Graded synaptic transmission at the Caenorhabditis elegans neuromuscular junction
Open accessAbstract
Most neurotransmission is mediated by action potentials, whereas sensory neurons propagate electrical signals passively and release neurotransmitter in a graded manner. Here, we demonstrate that Caenorhabditis elegans neuromuscular junctions release neurotransmitter in a graded fashion. When motor neurons were depolarized by light-activation of channelrhodopsin-2, the evoked postsynaptic current scaled with the strength of the stimulation. When motor neurons were hyperpolarized by light-activation of halorhodopsin, tonic release of synaptic vesicles was decreased. These data suggest that both evoked and tonic neurotransmitter release is graded in response to membrane potential. Acetylcholine synapses are depressed by high-frequency stimulation, in part due to desensitization of the nicotine-sensitve ACR-16 receptor. By contrast, GABA synapses facilitate before becoming depressed. Graded transmission and plasticity confer a broad dynamic range to these synapses. Graded release precisely transmits stimulation intensity, even hyperpolarizing inputs. Synaptic plasticity alters the balance of excitatory and inhibitory inputs into the muscle in a use-dependent manner.
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A recent publication by Liu et al. (2009) provides the first characterization of the C. elegans body wall neuromuscular junction response to optogenetic activation and inhibition of B-class neurons.
“A recent publication by Liu et al. (2009) provides the first characterization of the C. elegans body wall neuromuscular junction (NMJ) response to optogenetic activation and inhibition of B-class neurons.”
From Gait Modulation in C. elegans: An Integrated Neuromechanical Model (2012) · cites this paper as Liu et al., 2009
Liu et al. found that the postsynaptic current increases smoothly with increasing light intensity and is reduced by halorhodopsin inhibition.
“They found that the postsynaptic current increases smoothly as shown in Figure 8A. Liu et al. also used halorhodopsin, a light activated hyperpolarizing ion channel, to inhibit the presynaptic neuron, finding that the postsynaptic current is reduced.”
From Gait Modulation in C. elegans: An Integrated Neuromechanical Model (2012) · cites this paper as Liu et al., 2009
The data of Liu et al. (2009) are consistent with the bistable B-class neuron dynamics.
“While this model cannot be used conclusively to infer a single model of B-class neurons (or even to rule out passive behavior of these neurons), we can conclude that the data of Liu et al. (2009) are consistent with the bistable B-class neuron dynamics.”
From Gait Modulation in C. elegans: An Integrated Neuromechanical Model (2012) · cites this paper as Liu et al., 2009
Cites
Active Currents Regulate Sensitivity and Dynamic Range in C. elegans Neurons
Goodman, M. B., Hall, D. H., Avery, L., & Lockery, S. R. (1998) · Neuron · doi:10.1016/s0896-6273(00)81014-4 · Cited by 370 · see citing works
The quest for action potentials in C. elegans neurons hits a plateau
Lockery, S. R., & Goodman, M. B. (2009) · Nature Neuroscience · doi:10.1038/nn0409-377 · Cited by 81 · see citing works
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Glycolytic enzymes localize to synapses under energy stress to support synaptic function
Jang, S., Nelson, J. C., Bend, E. G., Rodríguez-Laureano, L., Tueros, F. G., Cartagenova, L., Underwood, K., Jorgensen, E. M., & Colón-Ramos, D. A. (2016) · Neuron · doi:10.1016/j.neuron.2016.03.011 · Cited by 270 · see citing works
Self-citationAction potentials drive body wall muscle contractions in <i>Caenorhabditis elegans</i>
Gao, S., & Zhen, M. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1012346108 · Cited by 149 · see citing works
Gait Modulation in C. elegans: An Integrated Neuromechanical Model
Boyle, J. H., Berri, S., & Cohen, N. (2012) · Frontiers in Computational Neuroscience · doi:10.3389/fncom.2012.00010 · Cited by 163 · see citing works
“To validate these assumptions against available data (Liu et al., 2009), we also presented a complementary conductance-based model of B-class neurons.”
BackgroundMethodResultInfluentialTwo Rab2 Interactors Regulate Dense-Core Vesicle Maturation
Ailion, M., Hannemann, M., Dalton, S., Pappas, A., Watanabe, S., Hegermann, J., Liu, Q., Han, H.-F., Gu, M., Goulding, M. Q., et al. (2014) · Neuron · doi:10.1016/j.neuron.2014.02.017 · Cited by 86 · see citing works
Self-citationAn integrative data-driven model simulating C. elegans brain, body and environment interactions
Zhao, M., Wang, N., Jiang, X., Ma, X., Ma, H., He, G., Du, K., Ma, L., & Huang, T. (2024) · Nature Computational Science · doi:10.1038/s43588-024-00738-w · Cited by 29 · see citing works
“The neuron models were connected by graded synapses 36,60 and gap junctions 61 in the C. elegans neural network.”
- Authors
- Liu, Q., Hollopeter, G., & Jorgensen, E. M.
- Affiliations
- Howard Hughes Medical Institute (US)
- Department of Biology and Howard Hughes Medical Institute, University of Utah, Salt Lake City, UT 84112-0840
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2009-06-30
- Volume
- 106
- Issue
- 26
- Pages
- 10823-10828
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC2705609
- OpenAlex
- W2140685510
- Cited by
- 149
- References
- 2
- Citations by year
- 2026: 3 · 2025: 5 · 2024: 7 · 2023: 3 · 2022: 9 · 2021: 12 · 2020: 9 · 2019: 6 · 2018: 10 · 2017: 10 · 2016: 4 · 2015: 8 · 2014: 14 · 2013: 14 · 2012: 12
- FWCI
- 4.84
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Howard Hughes Medical Institute
- National Institutes of Health (NS034307)
- National Institute of Neurological Disorders and Stroke (R37NS034307, NS034307, R01NS034307)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Nicotinic Acetylcholine Receptors Study
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurobiology and Insect Physiology Research
- Keywords
- neuromuscular junction, Caenorhabditis elegans, neurotransmitter release, evoked release, GABAergic synapses, synaptic plasticity, channelrhodopsin-2, halorhodopsin, hyperpolarization, synaptic depression, sensory neurons
- MeSH terms
- Acetylcholine, Animals, Electric Stimulation, Evoked Potentials, gamma-Aminobutyric Acid, Light, Membrane Potentials, Microscopy, Fluorescence, Motor Neurons, Synaptic Transmission, Neuromuscular Junction, Neuronal Plasticity, Caenorhabditis elegans, Neurotransmitter Agents, Sensory Rhodopsins
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