The DOI matches its Crossref record; 5 of the 5 references it cites were found in a registry or an index.
Synaptic polarity of the interneuron circuit controlling C. elegans locomotion
Open accessAbstract
Caenorhabditis elegans is the only animal for which a detailed neural connectivity diagram has been constructed. However, synaptic polarities in this diagram, and thus, circuit functions are largely unknown. Here, we deciphered the likely polarities of seven pre-motor neurons implicated in the control of worm's locomotion, using a combination of experimental and computational tools. We performed single and multiple laser ablations in the locomotor interneuron circuit and recorded times the worms spent in forward and backward locomotion. We constructed a theoretical model of the locomotor circuit and searched its all possible synaptic polarity combinations and sensory input patterns in order to find the best match to the timing data. The optimal solution is when either all or most of the interneurons are inhibitory and forward interneurons receive the strongest input, which suggests that inhibition governs the dynamics of the locomotor interneuron circuit. From the five pre-motor interneurons, only AVB and AVD are equally likely to be excitatory, i.e., they have probably similar number of inhibitory and excitatory connections to distant targets. The method used here has a general character and thus can be also applied to other neural systems consisting of small functional networks.
Overview
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
The main role of AVB is to influence B-class motorneurons to turn on and off forward locomotion, whereas the main role of AVA is to influence A-class motorneurons to turn on and off backward locomotion.
“the main role of the AVB class is to influence the B-class motorneuron to turn on and off forward locomotion, whereas the main role of AVA is to influence the A-class motorneuron to turn on and off backward locomotion (Kawano et al., 2011; Qi, Garren, Shu, Tsien, & Jin, 2012; Rakowski, Srinivasan, Sternberg, & Karbowski, 2013; Zheng, Brockie, Mellem, Madsen, & Maricq, 1999).”
From Potential role of a ventral nerve cord central pattern generator in forward and backward locomotion in Caenorhabditis elegans (2018) · cites this paper as Rakowski et al., 2013
The Introduction (page not specified) describes AVB as mainly connected to B-class motor neurons involved in forward motion, and AVA as mainly connected to A-class motor neurons involved in backward motion. The Discussion also describes AVB signaling to B neurons and AVA exciting A neurons. But the paper cautions that movement direction depends on the collective circuit and the balance of motor-neuron activity; it does not establish that either interneuron independently turns its associated movement on and off. (LLM, conf=0.86)
Experimental — accuracy not yet measured
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Citations
Cites
The structure of the nervous system of the nematode Caenorhabditis elegans
White, J. G., Southgate, E., Thomson, J. N., & Brenner, S. (1986) · Philosophical Transactions of the Royal Society of London. B, Biological Sciences · doi:10.1098/rstb.1986.0056 · Cited by 5,589 · cited 13×
“Because of its smallness a precise map of neural connections was possible to construct (White et al., 1986; Chen et al., 2006).”
