Abstract
Males and females often produce distinct responses to the same sensory stimuli. How such differences arise—at the level of sensory processing or in the circuits that generate behavior—remains largely unresolved across sensory modalities. We address this issue in the acoustic communication system of Drosophila. During courtship, males generate time-varying songs, and each sex responds with specific behaviors. We characterize male and female behavioral tuning for all aspects of song and show that feature tuning is similar between sexes, suggesting sex-shared song detectors drive divergent behaviors. We then identify higher-order neurons in the Drosophila brain, called pC2, that are tuned for multiple temporal aspects of one mode of the male's song and drive sex-specific behaviors. We thus uncover neurons that are specifically tuned to an acoustic communication signal and that reside at the sensory-motor interface, flexibly linking auditory perception with sex-specific behavioral responses.
| Original language | English |
|---|---|
| Pages (from-to) | 3200-3215.e5 |
| Journal | Current Biology |
| Volume | 29 |
| Issue number | 19 |
| DOIs | |
| State | Published - 7 Oct 2019 |
| Externally published | Yes |
Bibliographical note
Funding Information:We thank Isabel D'Allesandro for help with playback behavioral experiments; Alex Hammons and Nofar Ozeri-Engelhard for help with dissections for immunostaining; Diego Pacheco for help with aligning the volumetric GCaMP scans; Robert Court and Doug Armstrong (http://www.virtualflybrain.org) for help with brain registration; David Stern, Ben Arthur, and Barry Dickson for discussions during the development of the FLyTRAP assay; Kai Feng and Barry Dickson for sharing the design of their playback assay chamber; Bruce Baker, Stephen Goodwin, Gerry Rubin, and Peter Andolfatto for gifts of flies; and Kristin Scott, Asif Ghazanfar, Tim Buschman, and members of the Murthy lab for feedback on the manuscript. J.C. was supported by a postdoctoral fellowship through the Princeton Sloan-Swartz Center and an Emmy Noether grant from the Deutsche Forschungsgemeinschaft (CL 596-1/1). M.M. was supported by an NIH New Innovator award (DP2), NIH NINDS BRAIN Initiative R01 NS104899, and an HHMI Faculty Scholar award. D.D. J.C. and M.M. designed the study. S.Y.T. designed and built the two-photon microscope used for calcium imaging experiments. D.D. J.C. and G.G. collected data. D.D. and J.C. analyzed data and generated figures. D.D. J.C. and M.M. wrote the manuscript. The authors declare no competing interests.
Funding Information:
We thank Isabel D’Allesandro for help with playback behavioral experiments; Alex Hammons and Nofar Ozeri-Engelhard for help with dissections for immunostaining; Diego Pacheco for help with aligning the volumetric GCaMP scans; Robert Court and Doug Armstrong ( http://www.virtualflybrain.org ) for help with brain registration; David Stern, Ben Arthur, and Barry Dickson for discussions during the development of the FLyTRAP assay; Kai Feng and Barry Dickson for sharing the design of their playback assay chamber; Bruce Baker, Stephen Goodwin, Gerry Rubin, and Peter Andolfatto for gifts of flies; and Kristin Scott, Asif Ghazanfar, Tim Buschman, and members of the Murthy lab for feedback on the manuscript. J.C. was supported by a postdoctoral fellowship through the Princeton Sloan-Swartz Center and an Emmy Noether grant from the Deutsche Forschungsgemeinschaft ( CL 596-1/1 ). M.M. was supported by an NIH New Innovator award ( DP2 ), NIH NINDS BRAIN Initiative R01 NS104899 , and an HHMI Faculty Scholar award .
Publisher Copyright:
© 2019 Elsevier Ltd
Keywords
- Drosophila
- acoustic communication
- auditory
- behavior
- courtship
- neural circuits
- pattern recognition
- sensorimotor transformation
- sexually dimorphic
- social experience
- song detection
ASJC Scopus subject areas
- Biochemistry, Genetics and Molecular Biology (all)
- Agricultural and Biological Sciences (all)