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Sex-specific topology of the nociceptive circuit shapes dimorphic behavior in C. elegans

Vladyslava Pechuk, View ORCID ProfileYehuda Salzberg, Gal Goldman, Aditi H. Chaubey, R. Aaron Bola, Jonathon R. Hoffman, Morgan L. Endreson, Renee M. Miller, Noah J. Reger, View ORCID ProfileDouglas S. Portman, Denise M. Ferkey, View ORCID ProfileElad Schneidman, View ORCID ProfileMeital Oren-Suissa
doi: https://doi.org/10.1101/2021.12.14.472335
Vladyslava Pechuk
1Department of Brain Sciences, Weizmann Institute of Science, Rehovot, 7610001, Israel
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Yehuda Salzberg
1Department of Brain Sciences, Weizmann Institute of Science, Rehovot, 7610001, Israel
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  • ORCID record for Yehuda Salzberg
Gal Goldman
1Department of Brain Sciences, Weizmann Institute of Science, Rehovot, 7610001, Israel
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Aditi H. Chaubey
2Department of Biological Sciences, University at Buffalo, The State University of New York, Buffalo, NY 14260 USA
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R. Aaron Bola
2Department of Biological Sciences, University at Buffalo, The State University of New York, Buffalo, NY 14260 USA
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Jonathon R. Hoffman
2Department of Biological Sciences, University at Buffalo, The State University of New York, Buffalo, NY 14260 USA
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Morgan L. Endreson
2Department of Biological Sciences, University at Buffalo, The State University of New York, Buffalo, NY 14260 USA
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Renee M. Miller
3Department of Biomedical Genetics, University of Rochester, Rochester, NY 14642 USA
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Noah J. Reger
3Department of Biomedical Genetics, University of Rochester, Rochester, NY 14642 USA
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Douglas S. Portman
3Department of Biomedical Genetics, University of Rochester, Rochester, NY 14642 USA
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Denise M. Ferkey
2Department of Biological Sciences, University at Buffalo, The State University of New York, Buffalo, NY 14260 USA
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Elad Schneidman
1Department of Brain Sciences, Weizmann Institute of Science, Rehovot, 7610001, Israel
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  • For correspondence: meital.oren@weizmann.ac.il Elad.Schneidman@weizmann.ac.il
Meital Oren-Suissa
1Department of Brain Sciences, Weizmann Institute of Science, Rehovot, 7610001, Israel
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  • ORCID record for Meital Oren-Suissa
  • For correspondence: meital.oren@weizmann.ac.il Elad.Schneidman@weizmann.ac.il
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SUMMARY

How sexually dimorphic behavior is encoded in the nervous system is poorly understood. Here, we characterize the dimorphic nociceptive behavior in C. elegans and study the underlying circuits, which are composed of the same neurons but are wired differently. We show that while sensory transduction is similar in the two sexes, the downstream network topology markedly shapes behavior. We fit a network model that replicates the observed dimorphic behavior in response to external stimuli, and use it to predict simple network rewirings that would switch the behavior between the sexes. We then show experimentally that these subtle synaptic rewirings indeed flip behavior. Strikingly, when presented with aversive cues, rewired males were compromised in finding mating partners, suggesting that network topologies that enable efficient avoidance of noxious cues have a reproductive “cost”. Our results present a deconstruction of the design of a neural circuit that controls sexual behavior, and how to reprogram it.

Competing Interest Statement

The authors have declared no competing interest.

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Posted December 15, 2021.
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Sex-specific topology of the nociceptive circuit shapes dimorphic behavior in C. elegans
Vladyslava Pechuk, Yehuda Salzberg, Gal Goldman, Aditi H. Chaubey, R. Aaron Bola, Jonathon R. Hoffman, Morgan L. Endreson, Renee M. Miller, Noah J. Reger, Douglas S. Portman, Denise M. Ferkey, Elad Schneidman, Meital Oren-Suissa
bioRxiv 2021.12.14.472335; doi: https://doi.org/10.1101/2021.12.14.472335
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Sex-specific topology of the nociceptive circuit shapes dimorphic behavior in C. elegans
Vladyslava Pechuk, Yehuda Salzberg, Gal Goldman, Aditi H. Chaubey, R. Aaron Bola, Jonathon R. Hoffman, Morgan L. Endreson, Renee M. Miller, Noah J. Reger, Douglas S. Portman, Denise M. Ferkey, Elad Schneidman, Meital Oren-Suissa
bioRxiv 2021.12.14.472335; doi: https://doi.org/10.1101/2021.12.14.472335

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