Neural signal propagation atlas of Caenorhabditis elegans
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. Here, to better understand the relationship between the structure and the function of a nervous system, we systematically measure signal propagation in 23,433 pairs of neurons across the head of the nematode Caenorhabditis elegans by direct optogenetic activation and simultaneous whole-brain calcium imaging. We measure the sign (excitatory or inhibitory), strength, temporal properties and causal direction of signal propagation between these neurons to create a functional atlas. We find that signal propagation differs from model predictions that are based on anatomy. Using mutants, we show that extrasynaptic signalling not visible from anatomy contributes to this difference. We identify many instances of dense-core-vesicle-dependent signalling, including on timescales of less than a second, that evoke acute calcium transients-often where no direct wired connection exists but where relevant neuropeptides and receptors are expressed. We propose that, in such cases, extrasynaptically released neuropeptides serve a similar function to that of classical neurotransmitters. Finally, our measured signal propagation atlas better predicts the neural dynamics of spontaneous activity than do models based on anatomy. We conclude that both synaptic and extrasynaptic signalling drive neural dynamics on short timescales, and that measurements of evoked signal propagation are crucial for interpreting neural function.
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Activity propagation measured by calcium imaging is not well predicted by anatomical connectivity alone in Caenorhabditis elegans, demonstrating the importance of extrasynaptic signalling not accounted for in the model.
“This is consistent with recent studies showing that activity propagation measured by calcium imaging is not well predicted by anatomical connectivity alone in Caenorhabditis elegans, demonstrating the importance of extrasynaptic signalling not accounted for in our model50.”
From A Drosophila computational brain model reveals sensorimotor processing (2024) · cites this paper as [50]
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- Authors
- Randi, F., Sharma, A. K., Dvali, S., & Leifer, A. M.
- Affiliations
- Regeneron (United States) (US)
- Princeton University (US)
- Corresponding author
- Leifer, Andrew M.
- Venue
- Nature
- Published
- 2023-11-01
- Volume
- 623
- Issue
- 7986
- Pages
- 406-414
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- PMC
- PMC10632145
- OpenAlex
- W4388126567
- Cited by
- 153
- References
- 75
- Citations by year
- 2026: 32 · 2025: 62 · 2024: 52 · 2023: 6 · 2018: 1
- FWCI
- 18.43
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Locations
- Nature (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- ArTS Archivio della ricerca di Trieste (University of Trieste https://www.units.it/) (submittedVersion)
- Funders
- National Institutes of Health (1dp2ns116768-01, P40OD010440)
- National Institute of Neurological Disorders and Stroke (DP2-NS116768)
- 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 › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Keywords
- neural signal propagation, Caenorhabditis elegans, optogenetic stimulation, whole-brain calcium imaging, dense core vesicles, neuropeptides, synaptic transmission, spontaneous neuronal activity, neural dynamics, structure-function relationship
- MeSH terms
- Animals, Calcium, Models, Neurological, Mutation, Neural Pathways, Neurons, Neuropeptides, Synapses, Signal Transduction, Caenorhabditis elegans
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