An unusual potassium conductance protects Caenorhabditis elegans pharyngeal muscle rhythms against environmental noise
Open accessAbstract
The nematode Caenorhabditis elegans feeds by rhythmic contraction and relaxation of a neuromuscular organ called the pharynx, which draws in and filters water and bacterial food. This behavior is driven by myogenic plateau potentials, long-lasting depolarizations of the pharyngeal muscle, which are timed by neuronal input from a dedicated pharyngeal nervous system. While the timing of these plateaus’ initiation has received significant attention, their mechanisms of termination remain incompletely understood. In particular, it is unclear how plateaus resist early termination by hyperpolarizing current noise. Here, we present a computational model of pharyngeal plateaus against a noisy background. We propose that an unusual, rapidly inactivating potassium conductance confers exceptional noise robustness on the system. We further investigate the possibility that a similar mechanism in other systems permits switching between plateau and spiking behavior under noisy conditions.
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In computational models it is feasible to examine the structures of the parameter spaces that contribute to an output or a physiological state.
“In computational models it is feasible to examine the structures of the parameter spaces that contribute to an output or a physiological state [31,42,46,47].”
From A feature and not a bug: Replication failures can lead to new biology (2026) · cites this paper as [47]
C. elegans pharyngeal pumping consists of myogenic plateau potentials which are driven by the nervous system.
“C. elegans pharyngeal pumping consists of myogenic plateau potentials which are driven by the nervous system.”
From A feature and not a bug: Replication failures can lead to new biology (2026) · cites this paper as [47]
An unusual, rapidly inactivating potassium conductance confers exceptional noise robustness on the system.
“In this computational model an unusual, rapidly inactivating potassium conductance confers exceptional noise robustness on the system.”
From A feature and not a bug: Replication failures can lead to new biology (2026) · cites this paper as [47]
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Cites
Sensory-evoked LTP driven by dendritic plateau potentials in vivo
Gambino, F., Pagès, S., Kehayas, V., Baptista, D., Tatti, R., Carleton, A., & Holtmaat, A. (2014) · Nature · doi:10.1038/nature13664 · Cited by 253 · 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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Research works printed but not linked: 41
- [1]L. Avery, B. B. Shtonda, Food transport in the C. elegans pharynx. J. Exp. Biol. 206, 2441– 2457 (2003). 12796460 PMC3951750
- [2]D. M. Raizen, L. Avery, Electrical activity and behavior in the pharynx of Caenorhabditis elegans. Neuron 12, 483– 495 (1994). 8155316 PMC4460247
- [3]B. Song, L. Avery, The pharynx of the nematode C. elegans: A model system for the study of motor control. Worm 2, e21833 (2013). 24058858 PMC3670459
- [4]S. J. Cook, The connectome of the Caenorhabditis elegans pharynx. J. Comp. Neurol. 528, 2767– 2784 (2020). 32352566 PMC7601127
- [5]D. G. Albertson, J. Thompson, The pharynx of Caenorhabditis elegans. Philos. Trans. R. Soc. Lond. Ser. B, Biol. Sci. 275, 299– 325 (1976). 8805
- [6]C. Fang-Yen, L. Avery, A. D. Samuel, Two size-selective mechanisms specifically trap bacteria-sized food particles in Caenorhabditis elegans. Proc. Natl. Acad. Sci. U.S.A. 106, 20093– 20096 (2009). 19903886 PMC2785297
- [7]V. China, R. Holzman, Hydrodynamic starvation in first-feeding larval fishes. Proc. Natl. Acad. Sci. U.S.A. 111, 8083– 8088 (2014). 24843180 PMC4050599
- [8]N. Trojanowski, D. Raizen, C. Fang-Yen, Pharyngeal pumping in Caenorhabditis elegans depends on tonic and phasic signaling from the nervous system. Sci. Rep. 6, 22940 (2016). 26976078 PMC4791602
- [9]L. Avery, H. R. Horvitz, Pharyngeal pumping continues after laser killing of the pharyngeal nervous system of C. elegans. Neuron 3, 473– 485 (1989). 2642006
- [10]I. R. Brenner, D. M. Raizen, C. Fang-Yen, Pharyngeal timing and particle transport defects in Caenorhabditis elegans feeding mutants. J. Neurophysiol. 128, 302– 309 (2022). 35730757
- [11]J. C. Weeks, K. J. Robinson, S. R. Lockery, W. M. Roberts, Anthelmintic drug actions in resistant and susceptible C. elegans revealed by electrophysiological recordings in a multichannel microfluidic device. Int. J. Parasitol. Drugs Drug Resist. 8, 607– 628 (2018). 30503202 PMC6287544
- [12]O. Kiehn, Plateau potentials and active integration in the final common pathway-for motor behaviour. Trends Neurosci. 14, 68– 73 (1991). 1708539
- [13]R. A. Dicaprio, Plateau potentials in motor neurons in the ventilatory system of the crab. J. Exp. Biol. 200, 1725– 1736 (1997). 9319633
- [14]J. F. Perrier, R. Delgado-Lezama, Synaptic release of serotonin induced by stimulation of the raphe nucleus promotes plateau potentials in spinal motoneurons of the adult turtle. J. Neurosci. 25, 7993– 7999 (2005). 16135756 PMC6725458
- [15]J. Leugering, P. Nieters, G. Pipa, Dendritic plateau potentials can process spike sequences across multiple time-scales. Front. Cognit. 2, 1044216 (2023).