BackgroundMethodInfluentialStructural Properties of the Caenorhabditis elegans Neuronal Network
Varshney, L. R., Chen, B. L., Paniagua, E., Hall, D. H., & Chklovskii, D. B. (2011) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1001066 · Cited by 867
What Is Stochastic Resonance? Definitions, Misconceptions, Debates, and Its Relevance to Biology
McDonnell, M. D., & Abbott, D. (2009) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1000348 · Cited by 774
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
Faumont, S., Rondeau, G., Thiele, T. R., Lawton, K. J., McCormick, K. E., Sottile, M., Griesbeck, O., Heckscher, E. S., Roberts, W. M., Doe, C. Q., et al. (2011) · PLoS ONE · doi:10.1371/journal.pone.0024666 · Cited by 128
Flagged first, then by citations
Research works printed but not linked: 38
- Bargmann C. I. (1998). Neurobiology of the Caenorhabditis elegans genome. Science 282, 2028– 2033 10.1126/science.282.5396.2028 9851919 · DOI · Paper page
- Brenner S. (1974). The genetics of Caenorhabditis elegans. Genetics 77, 71– 94 4366476 PMC1213120
- Brockie P. J. Maricq A. V. (2006). Ionotropic glutamate receptors: genetics, behavior, and electrophysiology, in Wormbook, eds The C. elegans Research Community Available online at: http://www.wormbook.org PMC4781458 18050468
- Bryden J. A. Cohen N. (2008). Neural control of Caenorhabditis elegans forward locomotion: the role of sensory feedback. Biol. Cybern. 98, 339– 351 10.1007/s00422-008-0212-6 18350313 · DOI · Paper page
- Chalfie M. Sulston J. E. White J. G. Southgate E. Thomson J. N. Brenner S. (1985). The neural circuit for touch sensitivity in Caenorhabditis elegans. J. Neurosci. 5, 956– 964 3981252 PMC6565008
- Chen B. L. Hall D. H. Chklovskii D. B. (2006). Wiring optimization can relate neuronal structure and function. Proc. Natl. Acad. Sci. U.S.A. 103, 4723– 4728 10.1073/pnas.0506806103 16537428 PMC1550972 · DOI · Paper page
- Cherniak C. (1994). Component placement optimization in the brain. J. Neurosci. 14, 2418– 2427 8158278 PMC6577144
- Chklovskii D. B. (2004). Synaptic connectivity and neuronal morphology: two sides of the same coin. Neuron 43, 609– 617 10.1016/j.neuron.2004.08.012 15339643 · DOI
- Chronis N. Zimmer M. Bargmann C. I. (2007). Microfluidics for in vivo imaging of neuronal and behavioral activity in Caenorhabditis elegans. Nat. Methods 4, 727– 731 10.1038/nmeth1075 17704783 · DOI
- Cronin C. J. Mendel J. E. Mukhtar S. Kim Y. M. Stirbl R. C. Bruck J. (2005). An automated system for measuring parameters of nematode sinusoidal movement. BMC Genet. 6: 5 10.1186/1471-2156-6-5 15698479 PMC549551 · DOI
- Davis R. E. Stretton A. O. W. (1989). Passive membrane properties of motorneurons and their role in long-distance signaling in the nematode Ascaris. J. Neurosci. 9, 403– 414 2918369 PMC6569814
- de Bono M. Maricq A. V. (2005). Neuronal substrates of complex behaviors in C. elegans. Annu. Rev. Neurosci. 28, 451– 501 10.1146/annurev.neuro.27.070203.144259 16022603 · DOI
- DeFelipe J. Alonso-Nanclares L. Avellano J. (2002). Microstructure of the neocortex: Comparative aspects. J. Neurocytol. 31, 299– 316 10.1023/A:1024130211265 12815249 · DOI · Paper page
- Ermentrout G. B. Terman D. H. (2010). Mathematical Foundations of Neuroscience. New York, NY: Springer 10.1007/978-0-387-87708-2 · DOI · Paper page
- Gardiner C. W. (2004). Handbook of Stochastic Methods. 3rd Edn Berlin: Springer
