Neurexin controls plasticity of a mature, sexually dimorphic neuron
Open accessAbstract
During development and adulthood, brain plasticity is evident at several levels, from synaptic structure and function to the outgrowth of dendrites and axons. Whether and how sex impinges on neuronal plasticity is poorly understood. Here we show that the sex-shared GABA (γ-aminobutyric acid)-releasing DVB neuron in Caenorhabditis elegans displays experience-dependent and sexually dimorphic morphological plasticity, characterized by the stochastic and dynamic addition of multiple neurites in adult males. These added neurites enable synaptic rewiring of the DVB neuron and instruct a functional switch of the neuron that directly modifies a step of male mating behaviour. Both DVB neuron function and male mating behaviour can be altered by experience and by manipulation of postsynaptic activity. The outgrowth of DVB neurites is promoted by presynaptic neurexin and antagonized by postsynaptic neuroligin, revealing a non-conventional activity and mode of interaction of these conserved, human-disease-relevant factors.
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Connectivity reinforcement by circuit activity and experience has been demonstrated but remains little studied.
“Reinforcement of connectivity by circuit activity and hence experience has been demonstrated but little studied so far45.”
From Whole-animal connectomes of both Caenorhabditis elegans sexes (2019) · cites this paper as [45]
In “DVB neurites are experience and activity-dependent” (page unavailable), the paper reports that mating experience and repeated circuit activation increase DVB neurite growth. In “DVB plasticity impacts behavior via dimorphic synaptic connectivity” (page unavailable), it reports an increase in specific synaptic connections with age. It does not directly show that activity reinforces those connections, and its statement that molecular mechanisms are not well understood does not establish that connectivity reinforcement itself has been little studied. (LLM, conf=0.83)
Experimental — accuracy not yet measuredNeurite outgrowth and synapse formation in C. elegans continue through larval development, the L4 stage, and adulthood, and ectopic neurite sprouting continues with aging.
“Outgrowth of neurites and establishment of synapses in C. elegans occurs throughout larval development and continues through the L4 larval stage and into adulthood, and ectopic neurite sprouting continues as the nervous system ages45,46.”
From Whole-animal connectomes of both Caenorhabditis elegans sexes (2019) · cites this paper as [45]
The ‘Morphologic plasticity displayed by adult male DVB neuron’ section reports progressive neurite outgrowth from adult days 1 to 5, and ‘DVB plasticity impacts behavior via dimorphic synaptic connectivity’ reports an increase in specific synaptic connections over that period (page numbers not supplied). The paper does not establish continued outgrowth and synapse formation throughout larval development or the L4 stage, or general ectopic sprouting across the aging nervous system; its adult finding concerns the male DVB neuron. (LLM, conf=0.87)
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The synaptic basis for sexual dimorphism in the invertebrate nervous system
Salzberg, Y., Haque, R., & Oren‐Suissa, M. (2023) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2023.102757 · Cited by 4 · see citing works
Variation in Social Feeding Behaviors and Interactions Among Caenorhabditis Nematodes
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Self-citationEvolutionarily conserved behavioral plasticity enables context-dependent mating in C. elegans
Susoy, V., & Samuel, A. D. T. (2023) · Current Biology · doi:10.1016/j.cub.2023.09.003 · Cited by 2 · see citing works
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Self-citationSexual dimorphism in the nervous system: Three principles from the nematode C. elegans
Portman, D., Bainbridge, C., Ward, Z. C., & Zhang, J. (2026) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2026.103175 · Cited by 2 · see citing works
Sexual Dimorphisms: How Sex-Shared Neurons Generate Sex-Specific Behaviors
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Inferences of glia‐mediated control in Caenorhabditis elegans
Bowles, S. N., & Johnson, C. M. (2021) · Journal of Neuroscience Research · doi:10.1002/jnr.24803 · Cited by 2 · see citing works
Neurexin-1α regulates neurite growth of rat hippocampal neurons.
Wang, A., Xiang, Y., Yang, B. B., & Lu, W.-Y. (2019) · PubMed Central · Cited by 2 · see citing works
Insulin and epidermal signals independently shape sexually dimorphic neurite branching in C. elegans
Yang, J.-B., Chen, R.-T., Chen, Y., Lin, Y.-H., & Chen, C. (2025) · EMBO Reports · doi:10.1038/s44319-025-00608-0 · Cited by 1 · see citing works
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Mating status, independent of size, influences lethal fighting in an entomopathogenic nematode
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Neuronal plasticity in nematode worms
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Toolkits for detailed and high-throughput interrogation of synapses in C. elegansPreprint
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Self-citationEndpoints for Assessing the Toxicity on Primary Targeted Organs
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Endpoints for Assessing the Toxicity on Secondary Targeted Organs
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Multi-modal analysis and integration of single-cell morphological dataPreprint
Govek, K. W., Crawford, J., Saturnino, A. B., Zoga, K., Hart, M. P., & Cámara, P. G. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.05.19.492525
Self-citationDevelopmental biology: A hole in the matrix
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Modulation of stress responses in C. elegans: Sex differences and neuronal control
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Evolution of invertebrate sleep and its neural control
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Insertion of rare autism variants in synaptic genes induce novel behavioral phenotypes in C. elegansPreprint
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The claudin-like molecule CLC-3 regulates cholinergic neurotransmission in Caenorhabditis elegans
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Self-citation
- Authors
- Hart, M. P., & Hobert, O.
- Affiliations
- Howard Hughes Medical Institute (US)
- Corresponding author
- Hart, Michael P.
- Venue
- Nature
- Published
- 2018-01
- Volume
- 553
- Issue
- 7687
- Pages
- 165-170
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- PMC
- PMC5968453
- OpenAlex
- W2783553962
- Cited by
- 84
- References
- 41
- Citations by year
- 2026: 4 · 2025: 9 · 2024: 11 · 2023: 10 · 2022: 10 · 2021: 12 · 2020: 10 · 2019: 9 · 2018: 9
- FWCI
- 4.55
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- Funders
- Howard Hughes Medical Institute
- National Institutes of Health (P40OD010440)
- National Institute of Diabetes and Digestive and Kidney Diseases (T32DK007328)
- National Institute of Neurological Disorders and Stroke (R37NS039996, F32NS086285)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurobiology and Insect Physiology Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetics and Neurodevelopmental Disorders
- Keywords
- neurexin, neuroligins, neurite outgrowth, synaptic rewiring, male mating behavior, experience-dependent plasticity, adhesion molecules, Caenorhabditis elegans, postsynaptic activity, learning and memory
- MeSH terms
- Animals, gamma-Aminobutyric Acid, Male, Neuronal Plasticity, Sexual Behavior, Animal, Sex Characteristics, Synapses, Cell Adhesion Molecules, Neuronal, Neurites, Caenorhabditis elegans, Caenorhabditis elegans Proteins, Hermaphroditic Organisms, GABAergic Neurons
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