A Circuit for Gradient Climbing in C. elegans Chemotaxis

• Published in: Cell reports (Cambridge) Vol. 12; no. 11; pp. 1748 - 1760
• Main Authors: Larsch, Johannes, Flavell, Steven W., Liu, Qiang, Gordus, Andrew, Albrecht, Dirk R., Bargmann, Cornelia I.
• Format: Journal Article
• Language: English
• Published: United States Elsevier Inc 22.09.2015; Elsevier
• Subjects: Animals; Caenorhabditis elegans - physiology; Caenorhabditis elegans Proteins - physiology; Chemotaxis - physiology; Interneurons - physiology; Odorants; Olfactory Receptor Neurons - physiology; Sensory Receptor Cells - physiology; Signal Transduction
• ISSN: 2211-1247; 2211-1247
• DOI: 10.1016/j.celrep.2015.08.032

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. [Display omitted] •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 Sensory systems detect small changes in stimuli across a vast dynamic range. Larsch et al. identify an olfactory circuit in Caenorhabditis elegans that reports odor increases over a wide concentration range without saturation. Desensitization and amplification produce a stereotyped, asymmetric neuronal response to odor increases and a matching chemotaxis strategy.