Journal
JOURNAL OF NEUROSCIENCE
Volume 41, Issue 47, Pages 9732-9741Publisher
SOC NEUROSCIENCE
DOI: 10.1523/JNEUROSCI.1168-21.2021
Keywords
courtship; fixed action pattern; insect; olfaction; pheromone; sexual behavior
Categories
Funding
- Precursory Research for Embryonic Science and Technology (PRESTO) program of the Japan Science and Technology Agency
- Ministry of Education, Culture, Sports, Science, and Technology of Japan [24120509, 22770068, 26830026, 17K07480, 20K06733, 22680026, 18K06329]
- Grants-in-Aid for Scientific Research [22680026, 18K06329, 17K07480, 24120509, 26830026, 22770068, 20K06733] Funding Source: KAKEN
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The study revealed that the courtship behavior in male fruit flies is mediated by specific neurons, which respond to multimodal sensory stimuli and lead to a fixed sequence of behaviors. Furthermore, male flies are able to suppress or promote their courtship actions by receiving specific olfactory stimuli through neurons when in contact with females.
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.
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