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Published January 18, 2012 | Published
Journal Article Open

Neural Representations of Courtship Song in the Drosophila Brain

Abstract

Acoustic communication in drosophilid flies is based on the production and perception of courtship songs, which facilitate mating. Despite decades of research on courtship songs and behavior in Drosophila, central auditory responses have remained uncharacterized. In this study, we report on intracellular recordings from central neurons that innervate the Drosophila antennal mechanosensory and motor center (AMMC), the first relay for auditory information in the fly brain. These neurons produce graded-potential (nonspiking) responses to sound; we compare recordings from AMMC neurons to extracellular recordings of the receptor neuron population [Johnston's organ neurons (JONs)]. We discover that, while steady-state response profiles for tonal and broadband stimuli are significantly transformed between the JON population in the antenna and AMMC neurons in the brain, transient responses to pulses present in natural stimuli (courtship song) are not. For pulse stimuli in particular, AMMC neurons simply low-pass filter the receptor population response, thus preserving low-frequency temporal features (such as the spacing of song pulses) for analysis by postsynaptic neurons. We also compare responses in two closely related Drosophila species, Drosophila melanogaster and Drosophila simulans, and find that pulse song responses are largely similar, despite differences in the spectral content of their songs. Our recordings inform how downstream circuits may read out behaviorally relevant information from central neurons in the AMMC.

Additional Information

© 2012 The Authors. Received October 9, 2011. Accepted November 13, 2011. This work was supported by NIH–NIDCD Grant R01-DC7652 (to Gilles Laurent), funding from the Max Planck Society and a Natural Sciences and Engineering Research Council of Canada PGS-M award (S.T.), and a Helen Hay Whitney postdoctoral fellowship and start-up funds from Princeton University (M.M.). M.M. is also funded through an NSF CAREER award, and through grants from the Human Frontiers Science Program (HFSP) and the Alfred P. Sloan Foundation. We are extremely grateful to Gilles Laurent for critical advice on and funding for this project, to members of the Laurent Laboratory for valuable feedback, to Mark Konishi for donating equipment for fly song recordings, and to Hidehiko Inagaki for help with anatomical characterization of the GAL4 lines used in this study. We also thank Azusa Kamikouchi and Joerg Albert for comments on this manuscript. Author contributions: S.T. and M.M. designed research; P.C., R.K., and M.M. performed research; S.T., P.C., and M.M. analyzed data; M.M. wrote the paper.

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