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Contrasting responses within a single neuron class enable sex-specific attraction in Caenorhabditis elegans

Narayan, Anusha and Venkatachalam, Vivek and Durak, Omer and Reilly, Douglas K. and Bose, Neelanjan and Schroeder, Frank C. and Samuel, Aravinthan D. T. and Srinivasan, Jagan and Sternberg, Paul W. (2016) Contrasting responses within a single neuron class enable sex-specific attraction in Caenorhabditis elegans. Proceedings of the National Academy of Sciences of the United States of America, 113 (10). E1392-E1401. ISSN 0027-8424. PMCID PMC4791020. http://resolver.caltech.edu/CaltechAUTHORS:20160223-073624632

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Abstract

Animals find mates and food, and avoid predators, by navigating to regions within a favorable range of available sensory cues. How are these ranges set and recognized? Here we show that male Caenorhabditis elegans exhibit strong concentration preferences for sex-specific small molecule cues secreted by hermaphrodites, and that these preferences emerge from the collective dynamics of a single male-specific class of neurons, the cephalic sensory neurons (CEMs). Within a single worm, CEM responses are dissimilar, not determined by anatomical classification and can be excitatory or inhibitory. Response kinetics vary by concentration, suggesting a mechanism for establishing preferences. CEM responses are enhanced in the absence of synaptic transmission, and worms with only one intact CEM show nonpreferential attraction to all concentrations of ascaroside for which CEM is the primary sensor, suggesting that synaptic modulation of CEM responses is necessary for establishing preferences. A heterogeneous concentration-dependent sensory representation thus appears to allow a single neural class to set behavioral preferences and recognize ranges of sensory cues.


Item Type:Article
Related URLs:
URLURL TypeDescription
http://dx.doi.org/10.1073/pnas.1600786113 DOIArticle
http://www.pnas.org/content/113/10/E1392PublisherArticle
http://www.pnas.org/lookup/suppl/doi:10.1073/pnas.1600786113/-/DCSupplementalPublisherSupporting Information
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4791020/PubMed CentralArticle
ORCID:
AuthorORCID
Schroeder, Frank C.0000-0002-4420-0237
Srinivasan, Jagan0000-0001-5449-7938
Sternberg, Paul W.0000-0002-7699-0173
Additional Information:© 2016 National Academy of Sciences. Contributed by Paul W. Sternberg, January 22, 2016 (sent for review July 5, 2015; reviewed by Mala Murthy and Douglas Portman). Published online before print February 22, 2016. We thank Ofer Mazor, Michale Fee, and Vivek Jayaraman for helpful suggestions; Scott Emmons for sharing unpublished information on the male connectome; and Robyn Lints for the generous gift of the ppkd-2::GCAMP6 strain. This work was supported in part by National Science Foundation Grant PHY-0957185 and National Institutes of Health (NIH) Grant 8DP1GM105383-05 (to A.D.T.S.), startup funds from Worcester Polytechnic Institute (to J.S.), NIH Grant GM085285 (to F.C.S. and P.W.S.), and the Howard Hughes Medical Institute, with which P.W.S. is an Investigator. Author contributions: A.N. and J.S. designed research; A.N., O.D., D.K.R., N.B., F.C.S., and J.S. performed research; A.N., V.V., A.D.T.S., J.S., and P.W.S. analyzed data; A.N., V.V., A.D.T.S., J.S., and P.W.S. wrote the paper; and N.B. and F.C.S. synthesized ascr#3 and #8. Reviewers: M.M., Princeton University; and D.P., University of Rochester Medical Center. The authors declare no conflict of interest. This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1600786113/-/DCSupplemental.
Funders:
Funding AgencyGrant Number
NSFPHY-0957185
NIH8DP1GM105383-05
Worcester Polytechnic InstituteUNSPECIFIED
NIHGM085285
Howard Hughes Medical Institute (HHMI)UNSPECIFIED
Subject Keywords:population coding; electrophysiology; chemosensation; calcium imaging; animal behavior
PubMed Central ID:PMC4791020
Record Number:CaltechAUTHORS:20160223-073624632
Persistent URL:http://resolver.caltech.edu/CaltechAUTHORS:20160223-073624632
Official Citation:Anusha Narayan, Vivek Venkatachalam, Omer Durak, Douglas K. Reilly, Neelanjan Bose, Frank C. Schroeder, Aravinthan D. T. Samuel, Jagan Srinivasan, and Paul W. Sternberg Contrasting responses within a single neuron class enable sex-specific attraction in Caenorhabditis elegans PNAS 2016 113 (10) E1392-E1401; published ahead of print February 22, 2016, doi:10.1073/pnas.1600786113
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:64670
Collection:CaltechAUTHORS
Deposited By: Tony Diaz
Deposited On:23 Feb 2016 17:10
Last Modified:18 May 2017 23:00

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