Contrasting responses within a single neuron class enable sex-specific attraction in Caenorhabditis elegans
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.
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 We thank Ofer Mazor, Michale Fee, and Vivek Jayaraman for helpful suggestions; Scott Emmons for sharing unpublished information on the male connectome; and Robyn Lints for the generous gift of the ppkd-2::GCAMP6 strain.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.Attached Files
Published - PNAS-2016-Narayan-E1392-401.pdf
Supplemental Material - pnas.1600786113.sapp.pdf
Supplemental Material - pnas.1600786113.sm01.mp4
Supplemental Material - pnas.1600786113.sm02.mp4
Supplemental Material - pnas.201600786SI.pdf
Files
Name | Size | Download all |
---|---|---|
md5:55b4abc5bb535a3290921cd25990b4f6
|
2.0 MB | Preview Download |
md5:1ee8de92f714e7ed5ec63409f3e3637f
|
15.7 MB | Preview Download |
md5:4cc53feea5a6a82400bbf2cdfe6597b9
|
110.2 kB | Download |
md5:ff101319520c2adcf939f6857afda2a5
|
90.8 kB | Download |
md5:afc4e076a0f755f152fd3e15110c9d41
|
64.4 kB | Preview Download |
Additional details
- PMCID
- PMC4791020
- Eprint ID
- 64670
- Resolver ID
- CaltechAUTHORS:20160223-073624632
- NSF
- PHY-0957185
- NIH
- 8DP1GM105383-05
- Worcester Polytechnic Institute
- NIH
- GM085285
- Howard Hughes Medical Institute (HHMI)
- Created
-
2016-02-23Created from EPrint's datestamp field
- Updated
-
2022-05-06Created from EPrint's last_modified field