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J Neurosci


Title:A Sexually Dimorphic Olfactory Neuron Mediates Fixed Action Transition during Courtship Ritual in Drosophila melanogaster
Author(s):Tanaka NK; Hirao T; Chida H; Ejima A;
Address:"Division of Biology, Department of Biological Sciences, School of Science, Hokkaido University, Sapporo 060-0810, Japan nktanaka@sci.hokudai.ac.jp aki@g.ecc.u-tokyo.ac.jp. Faculty of Science, Hokkaido University, Sapporo 060-0810, Japan. Graduate School of Life Sciences, Hokkaido University, Sapporo 060-0810, Japan. Career-Path Promotion Unit for Young Life Scientists, Kyoto University, Kyoto 606-8501, Japan. Division of Biology, Department of Biological Sciences, School of Science, Hokkaido University, Sapporo 060-0810, Japan. Career-Path Promotion Unit for Young Life Scientists, Kyoto University, Kyoto 606-8501, Japan nktanaka@sci.hokudai.ac.jp aki@g.ecc.u-tokyo.ac.jp. Institute for Quantitative Biosciences, University of Tokyo, Tokyo 113-0032, Japan"
Journal Title:J Neurosci
Year:2021
Volume:20211014
Issue:47
Page Number:9732 - 9741
DOI: 10.1523/JNEUROSCI.1168-21.2021
ISSN/ISBN:1529-2401 (Electronic) 0270-6474 (Print) 0270-6474 (Linking)
Abstract:"Animals perform a series of actions in a fixed order during ritualistic innate behaviors. Although command neurons and sensory pathways responding to external stimuli that trigger these behaviors have been identified, how each action is induced in a fixed order in response to multimodal sensory stimuli remains unclear. Here, the sexually dimorphic lateral antennal lobe tract projection neuron 4 (lPN4) in male Drosophila melanogaster mediates the expression of a fixed behavioral action pattern at the beginning of the courtship ritual, in which a male taps a female body and then extends a wing unilaterally to produce a courtship song. We found that blocking the synaptic output of lPN4 caused an increase in the ratio of male flies that extended a wing unilaterally without tapping the female body, whereas excitation of lPN4 suppressed the transition from the tapping phase to the unilateral wing extension phase. Real-time calcium imaging showed that lPN4 is activated by a volatile pheromone, palmitoleic acid, whose responses were inhibited by simultaneous gustatory stimulation with female cuticular hydrocarbons, showing the existence of an 'AND-gate' for multimodal sensory inputs during male courtship behaviors. These results suggest that the function of lPN4 is to suppress unilateral wing extension while responding to a female smell, which is released by appropriate contact chemosensory inputs received when tapping a female. As the female smell also promotes male courtship behaviors, the olfactory system is ready to simultaneously promote and suppress the progress of courtship actions while responding to a female smell.SIGNIFICANCE STATEMENT Although it has been 80 years since Konrad Lorenz and Niko Tinbergen introduced how multiple acts comprising separate innate behaviors are released in a fixed order according to external stimuli, the neural circuits responsible for such fixed action patterns remain largely unknown. The male courtship behavior of Drosophila melanogaster is a good model to investigate how such a fixed behavioral sequence is determined in the brain. Here, we show that lateral antennal lobe tract projection neuron 4 (lPN4) in D. melanogaster functions as an 'AND-gate' for volatile and contact chemosensory inputs, mediating the expression of tapping behaviors before unilateral wing extension during male courtship rituals"
Keywords:"Animals;Animals *Courtship Drosophila melanogaster/*physiology Female *Instinct Male Neurons/*physiology Olfactory Pathways/*physiology Sex Characteristics Sexual Behavior, Animal/physiology courtship fixed action pattern insect olfaction pheromone sexual behavio;"
Notes:"MedlineTanaka, Nobuaki K Hirao, Takashi Chida, Hikaru Ejima, Aki eng Research Support, Non-U.S. Gov't 2021/10/16 J Neurosci. 2021 Nov 24; 41(47):9732-9741. doi: 10.1523/JNEUROSCI.1168-21.2021. Epub 2021 Oct 14"

 
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