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Proc Natl Acad Sci U S A. 2016 Mar 8;113(10):E1392-401. doi: 10.1073/pnas.1600786113. Epub 2016 Feb 22.

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

Author information

1
Howard Hughes Medical Institute, California Institute of Technology, Pasadena, CA 91125; Division of Biology and Biological Engineering, California Institute of Technology, Pasadena, CA 91125; Department of Brain and Cognitive Sciences, McGovern Institute for Brain Research, Massachusetts Institute of Technology, Cambridge, MA 02139;
2
Center for Brain Science and Department of Physics, Harvard University, Cambridge, MA 02138;
3
Howard Hughes Medical Institute, California Institute of Technology, Pasadena, CA 91125; Division of Biology and Biological Engineering, California Institute of Technology, Pasadena, CA 91125; Neuroscience Graduate Program, Massachusetts Institute of Technology, Cambridge, MA 02139;
4
Department of Biology and Biotechnology, Worcester Polytechnic Institute, Worcester, MA 01609;
5
Boyce Thompson Institute and Department of Chemistry and Chemical Biology, Cornell University, Ithaca, NY 14853.
6
Howard Hughes Medical Institute, California Institute of Technology, Pasadena, CA 91125; Division of Biology and Biological Engineering, California Institute of Technology, Pasadena, CA 91125; Department of Biology and Biotechnology, Worcester Polytechnic Institute, Worcester, MA 01609; pws@caltech.edu jsrinivasan@wpi.edu.
7
Howard Hughes Medical Institute, California Institute of Technology, Pasadena, CA 91125; Division of Biology and Biological Engineering, California Institute of Technology, Pasadena, CA 91125; pws@caltech.edu jsrinivasan@wpi.edu.

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.

KEYWORDS:

animal behavior; calcium imaging; chemosensation; electrophysiology; population coding

PMID:
26903633
PMCID:
PMC4791020
DOI:
10.1073/pnas.1600786113
[Indexed for MEDLINE]
Free PMC Article

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