DOI: 10.1242/dev.126.9.1891. Sensory activity affects sensory axon development in <i>C. elegans</i>

Sensory activity affects sensory axon development in C. elegans

10.1242/dev.126.9.1891

Crossref journal-article

The Company of Biologists

Development (237)

Abstract

Abstract The simple nervous system of the nematode C. elegans consists of 302 neurons with highly reproducible morphologies, suggesting a hard-wired program of axon guidance. Surprisingly, we show here that sensory activity shapes sensory axon morphology in C. elegans. A class of mutants with deformed sensory cilia at their dendrite endings have extra axon branches, suggesting that sensory deprivation disrupts axon outgrowth. Mutations that alter calcium channels or membrane potential cause similar defects. Cell-specific perturbations of sensory activity can cause cell-autonomous changes in axon morphology. Although the sensory axons initially reach their targets in the embryo, the mutations that alter sensory activity cause extra axon growth late in development. Thus, perturbations of activity affect the maintenance of sensory axon morphology after an initial pattern of innervation is established. This system provides a genetically tractable model for identifying molecular mechanisms linking neuronal activity to nervous system structure.

Bibliography

Peckol, E. L., Zallen, J. A., Yarrow, J. C., & Bargmann, C. I. (1999). Sensory activity affects sensory axon development in C. elegans. Development, 126(9), 1891â1902.

Authors 4

Erin L. Peckol (first)
Jennifer A. Zallen (additional)
Justin C. Yarrow (additional)
Cornelia I. Bargmann (additional)

