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PDF-1 neuropeptide signaling modulates a neural circuit for mate-searching behavior in C. elegans

Abstract

Appetitive behaviors require complex decision making that involves the integration of environmental stimuli and physiological needs. C. elegans mate searching is a male-specific exploratory behavior regulated by two competing needs: food and reproductive appetite. We found that the pigment dispersing factor receptor (PDFR-1) modulates the circuit that encodes the male reproductive drive that promotes male exploration following mate deprivation. PDFR-1 and its ligand, PDF-1, stimulated mate searching in the male, but not in the hermaphrodite. pdf-1 was required in the gender-shared interneuron AIM, and the receptor acted in internal and external environment-sensing neurons of the shared nervous system (URY, PQR and PHA) to produce mate-searching behavior. Thus, the pdf-1 and pdfr-1 pathway functions in non–sex-specific neurons to produce a male-specific, goal-oriented exploratory behavior. Our results indicate that secretin neuropeptidergic signaling is involved in regulating motivational internal states.

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Figure 1: PDF-1 neuropeptide signaling stimulates mate searching.
Figure 2: The PDF-1 and PDFR-1 pathway stimulates dispersal following mate deprivation.
Figure 3: Mate sensation and ray activity modulate the effects of PDF-1 signaling.
Figure 4: pdfr-1 is required in sensory neurons URY, PQR and PHA to produce mate-searching behavior.
Figure 5: The interneuron AIM is a source of PDF-1 for mate-searching behavior.

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Acknowledgements

We thank the Maricq (University of Utah), Rongo (Rutgers University) and Hobert (Columbia University) laboratories for strains and reagents, and the Mitani laboratory (Tokyo Women's Medical College) and Japan's National BioResource Project for mutants. Additional strains were obtained from the Caenorhabditis Genetics Center. We thank R. Poole and members of the Barr laboratory for advice and many helpful discussions on the manuscript and L. Vaynerchuk for experimental aid. This research was supported by US National Institutes of Health grant 2R01DK059418 to M.M.B.

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A.B. designed and performed the experiments and co-wrote the manuscript. R.G. performed the genetic screen. C.F. contributed to mapping process. S.W.E. and M.M.B. co-wrote and discussed the manuscript with A.B.

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Correspondence to Arantza Barrios.

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Barrios, A., Ghosh, R., Fang, C. et al. PDF-1 neuropeptide signaling modulates a neural circuit for mate-searching behavior in C. elegans. Nat Neurosci 15, 1675–1682 (2012). https://doi.org/10.1038/nn.3253

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