@article{2d9ef6e16aa04e66a8d487b290bd5b98,
title = "Neural network organization for courtship-song feature detection in Drosophila",
abstract = "Animals communicate using sounds in a wide range of contexts, and auditory systems must encode behaviorally relevant acoustic features to drive appropriate reactions. How feature detection emerges along auditory pathways has been difficult to solve due to challenges in mapping the underlying circuits and characterizing responses to behaviorally relevant features. Here, we study auditory activity in the Drosophila melanogaster brain and investigate feature selectivity for the two main modes of fly courtship song, sinusoids and pulse trains. We identify 24 new cell types of the intermediate layers of the auditory pathway, and using a new connectomic resource, FlyWire, we map all synaptic connections between these cell types, in addition to connections to known early and higher-order auditory neurons—this represents the first circuit-level map of the auditory pathway. We additionally determine the sign (excitatory or inhibitory) of most synapses in this auditory connectome. We find that auditory neurons display a continuum of preferences for courtship song modes and that neurons with different song-mode preferences and response timescales are highly interconnected in a network that lacks hierarchical structure. Nonetheless, we find that the response properties of individual cell types within the connectome are predictable from their inputs. Our study thus provides new insights into the organization of auditory coding within the Drosophila brain.",
keywords = "acoustic communication, auditory, calcium imaging, connectomics, neural network, sensory responses",
author = "Baker, {Christa A.} and Claire McKellar and Rich Pang and Aljoscha Nern and Sven Dorkenwald and Pacheco, {Diego A.} and Nils Eckstein and Jan Funke and Dickson, {Barry J.} and Mala Murthy",
note = "Funding Information: We thank Xiao-Juan Guan for help with crosses; David Deutsch for help with calcium imaging pre-analysis and for identifying pC2l neurons in FlyWire; Stephan Thiberge for help with two-photon imaging; Sebastian Seung for assistance with FlyWire infrastructure; Greg Jefferis for feedback on the cell type naming scheme; Alex Bates and Greg Jefferis for helpful discussions and ideas with regard to neurotransmitter analysis; Nat Tabris and Arie Matsliah for help with connectivity analysis; Lucas Encarnacion-Rivera, Ben Silverman, Jay Gager, Merlin Moore, Selden Koolman, James Hebditch, Sarah Morejohn, Kyle Willie, Austin Burke, Celia David, Ryan Willie, Sandeep Kumar, Doug Bland, Shirleyjoy Serona, J. Anthony Ocho, Nash Hadjerol, Zhihao Zheng, Szi-chieh Yu, Stefanie Hampel, Lucia Kmecova, Fernando J. Figueroa Santiago, Fabianna Szorenyi, Yijie Yin, Imaan Tamimi, Varun Sane, Siqi Fang, Griffin Badalemente, Laia Serratosa Capdevila, Greg Jefferis, Katharina Eichler, Alexander Bates, Irene Salgarella, Marlon Blanquart, A. Javier, Arti Yadav, Joseph Hsu, and Kyle Thieringer for proofreading FlyWire neurons; Marta Costa, Jan Clemens, and Istvan Taisz for comments on the manuscript; and the Janelia Fly Core, FlyLight, and Scientific Computing groups. A.N. thanks Gerry Rubin, in whose lab he performed this work, for his support and encouragement. We acknowledge funding from the Jane Coffin Childs Memorial Fund for Medical Research (to C.A.B.); NIH NINDS DP2 New Innovator Award, HHMI Faculty Scholar Award, and NIH BRAIN Initiative R01 MH117815-01 (to M.M.); and the Howard Hughes Medical Institute (to C.M. A.N. N.E. J.F. and B.J.D.). Conceptualization, C.A.B. C.M. and M.M.; methodology, C.A.B. D.A.P. S.D. R.P. and M.M.; investigation, C.A.B. C.M. A.N. N.E. J.F. and B.J.D.; formal analysis, C.A.B. R.P. D.A.P. and S.D.; visualization, C.A.B. C.M. and R.P.; writing – original draft, C.A.B. R.P. C.M. and M.M.; writing – review & editing, C.A.B. and M.M. with feedback from all authors. The authors declare no competing interests. Funding Information: We thank Xiao-Juan Guan for help with crosses; David Deutsch for help with calcium imaging pre-analysis and for identifying pC2l neurons in FlyWire; Stephan Thiberge for help with two-photon imaging; Sebastian Seung for assistance with FlyWire infrastructure; Greg Jefferis for feedback on the cell type naming scheme; Alex Bates and Greg Jefferis for helpful discussions and ideas with regard to neurotransmitter analysis; Nat Tabris and Arie Matsliah for help with connectivity analysis; Lucas Encarnacion-Rivera, Ben Silverman, Jay Gager, Merlin Moore, Selden Koolman, James Hebditch, Sarah Morejohn, Kyle Willie, Austin Burke, Celia David, Ryan Willie, Sandeep Kumar, Doug Bland, Shirleyjoy Serona, J. Anthony Ocho, Nash Hadjerol, Zhihao Zheng, Szi-chieh Yu, Stefanie Hampel, Lucia Kmecova, Fernando J. Figueroa Santiago, Fabianna Szorenyi, Yijie Yin, Imaan Tamimi, Varun Sane, Siqi Fang, Griffin Badalemente, Laia Serratosa Capdevila, Greg Jefferis, Katharina Eichler, Alexander Bates, Irene Salgarella, Marlon Blanquart, A. Javier, Arti Yadav, Joseph Hsu, and Kyle Thieringer for proofreading FlyWire neurons; Marta Costa, Jan Clemens, and Istvan Taisz for comments on the manuscript; and the Janelia Fly Core, FlyLight, and Scientific Computing groups. A.N. thanks Gerry Rubin, in whose lab he performed this work, for his support and encouragement. We acknowledge funding from the Jane Coffin Childs Memorial Fund for Medical Research (to C.A.B.); NIH NINDS DP2 New Innovator Award, HHMI Faculty Scholar Award, and NIH BRAIN Initiative R01 MH117815-01 (to M.M.); and the Howard Hughes Medical Institute (to C.M., A.N., N.E., J.F., and B.J.D.). Publisher Copyright: {\textcopyright} 2022 The Authors",
year = "2022",
month = aug,
day = "8",
doi = "10.1016/j.cub.2022.06.019",
language = "English (US)",
volume = "32",
pages = "3317--3333.e7",
journal = "Current Biology",
issn = "0960-9822",
publisher = "Cell Press",
number = "15",
}