References 73 Referenced 79

10.1002/cne.902190407 / J. Comp. Neurol / Developmental alterations in sensory neuroanatomy of the Caenorhabditis elegans dauer larva by Albert (1983)
10.1523/JNEUROSCI.13-08-03549.1993 / J. Neurosci / Development of individual geniculocortical arbors in cat striate cortex and effects of binocular impulse blockade by Antonini (1993)
10.1093/genetics/133.4.897 / Genetics / The genetics of feeding in Caenorhabditis elegans by Avery (1993)
10.1093/genetics/134.2.455 / Genetics / The Caenorhabditis elegans unc-31 gene affects multiple nervous system-controlled functions by Avery (1993)
10.1016/0092-8674(93)80053-H / Cell / Odorant-selective genes and neurons mediate olfaction in C. elegans by Bargmann (1993)
{'key': '2023090605553163200_DEVELOP_126_9_1891C6', 'first-page': '717', 'article-title': 'Chemotaxis and thermotaxis', 'volume-title': 'C. elegans II', 'author': 'Bargmann', 'year': '1997'} / C. elegans II / Chemotaxis and thermotaxis by Bargmann (1997)
10.1002/j.1460-2075.1988.tb03092.x / EMBO J / Structure of the voltage-dependent potassium channel is highly conserved from Drosophila to vertebrate central nervous systems by Baumann (1988)
10.1042/bst0240661 / Biochem Soc Trans / Mammalian unc-13 homologues as possible regulators of neurotransmitter release by Betz (1996)
10.1093/genetics/77.1.71 / Genetics / The genetics of Caenorhabditis elegans by Brenner (1974)
10.1016/0896-6273(93)90073-Z / Neuron / Activity-dependent development of the neuromuscular synapse during Drosophila embryogenesis by Broadie (1993)
10.1523/JNEUROSCI.06-10-02968.1986 / J. Neurosci / Differentiation and central projections of peripheral sensory cells with action-potential block in Drosophila mosaics by Burg (1986)
10.1002/neu.480220204 / J. Neurobiol / Connectivity of identified central synapses in the cricket is normal following regeneration and blockade of presynaptic activity by Chiba (1991)
10.1016/S0896-6273(00)80201-9 / Neuron / A putative cyclic nucleotide-gated channel is required for sensory development and function in C. elegans by Coburn (1996)
10.1242/dev.125.2.249 / Development / A cyclic nucleotide-gated channel inhibits sensory axon outgrowth in larval and adult Caenorhabditis elegans: a distinct pathway for maintenance of sensory axon structure by Coburn (1998)
10.1083/jcb.141.4.993 / J. Cell Biol / Chlamydomonas kinesin-II-dependent intraflaggellar transport (IFT): IFT particles contain proteins required for cilia assembly in Caenorhabditis elegans sensory neurons by Cole (1998)
10.1093/genetics/148.1.187 / Genetics / Analysis of osm-6, a gene that affects sensory cilium structure and sensory neuron function in Caenorhabditis elegans by Collet (1998)
10.1126/science.279.5350.566 / Science / The role of visual experience in the development of columns in cat visual cortex by Crair (1998)
10.1038/32176 / Nature / Synapse-specific control of synaptic efficacy at the terminals of a single neuron by Davis (1998)
10.1523/JNEUROSCI.15-12-08408.1995 / J. Neurosci / Mutations in the Caenorhabditis elegans Na,K-ATPase alpha-subunit gene, eat-6, disrupt excitable cell function by Davis (1995)
10.1016/S0092-8674(00)81173-3 / Cell / Odorant receptor localization to olfactory cilia is mediated by ODR-4, a novel membrane-associated protein by Dwyer (1998)
10.1523/JNEUROSCI.12-05-01826.1992 / J. Neurosci / A critical period for experience-dependent synaptic plasticity in rat barrel cortex by Fox (1992)
10.1073/pnas.93.11.5584 / Proc. Natl. Acad. Sci. USA / Glutamate receptor blockade at cortical synapses disrupts development of thalamocortical and columnar organization in somatosensory cortex by Fox (1996)
10.1016/S0092-8674(05)80030-3 / Cell / Developmental mechanisms that generate precise patterns of neuronal connectivity by Goodman (1993)
10.1016/S0896-6273(00)81014-4 / Neuron / Active currents regulate sensitivity and dynamic range in C. elegans neurons by Goodman (1998)
