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Functional asymmetry in Caenorhabditis elegans taste neurons and its computational role in chemotaxis
Open accessAbstract
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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“This is similar to what has been observed in ASE [69].”
From Connecting a Connectome to Behavior: An Ensemble of Neuroanatomical Models of C. elegans Klinotaxis (2013) · cites this paper as [69]
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“Changes in salt concentration were encoded by ON and OFF chemosensory cells [69] using an instantaneous function of a derivative operator applied to the recent history of attractant concentration [94]:”
From Connecting a Connectome to Behavior: An Ensemble of Neuroanatomical Models of C. elegans Klinotaxis (2013) · cites this paper as [69]
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Metadata
- 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.
- Venue
- Nature
- Published
- 2008-07
- Volume
- 454
- Issue
- 7200
- Pages
- 114-117
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- 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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