Cell Reports
Volume 12, Issue 11, 22 September 2015, Pages 1748-1760
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Article
A Circuit for Gradient Climbing in C. elegans Chemotaxis

https://doi.org/10.1016/j.celrep.2015.08.032Get rights and content
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open access

Highlights

  • AWA sensory neurons and AIA interneurons are tuned to small odor increases

  • AWA has concentration- and history-dependent odor desensitization

  • Amplification and desensitization result in a stereotyped AIA response

  • AWA desensitization requires intraflagellar transport in cilia

Summary

Animals have a remarkable ability to track dynamic sensory information. For example, the nematode Caenorhabditis elegans can locate a diacetyl odor source across a 100,000-fold concentration range. Here, we relate neuronal properties, circuit implementation, and behavioral strategies underlying this robust navigation. Diacetyl responses in AWA olfactory neurons are concentration and history dependent; AWA integrates over time at low odor concentrations, but as concentrations rise, it desensitizes rapidly through a process requiring cilia transport. After desensitization, AWA retains sensitivity to small odor increases. The downstream AIA interneuron amplifies weak odor inputs and desensitizes further, resulting in a stereotyped response to odor increases over three orders of magnitude. The AWA-AIA circuit drives asymmetric behavioral responses to odor increases that facilitate gradient climbing. The adaptation-based circuit motif embodied by AWA and AIA shares computational properties with bacterial chemotaxis and the vertebrate retina, each providing a solution for maintaining sensitivity across a dynamic range.

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This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

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Present address: Department Genes-Circuits-Behavior, Max Planck Institute of Neurobiology, Am Klopferspitz 18, 82152 Martinsried, Germany

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Present address: Department of Biomedical Engineering, Worcester Polytechnic Institute, Worcester, MA 01609, USA