{'key': '2023090605553163200_DEVELOP_126_9_1891C25', 'first-page': '1227', 'article-title': 'Pharmacological characterization of five cloned voltage-gated K+ channels, types Kv1. 1, 1.2, 1.3, 1.5, and 3.1, stably expressed in mammalian cell lines', 'volume': '45', 'author': 'Grissmer', 'year': '1994', 'journal-title': 'Mol. Pharmacol'} / Mol. Pharmacol / Pharmacological characterization of five cloned voltage-gated K+ channels, types Kv1. 1, 1.2, 1.3, 1.5, and 3.1, stably expressed in mammalian cell lines by Grissmer (1994)
10.1016/0092-8674(91)90391-B / Cell / Kinesin-related gene unc-104 is required for axonal transport of synaptic vesicles in C. elegans by Hall (1991)
10.1002/cne.901960302 / J. Comp. Neurol / Dendritic plasticity in mouse barrel cortex following postnatal vibrissa follicle damage by Harris (1981)
10.1038/366347a0 / Nature / Synaptic vesicle fusion complex contains unc-18 homologue bound to syntaxin by Hata (1993)
10.1093/genetics/116.3.377 / Genetics / Mosaic analysis of two genes that affect nervous system structure in Caenorhabditis elegans by Herman (1987)
10.1038/348169a0 / Nature / Limitation of the size of the vulval primordium of Caenorhabditis elegans by lin-15 expression in surrounding hypodermis by Herman (1990)
10.1111/j.1471-4159.1992.tb11373.x / J. Neurochem / The unc-18 gene encodes a novel protein affecting the kinetics of acetylcholine metabolism in the nematode Caenorhabditis elegans by Hosono (1992)
10.1091/mbc.5.4.395 / Mol. Biol. Cell / The lin-15 locus encodes two negative regulators of Caenorhabditis elegans vulval development by Huang (1994)
10.1098/rstb.1977.0050 / Philos. Trans. R. Soc. Lond. B Biol. Sci / Plasticity of ocular dominance columns in monkey striate cortex by Hubel (1977)
10.1523/JNEUROSCI.15-12-08177.1995 / J. Neurosci / Role of neural activity during synaptogenesis in Drosophila by Jarecki (1995)
10.1038/378196a0 / Nature / Defective recycling of synaptic vesicles in synaptotagmin mutants of Caenorhabditis elegans by Jorgensen (1995)
10.1073/pnas.90.6.2227 / Proc. Natl. Acad. Sci. USA / A dual mechanosensory and chemosensory neuron in Caenorhabditis elegans by Kaplan (1993)
10.1126/science.2443978 / Science / Blockade of ‘NMDA’ receptors disrupts experience-dependent plasticity of kitten striate cortex by Kleinschmidt (1987)
10.1016/S0006-8993(99)01111-7 / Brain Res / Functional reconstitution of a heteromeric cyclic nucleotide-gated channel of C. elegans in cultured cells by Komatsu (1999)
10.1016/S0896-6273(00)80202-0 / Neuron / Mutations in a cyclic nucleotide-gated channel lead to abnormal thermosensation and chemosensation in C. elegans by Komatsu (1996)
10.1093/emboj/16.20.6066 / EMBO J / Mutations in the alpha1 subunit of an L-type voltage-activated Ca2+ channel cause myotonia in Caenorhabditis elegans by Lee (1997)
10.1002/cne.901910102 / J. Comp. Neurol / The development of ocular dominance columns in normal and visually deprived monkeys by LeVay (1980)
10.1002/cne.901720306 / J. Comp. Neurol / Specific neuroanatomical changes in chemosensory mutants of the nematode Caenorhabditis elegans by Lewis (1977)
10.1016/0092-8674(94)90108-2 / Cell / Whisker-related neuronal patterns fail to develop in the trigeminal brainstem nuclei of NMDAR1 knockout mice by Li (1994)
10.1038/378078a0 / Nature / Mechanosensory signalling in C. elegans mediated by the GLR-1 glutamate receptor by Maricq (1995)
10.1073/pnas.88.13.5729 / Proc. Natl. Acad. Sci. USA / A phorbol ester/diacylglycerol-binding protein encoded by the unc-13 gene of Caenorhabditis elegans by Maruyama (1991)
10.1016/S0091-679X(08)61396-5 / Caenorhabditis elegans: Modern Biological Analysis of an Organism / Immunofluorescence microscopy by Miller (1995)
10.1073/pnas.86.13.5183 / Proc. Natl. Acad. Sci. USA / Visual responses in adult cat visual cortex depend on N-methyl-D-aspartate receptors by Miller (1989)