- Gray J. M. Hill J. J. Bargmann C. I. (2005). A circuit for navigation in Caenorhabditis elegans. Proc. Natl. Acad. Sci. U.S.A. 102, 3184– 3191 10.1073/pnas.0409009101 15689400 PMC546636 · DOI · Paper page
- Ha H. Hendricks M. Shen Y. Gabel C. V. Fang-Yen C. Qin Y. (2010). Functional organization of a neural network for aversive olfactory learning in Caenorhabditis elegans. Neuron 68, 1173– 1186 10.1016/j.neuron.2010.11.025 21172617 PMC3038580 · DOI
- Haider B. Duque A. Hasenstaub A. R. McCormick D. A. (2006). Neocortical network activity in vivo is generated through a dynamic balance of excitation and inhibition. J. Neurosci. 26, 4535– 4545 10.1523/JNEUROSCI.5297-05.2006 16641233 PMC6674060 · DOI · Paper page
- Haspel G. O'Donovan M. J. Hart A. C. (2010). Motorneurons dedicated to either forward or backward locomotion in the nematode C. elegans. J. Neurosci. 30, 11151– 11156 10.1523/JNEUROSCI.2244-10.2010 20720122 PMC2945236 · DOI · Paper page
- Hobert O. (2003). Behavioral plasticity in C. elegans: paradigms, circuits, genes. J. Neurobiol. 54, 203– 223 10.1002/neu.10168 12486705 · DOI
- Jospin M. Qi Y. Stawicki T. Boulin T. Schuske K. Horvitz H. (2009). A neuronal acetylcholine receptor regulates the balance of muscle excitation and inhibition in Caenorhabditis elegans. PLoS Biol. 7: e1000265 10.1371/journal.pbio.1000265 20027209 PMC2787625 · DOI
- Kaiser M. Hilgetag C. C. (2006). Nonoptimal component placement, but short processing paths, due to long-distance projections in neural systems. PLoS Comput. Biol. 2: e95 10.1371/journal.pcbi.0020095 16848638 PMC1513269 · DOI
- Kaplan J. M. Horvitz H. R. (1993). A dual mechanosensory and chemosensory neuron in Caenorhabditis elegans. Proc. Natl. Acad. Sci. U.S.A. 90, 2227– 2231 10.1073/pnas.90.6.2227 8460126 PMC46059 · DOI
- Karbowski J. (2001). Optimal wiring principle and plateaus in the degree of separation for cortical neurons. Phys. Rev. Lett. 86, 3674– 3677 10.1103/PhysRevLett.86.3674 11328051 · DOI
- Karbowski J. (2003). How does connectivity between cortical areas depend on brain size? Implications for efficient computations. J. Comput. Neurosci. 15, 347– 356 10.1023/A:1027467911225 14618069 · DOI
- Karbowski J. Cronin C. J. Seah A. Mendel J. E. Cleary D. Sternberg P. W. (2006). Conservation rules, their breakdown, and optimality in Caenorhabditis sinusoidal locomotion. J. Theor. Biol. 242, 652– 669 10.1016/j.jtbi.2006.04.012 16759670 · DOI · Paper page
- Karbowski J. Schindelman G. Cronin C. J. Seah A. Sternberg P. W. (2008). Systems level circuit model of C. elegans undulatory locomotion: mathematical modeling and molecular genetics. J. Comput. Neurosci. 24, 253– 276 10.1007/s10827-007-0054-6 17768672 · DOI · Paper page
- Kawano T. Po M. D. Gao S. Leung G. Ryu W. S. Zhen M. (2011). An imbalancing act: gap junctions reduce the backward motor circuit activity to bias C. elegans forward locomotion. Neuron 72, 572– 586 10.1016/j.neuron.2011.09.005 22099460 · DOI · Paper page
- Koch C. (1998). Biophysics of Computation. Oxford: Oxford University Press
- Li W. Feng Z. Sternberg P. W. Xu S. X. Z. (2006). A C. elegans stretch receptor neuron revealed by a mechanosensitive TRP channel homologue. Nature 440, 684– 687 10.1038/nature04538 16572173 PMC2865900 · DOI
- Mellem J. E. Brockie P. J. Zheng Y. Madsen D. M. Maricq A. V. (2002). Decoding of polymodal sensory stimuli by postsynaptic glutamate receptors in C. elegans. Neuron 36, 933– 944 10.1016/S0896-6273(02)01088-7 12467596 · DOI
- Piggott B. J. Liu J. Feng Z. Wescott S. A. Xu X. Z. S. (2011). The neural circuits and synaptic mechanisms underlying motor initiation in C. elegans. Cell 147, 922– 933 10.1016/j.cell.2011.08.053 22078887 PMC3233480 · DOI
