently been found to be involved in visual pattern memory for "contour orientation" and "elevation" in a rut-dependent manner. The F5 neurons have been found to be responsible for the parameter "elevation" in a for-dependent manner. We have shown here that the F1 neuron also affects visual memory for "contour orientation" in a for-dependent way. With the help of Gal4/UAS and FLP-out techniques, we have characterized the morphological features of these two groups of neurons at single neuron resolution. We have observed that F1 or F5 neurons are groups of isomorphic individual neurons. Single F1 neurons have three main arborization regions: one in the first layer of the fan-shaped body, one in the ventral body, and another in the inferior medial protocerebrum. Single F5 neurons have two arborization regions: one in the fifth layer of the fan-shaped body and the other in the superior medial protocerebrum. The polarity of the F1 and F5 neurons has been studied with the Syt-GFP marker. Our results indicate the existence of presynaptic sites of both F1 and F5 neurons located in the fan-shaped body and postsynaptic sites outside of the fan-shaped body.

}, keywords = {Animals, Cell Shape, Drosophila melanogaster, Memory, Neurons, Pattern Recognition, Presynaptic Terminals, Visual}, issn = {1432-0878}, doi = {10.1007/s00441-009-0781-2}, author = {Li, Weizhe and Pan, Yufeng and Wang, Zhipeng and Gong, Haiyun and Gong, Zhefeng and Liu, Li} } @article {1227, title = {Visual pattern memory requires foraging function in the central complex of Drosophila.}, journal = {Learning \& Memory}, volume = {15}, year = {2008}, month = {2008 Mar}, pages = {133-42}, abstract = {

The role of the foraging (for) gene, which encodes a cyclic guanosine-3{\textquoteright},5{\textquoteright}-monophosphate (cGMP)-dependent protein kinase (PKG), in food-search behavior in Drosophila has been intensively studied. However, its functions in other complex behaviors have not been well-characterized. Here, we show experimentally in Drosophila that the for gene is required in the operant visual learning paradigm. Visual pattern memory was normal in a natural variant rover (for(R)) but was impaired in another natural variant sitter (for(S)), which has a lower PKG level. Memory defects in for(S) flies could be rescued by either constitutive or adult-limited expression of for in the fan-shaped body. Interestingly, we showed that such rescue also occurred when for was expressed in the ellipsoid body. Additionally, expression of for in the fifth layer of the fan-shaped body restored sufficient memory for the pattern parameter "elevation" but not for "contour orientation," whereas expression of for in the ellipsoid body restored sufficient memory for both parameters. Our study defines a Drosophila model for further understanding the role of cGMP-PKG signaling in associative learning/memory and the neural circuit underlying this for-dependent visual pattern memory.

}, keywords = {Alleles, Animals, Brain, Conditioning, Cyclic GMP-Dependent Protein Kinases, Drosophila melanogaster, Drosophila Proteins, Gene Library, Genetically Modified, Insertional, Isoenzymes, Memory, Mutagenesis, Nerve Tissue Proteins, Operant, Pattern Recognition, Recombinant Fusion Proteins, Short-Term, Visual}, issn = {1549-5485}, doi = {10.1101/lm.873008}, author = {Wang, Zhipeng and Pan, Yufeng and Li, Weizhe and Jiang, Huoqing and Chatzimanolis, Lazaros and Chang, Jianhong and Gong, Zhefeng and Liu, Li} }