10.1016/0092-8674(93)90357-V / Cell / Synaptic function is impaired but not eliminated in C. elegans mutants lacking synaptotagmin by Nonet (1993)
10.1016/0896-6273(91)90126-K / Neuron / The C. elegans unc-104 gene encodes a putative kinesin heavy chain-like protein by Otsuka (1991)
10.1016/0012-1606(86)90314-3 / Dev. Biol / Mutant sensory cilia in the nematode Caenorhabditis elegans by Perkins (1986)
10.1016/S0092-8674(00)81068-5 / Cell / odr-10 encodes a seven transmembrane domain olfactory receptor required for responses to the odorant diacetyl by Sengupta (1996)
10.1016/0736-5748(94)90061-2 / Int. J. Dev. Neurosci / Viktor Hamburger Award review. Role for spontaneous neural activity in the patterning of connections between retina and LGN during visual system development by Shatz (1994)
10.1073/pnas.93.2.602 / Proc. Natl. Acad. Sci. USA / Emergence of order in visual system development by Shatz (1996)
10.1113/jphysiol.1978.sp012421 / J. Physiol / Ocular dominance in layer IV of the cat’s visual cortex and the effects of monocular deprivation by Shatz (1978)
10.1126/science.3175636 / Science / Prenatal tetrodotoxin infusion blocks segregation of retinogeniculate afferents by Shatz (1988)
10.1038/336468a0 / Nature / Modification of retinal ganglion cell axon morphology by prenatal infusion of tetrodotoxin by Sretavan (1988)
10.1093/genetics/139.1.171 / Genetics / Mutations affecting the chemosensory neurons of Caenorhabditis elegans by Starich (1995)
10.1523/JNEUROSCI.06-08-02117.1986 / J. Neurosci / Binocular impulse blockade prevents the formation of ocular dominance columns in cat visual cortex by Stryker (1986)
10.1002/j.1460-2075.1989.tb08483.x / EMBO J / Molecular basis of functional diversity of voltage-gated potassium channels in mammalian brain by Stuhmer (1989)
10.1016/0012-1606(83)90201-4 / Dev. Biol / The embryonic cell lineage of the nematode Caenorhabditis elegans by Sulston (1983)
10.1038/332837a0 / Nature / Cloning of a probable potassium channel gene from mouse brain by Tempel (1988)
10.1016/S0092-8674(00)81993-5 / Cell / Regions responsible for the assembly of inwardly rectifying potassium channels by Tinker (1996)
10.1016/0092-8674(95)90162-0 / Cell / Divergent seven transmembrane receptors are candidate chemosensory receptors in C. elegans by Troemel (1995)
10.1016/S0092-8674(00)80399-2 / Cell / Reprogramming chemotaxis responses: sensory neurons define olfactory preferences in C. elegans by Troemel (1997)
10.1093/genetics/138.2.303 / Genetics / Multiple chemosensory defects in daf-11 and daf-21 mutants of Caenorhabditis elegans by Vowels (1994)
10.1002/cne.901600305 / J. Comp. Neurol / Electron microscopical reconstruction of the anterior sensory anatomy of the nematode Caenorhabditis elegans by Ward (1975)
10.1002/cne.901620106 / J. Comp. Neurol / The nerve ring of the nematode Caenorhabditis elegans: sensory input and motor output by Ware (1975)
10.1016/0028-3908(96)00126-8 / Neuropharmacology / Eight potassium channel families revealed by the C. elegans genome project by Wei (1996)
10.1038/271764a0 / Nature / Connectivity changes in a class of motoneurone during the development of a nematode by White (1978)
10.1098/rstb.1986.0056 / Philos. Trans. R. Soc. Lond. B Biol. Sci / The structure of the nervous system of the nematode Caenorhabditis elegans by White (1986)
10.1073/pnas.94.7.3384 / Proc. Natl. Acad. Sci. USA / Guanylyl cyclase expression in specific sensory neurons: a new family of chemosensory receptors by Yu (1997)
10.1016/S0092-8674(00)80916-2 / Cell / The conserved immunoglobulin superfamily member SAX-3/Robo directs multiple aspects of axon guidance in C. elegans by Zallen (1998)
10.1523/JNEUROSCI.12-02-00644.1992 / J. Neurosci / Synaptic plasticity in Drosophila memory and hyperexcitable mutants: role of cAMP cascade by Zhong (1992)