- Qi Y. B. Garren E. J. Shu X. Tsien R. Y. Jin Y. (2012). Photo-inducible cell ablation in Caenorhabditis elegans using the genetically encoded singlet oxygen generating protein miniSOG. Proc. Natl. Acad. Sci. U.S.A. 109, 7499– 7504 10.1073/pnas.1204096109 22532663 PMC3358873 · DOI
- Sengupta P. Samuel A. D. T. (2009). Caenorhabditis elegans: a model system for systems neuroscience. Curr. Opin. Neurobiol. 19, 637– 643 10.1016/j.conb.2009.09.009 19896359 PMC2904967 · DOI
- van Vreeswijk C. Sompolinsky H. (1996). Chaos in neuronal networks with balanced excitatory and inhibitory activity. Science 274, 1724– 1726 10.1126/science.274.5293.1724 8939866 · DOI
- Vogels T. P. Sprekeler H. Zenke F. Clopath C. Gerstner W. (2011). Inhibitory plasticity balances excitation and inhibition in sensory pathways and memory networks. Science 334, 1569– 1573 10.1126/science.1211095 22075724 · DOI
- Wicks S. R. Roehrig C. J. Rankin C. H. (1996). A dynamic network simulation of the nematode tap withdrawal circuit: predictions concerning synaptic function using behavioral criteria. J. Neurosci. 16, 4017– 4031 8656295 PMC6578605
- Zheng Y. Brockie P. J. Mellem J. E. Madsen D. M. Maricq A. V. (1999). Neuronal control of locomotion in C. elegans is modified by a dominant mutation in the GLR-1 ionotropic glutamate receptor. Neuron 24, 347– 361 10.1016/S0896-6273(00)80849-1 10571229 · DOI
Cited by
Sorted by citations
A cellular and regulatory map of the cholinergic nervous system of C. elegans
Pereira, L., Kratsios, P., Serrano-Saiz, E., Sheftel, H., Mayo, A. E., Hall, D. H., White, J. G., LeBoeuf, B., Garcia, L. R., Alon, U., et al. (2015) · eLife · doi:10.7554/elife.12432 · Cited by 365
Olivares, E. O., Izquierdo, E. J., & Beer, R. D. (2018) · Network Neuroscience · doi:10.1162/netn_a_00036 · Cited by 38
The whole worm: brain–body–environment models of C. elegans
Izquierdo, E. J., & Beer, R. D. (2016) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2016.06.005 · Cited by 27
Metadata
- Authors
- Rakowski, F., Srinivasan, J., Sternberg, P. W., & Karbowski, J.
- Affiliations
- Interdisciplinary Centre for Mathematical and Computational Modelling, University of Warsaw (PL)
- California Institute of Technology (US)
- University of Warsaw (PL)
- Corresponding author
- Karbowski, Jan
- Venue
- Frontiers in Computational Neuroscience
- Publisher
- Frontiers Media SA
- Published
- 2013
- Volume
- 7
- Pages
- 128-128
- ISSN
- 1662-5188 (ISSN-L)
- PMC
- PMC3788333
- OpenAlex
- W2146252121
- Cited by
- 41
- References
- 5
- Citations by year
- 2026: 2 · 2025: 3 · 2024: 2 · 2022: 5 · 2021: 1 · 2020: 6 · 2019: 5 · 2018: 5 · 2017: 4 · 2016: 4 · 2015: 3 · 2014: 1
- FWCI
- 1.31
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- cc-by
- Locations
- Frontiers in Computational Neuroscience (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- arXiv (Cornell University) (submittedVersion)
- CaltechAUTHORS (California Institute of Technology) (submittedVersion, cc-by)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
- arXiv (Cornell University)
- Funders
- Uniwersytet Warszawski
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurobiology and Insect Physiology Research
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Keywords
- Caenorhabditis elegans locomotion, laser ablation, inhibition, neuronal connectivity
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review