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Functional asymmetry in Caenorhabditis elegans taste neurons and its computational role in chemotaxis

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Suzuki, Hiroshi, Thiele, Tod R., Faumont, Serge, Ezcurra, Marina, Lockery, Shawn R., Schafer, William R.·2008·Nature

DOI 10.1038/nature06927PMC PMC2984562

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Abstract

Chemotaxis in Caenorhabditis elegans, like chemotaxis in bacteria, involves a random walk biased by the time derivative of attractant concentration, but how the derivative is computed is unknown. Laser ablations have shown that the strongest deficits in chemotaxis to salts are obtained when the ASE chemosensory neurons (ASEL and ASER) are ablated, indicating that this pair has a dominant role. Although these neurons are left–right homologues anatomically, they exhibit marked asymmetries in gene expression and ion preference. Here, using optical recordings of calcium concentration in ASE neurons in intact animals, we demonstrate an additional asymmetry: ASEL is an ON-cell, stimulated by increases in NaCl concentration, whereas ASER is an OFF-cell, stimulated by decreases in NaCl concentration. Both responses are reliable yet transient, indicating that ASE neurons report changes in concentration rather than absolute levels. Recordings from synaptic and sensory transduction mutants show that the ON–OFF asymmetry is the result of intrinsic differences between ASE neurons. Unilateral activation experiments indicate that the asymmetry extends to the level of behavioural output: ASEL lengthens bouts of forward locomotion (runs) whereas ASER promotes direction changes (turns). Notably, the input and output asymmetries of ASE neurons are precisely those of a simple yet novel neuronal motif for computing the time derivative of chemosensory information, which is the fundamental computation of C. elegans chemotaxis. Evidence for ON and OFF cells in other chemosensory networks suggests that this motif may be common in animals that navigate by taste and smell.

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Authors: Suzuki, H., Thiele, T. R., Faumont, S., Ezcurra, M., Lockery, S. R., & Schafer, W. R.
Affiliations: University of California San Diego (US)
University of Oregon (US)
MRC Laboratory of Molecular Biology (GB)
Corresponding author: Lockery, Shawn R.
ORCID: Suzuki, Hiroshi
Thiele, Tod R.
Faumont, Serge
Ezcurra, Marina
Lockery, Shawn R.
Schafer, William R.
Venue: Nature
Publisher: Springer Science and Business Media LLC
Published: 2008-07
Volume: 454
Issue: 7200
Pages: 114-117
ISSN: 0028-0836 (ISSN-L)
1476-4687
DOI: 10.1038/nature06927
PMC: PMC2984562
OpenAlex: W2003026101
Semantic Scholar: 3c75c57d74fd5e24be78ea6c1d61e14ec4c6194f
Cited by: 256
References: 31
Citations by year: 2026: 10 · 2025: 25 · 2024: 15 · 2023: 10 · 2022: 10 · 2021: 16 · 2020: 11 · 2019: 10 · 2018: 14 · 2017: 12 · 2016: 12 · 2015: 22 · 2014: 13 · 2013: 14 · 2012: 10
FWCI: 7.35
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.springer.com/tdm (tdm)
Locations: Nature (publishedVersion)
PubMed (publishedVersion)
PubMed Central (acceptedVersion)
RePEc: Research Papers in Economics (submittedVersion)
UCL Discovery (University College London) (submittedVersion)
Funders: National Institute of Mental Health (R21MH112105, MH051383, R29MH051383, R01MH051383)
National Institute on Drug Abuse (R01DA016445, DA016445)
Topics: Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurobiology and Insect Physiology Research
Life Sciences › Neuroscience › Sensory Systems › Ion Channels and Receptors
Life Sciences › Biochemistry, Genetics and Molecular Biology › Aging › Genetics, Aging, and Longevity in Model Organisms
Keywords: Caenorhabditis elegans, chemotaxis, salty taste, ASER, forward locomotion, turning behavior, calcium imaging, chemotaxis mutants, bilateral asymmetry, retinal organization
MeSH terms: Animals, Bacterial Proteins, Chemoreceptor Cells, Chemotaxis, Mutation, Neurons, Afferent, Sodium Chloride, Synapses, Taste, Signal Transduction, Caenorhabditis elegans

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Functional asymmetry in Caenorhabditis elegans taste neurons and its computational role in chemotaxis

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