Dates

Type	When
Created	4 years, 4 months ago (April 26, 2021, 12:03 a.m.)
Deposited	1 year, 11 months ago (Sept. 6, 2023, 1:55 a.m.)
Indexed	2 months ago (July 2, 2025, 2:48 p.m.)
Issued	26 years, 4 months ago (May 1, 1999)
Published	26 years, 4 months ago (May 1, 1999)
Published Online	26 years, 4 months ago (May 1, 1999)
Published Print	26 years, 4 months ago (May 1, 1999)

Funders 0

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BibTeX

@article{Peckol_1999, title={Sensory activity affects sensory axon development in C. elegans}, volume={126}, ISSN={1477-9129}, url={http://dx.doi.org/10.1242/dev.126.9.1891}, DOI={10.1242/dev.126.9.1891}, number={9}, journal={Development}, publisher={The Company of Biologists}, author={Peckol, Erin L. and Zallen, Jennifer A. and Yarrow, Justin C. and Bargmann, Cornelia I.}, year={1999}, month=may, pages={1891–1902} }

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      "author": "Albert",
      "year": "1983",
      "journal-title": "J. Comp. Neurol"
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      "volume": "13",
      "author": "Antonini",
      "year": "1993",
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      "volume": "134",
      "author": "Avery",
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      "author": "Bargmann",
      "year": "1993",
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      "article-title": "Chemotaxis and thermotaxis",
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      "author": "Davis",
      "year": "1998",
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      "volume": "12",
      "author": "Fox",
      "year": "1992",
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      "volume": "93",
      "author": "Fox",
      "year": "1996",
      "journal-title": "Proc. Natl. Acad. Sci. USA"
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      "article-title": "Developmental mechanisms that generate precise patterns of neuronal connectivity",
      "volume": "72",
      "author": "Goodman",
      "year": "1993",
      "journal-title": "Cell"
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      "author": "Goodman",
      "year": "1998",
      "journal-title": "Neuron"
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      "volume": "45",
      "author": "Grissmer",
      "year": "1994",
      "journal-title": "Mol. Pharmacol"
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      "author": "Hall",
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      "volume": "196",
      "author": "Harris",
      "year": "1981",
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      "author": "Hata",
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      "author": "Herman",
      "year": "1987",
      "journal-title": "Genetics"
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      "volume": "348",
      "author": "Herman",
      "year": "1990",
      "journal-title": "Nature"
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      "volume": "58",
      "author": "Hosono",
      "year": "1992",
      "journal-title": "J. Neurochem"
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      "volume": "5",
      "author": "Huang",
      "year": "1994",
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      "author": "Hubel",
      "year": "1977",
      "journal-title": "Philos. Trans. R. Soc. Lond. B Biol. Sci"
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      "author": "Jarecki",
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      "author": "Jorgensen",
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      "volume": "90",
      "author": "Kaplan",
      "year": "1993",
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      "volume": "238",
      "author": "Kleinschmidt",
      "year": "1987",
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      "volume-title": "Brain Res",
      "author": "Komatsu",
      "year": "1999"
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      "author": "Komatsu",
      "year": "1996",
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      "volume": "16",
      "author": "Lee",
      "year": "1997",
      "journal-title": "EMBO J"
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      "volume": "191",
      "author": "LeVay",
      "year": "1980",
      "journal-title": "J. Comp. Neurol"
    },
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      "first-page": "489",
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      "volume": "172",
      "author": "Lewis",
      "year": "1977",
      "journal-title": "J. Comp. Neurol"
    },
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      "first-page": "427",
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      "volume": "76",
      "author": "Li",
      "year": "1994",
      "journal-title": "Cell"
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      "author": "Maricq",
      "year": "1995",
      "journal-title": "Nature"
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      "volume": "88",
      "author": "Maruyama",
      "year": "1991",
      "journal-title": "Proc. Natl. Acad. Sci. USA"
    },
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      "first-page": "365",
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      "volume-title": "Caenorhabditis elegans: Modern Biological Analysis of an Organism",
      "author": "Miller",
      "year": "1995"
    },
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      "volume": "86",
      "author": "Miller",
      "year": "1989",
      "journal-title": "Proc. Natl. Acad. Sci. USA"
    },
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      "doi-asserted-by": "publisher",
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      "volume": "73",
