A Circuit for Gradient Climbing in C. elegans Chemotaxis
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...
Main Authors: | , , , , , |
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Format: | Article |
Language: | English |
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Elsevier
2015-09-01
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Series: | Cell Reports |
Online Access: | http://www.sciencedirect.com/science/article/pii/S2211124715009171 |
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author | Johannes Larsch Steven W. Flavell Qiang Liu Andrew Gordus Dirk R. Albrecht Cornelia I. Bargmann |
author_facet | Johannes Larsch Steven W. Flavell Qiang Liu Andrew Gordus Dirk R. Albrecht Cornelia I. Bargmann |
author_sort | Johannes Larsch |
collection | DOAJ |
description | 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. |
first_indexed | 2024-04-13T14:06:11Z |
format | Article |
id | doaj.art-2188d29c001747e2aeb43750aef2c9a3 |
institution | Directory Open Access Journal |
issn | 2211-1247 |
language | English |
last_indexed | 2024-04-13T14:06:11Z |
publishDate | 2015-09-01 |
publisher | Elsevier |
record_format | Article |
series | Cell Reports |
spelling | doaj.art-2188d29c001747e2aeb43750aef2c9a32022-12-22T02:43:54ZengElsevierCell Reports2211-12472015-09-0112111748176010.1016/j.celrep.2015.08.032A Circuit for Gradient Climbing in C. elegans ChemotaxisJohannes Larsch0Steven W. Flavell1Qiang Liu2Andrew Gordus3Dirk R. Albrecht4Cornelia I. Bargmann5Howard Hughes Medical Institute, Lulu and Anthony Wang Laboratory of Neural Circuits and Behavior, The Rockefeller University, New York, NY 10065, USAHoward Hughes Medical Institute, Lulu and Anthony Wang Laboratory of Neural Circuits and Behavior, The Rockefeller University, New York, NY 10065, USAHoward Hughes Medical Institute, Lulu and Anthony Wang Laboratory of Neural Circuits and Behavior, The Rockefeller University, New York, NY 10065, USAHoward Hughes Medical Institute, Lulu and Anthony Wang Laboratory of Neural Circuits and Behavior, The Rockefeller University, New York, NY 10065, USAHoward Hughes Medical Institute, Lulu and Anthony Wang Laboratory of Neural Circuits and Behavior, The Rockefeller University, New York, NY 10065, USAHoward Hughes Medical Institute, Lulu and Anthony Wang Laboratory of Neural Circuits and Behavior, The Rockefeller University, New York, NY 10065, USAAnimals 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.http://www.sciencedirect.com/science/article/pii/S2211124715009171 |
spellingShingle | Johannes Larsch Steven W. Flavell Qiang Liu Andrew Gordus Dirk R. Albrecht Cornelia I. Bargmann A Circuit for Gradient Climbing in C. elegans Chemotaxis Cell Reports |
title | A Circuit for Gradient Climbing in C. elegans Chemotaxis |
title_full | A Circuit for Gradient Climbing in C. elegans Chemotaxis |
title_fullStr | A Circuit for Gradient Climbing in C. elegans Chemotaxis |
title_full_unstemmed | A Circuit for Gradient Climbing in C. elegans Chemotaxis |
title_short | A Circuit for Gradient Climbing in C. elegans Chemotaxis |
title_sort | circuit for gradient climbing in c elegans chemotaxis |
url | http://www.sciencedirect.com/science/article/pii/S2211124715009171 |
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