      "author": "Nonet",
      "year": "1993",
      "journal-title": "Cell"
    },
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      "volume": "6",
      "author": "Otsuka",
      "year": "1991",
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      "volume": "117",
      "author": "Perkins",
      "year": "1986",
      "journal-title": "Dev. Biol"
    },
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      "volume": "84",
      "author": "Sengupta",
      "year": "1996",
      "journal-title": "Cell"
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      "article-title": "Viktor Hamburger Award review. Role for spontaneous neural activity in the patterning of connections between retina and LGN during visual system development",
      "volume": "12",
      "author": "Shatz",
      "year": "1994",
      "journal-title": "Int. J. Dev. Neurosci"
    },
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      "first-page": "602",
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      "year": "1996",
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    },
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      "volume": "281",
      "author": "Shatz",
      "year": "1978",
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    },
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      "year": "1988",
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      "author": "Sretavan",
      "year": "1988",
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    },
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      "author": "Starich",
      "year": "1995",
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    },
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      "volume": "6",
      "author": "Stryker",
      "year": "1986",
      "journal-title": "J. Neurosci"
    },
    {
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      "doi-asserted-by": "publisher",
      "first-page": "3235",
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      "volume": "8",
      "author": "Stuhmer",
      "year": "1989",
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    },
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      "first-page": "64",
      "DOI": "10.1016/0012-1606(83)90201-4",
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      "volume": "100",
      "author": "Sulston",
      "year": "1983",
      "journal-title": "Dev. Biol"
    },
    {
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      "first-page": "837",
      "DOI": "10.1038/332837a0",
      "article-title": "Cloning of a probable potassium channel gene from mouse brain",
      "volume": "332",
      "author": "Tempel",
      "year": "1988",
      "journal-title": "Nature"
    },
    {
      "key": "2023090605553163200_DEVELOP_126_9_1891C62",
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      "first-page": "857",
      "DOI": "10.1016/S0092-8674(00)81993-5",
      "article-title": "Regions responsible for the assembly of inwardly rectifying potassium channels",
      "volume": "87",
      "author": "Tinker",
      "year": "1996",
      "journal-title": "Cell"
    },
    {
      "key": "2023090605553163200_DEVELOP_126_9_1891C63",
      "doi-asserted-by": "publisher",
      "first-page": "207",
      "DOI": "10.1016/0092-8674(95)90162-0",
      "article-title": "Divergent seven transmembrane receptors are candidate chemosensory receptors in C. elegans",
      "volume": "83",
      "author": "Troemel",
      "year": "1995",
      "journal-title": "Cell"
    },
    {
      "key": "2023090605553163200_DEVELOP_126_9_1891C64",
      "doi-asserted-by": "publisher",
      "first-page": "161",
      "DOI": "10.1016/S0092-8674(00)80399-2",
      "article-title": "Reprogramming chemotaxis responses: sensory neurons define olfactory preferences in C. elegans",
      "volume": "91",
      "author": "Troemel",
      "year": "1997",
      "journal-title": "Cell"
    },
    {
      "key": "2023090605553163200_DEVELOP_126_9_1891C65",
      "doi-asserted-by": "publisher",
      "first-page": "303",
      "DOI": "10.1093/genetics/138.2.303",
      "article-title": "Multiple chemosensory defects in daf-11 and daf-21 mutants of Caenorhabditis elegans",
      "volume": "138",
      "author": "Vowels",
      "year": "1994",
      "journal-title": "Genetics"
    },
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      "DOI": "10.1002/cne.901600305",
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      "volume": "160",
      "author": "Ward",
      "year": "1975",
      "journal-title": "J. Comp. Neurol"
    },
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      "doi-asserted-by": "publisher",
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      "article-title": "The nerve ring of the nematode Caenorhabditis elegans: sensory input and motor output",
      "volume": "162",
      "author": "Ware",
      "year": "1975",
      "journal-title": "J. Comp. Neurol"
    },
    {
      "key": "2023090605553163200_DEVELOP_126_9_1891C68",
      "doi-asserted-by": "publisher",
      "first-page": "805",
      "DOI": "10.1016/0028-3908(96)00126-8",
      "article-title": "Eight potassium channel families revealed by the C. elegans genome project",
      "volume": "35",
      "author": "Wei",
      "year": "1996",
      "journal-title": "Neuropharmacology"
    },
    {
      "key": "2023090605553163200_DEVELOP_126_9_1891C69",
      "doi-asserted-by": "publisher",
      "first-page": "764",
      "DOI": "10.1038/271764a0",
      "article-title": "Connectivity changes in a class of motoneurone during the development of a nematode",
      "volume": "271",
      "author": "White",
      "year": "1978",
      "journal-title": "Nature"
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