- [16]K. D. Oikonomou, M. B. Singh, E. V. Sterjanaj, S. D. Antic, Spiny neurons of amygdala, striatum, and cortex use dendritic plateau potentials to detect network up states. Front. Cell. Neurosci. 8, 292 (2014). 25278841 PMC4166350
- [17]M. Bouhadfane, S. Tazerart, A. Moqrich, L. Vinay, F. Brocard, Sodium-mediated plateau potentials in lumbar motoneurons of neonatal rats. J. Neurosci. 33, 15626– 15641 (2013). 24068829 PMC6618457
- [18]D. J. Bennett, Y. Li, M. Siu, Plateau potentials in sacrocaudal motoneurons of chronic spinal rats, recorded in vitro. J. Neurophysiol. 86, 1955– 1971 (2001). 11600653
- [19]P. Guertin, J. Hounsgaard, Non-volatile general anaesthetics reduce spinal activity by suppressing plateau potentials. Neuroscience 88, 353– 358 (1999). 10197758
- [20]L. Avery, Motor neuron M3 controls pharyngeal muscle relaxation timing in Caenorhabditis elegans. J. Exp. Biol. 175, 283– 297 (1993). 8440973
- [22]J. A. White, J. T. Rubinstein, A. R. Kay, Channel noise in neurons. Trends Neurosci. 23, 131– 137 (2000). 10675918
- [23]B. Shtonda, L. Avery, Cca-1, egl-19 and exp-2 currents shape action potentials in the Caenorhabditis elegans pharynx. J. Exp. Biol. 208, 2177– 2190 (2005). 15914661 PMC1351090
- [24]V. Booth, J. Rinzel, O. Kiehn, Compartmental model of vertebrate motoneurons for Ca2+-dependent spiking and plateau potentials under pharmacological treatment J. Neurophysiol. 78, 3371– 3385 (1997). 9405551
- [25]C. L. Neveu, P. Smolen, D. A. Baxter, J. H. Byrne, Voltage- and calcium-gated membrane currents tune the plateau potential properties of multiple neuron types. J. Neurosci. 43, 7601– 7615 (2023). 37699717 PMC10634553
- [27]K. A. Steger, B. B. Shtonda, C. Thacker, T. P. Snutch, L. Avery, The C. elegans t-type calcium channel cca-1 boosts neuromuscular transmission. J. Exp. Biol. 208, 2191– 2203 (2005). 15914662 PMC1382270
- [28]P. Dayan, L. F. Abbott, Theoretical Neuroscience: Computational and Mathematical Modeling of Neural Systems (MIT Press, Cambridge, MA, 2001).
- [29]S. Stern, C. Kirst, C. I. Bargmann, Neuromodulatory control of long-term behavioral patterns and individuality across development. Cell 171, 1649– 1662 (2017). 29198526
- [30]J. Ratliff, A. Franci, E. Marder, T. O’Leary, Neuronal oscillator robustness to multiple global perturbations. Biophys. J. 120, 1454– 1468 (2021). 33610580 PMC8105708
- [31]M. Chesler, Regulation and modulation of pH in the brain. Physiol. Rev. 83, 1183– 1221 (2003). 14506304
- [32]J. M. Ramirez, K. G. Pearson, Octopamine induces bursting and plateau potentials in insect neurones. Behav. Brain Res. 549, 332– 337 (1991). 1884227
- [33]J. Hounsgaard, O. Kiehn, Serotonin-induced bistability of turtle motoneurones caused by a nifedipine-sensitive calcium plateau potential. J. Physiol. 414, 265– 282 (1989). 2607432 PMC1189141
- [34]T. Niacaris, L. Avery, Serotonin regulates repolarization of the C. elegans pharyngeal muscle. J. Exp. Biol. 206, 223– 231 (2003). 12477893 PMC4441752
- [35]D. M. Raizen, R. Lee, L. Avery, Interacting genes required for pharyngeal excitation by motor neuron MC in Caenorhabditis elegans. Genetics 141, 1365– 1382 (1995). 8601480 PMC1206873
- [36]M. W. Davis, R. Fleischhauer, J. A. Dent, R. H. Joho, L. Avery, A mutation in the C. elegans exp-2 potassium channel that alters feeding behavior. Science 286, 2501– 2504 (1999). 10617464 PMC3791429
- [37]R. Fleischhauer, Ultrafast inactivation causes inward rectification in a voltage-gated K+ channel from Caenorhabditis elegans. J. Neurosci. 20, 511– 520 (2000). 10632580 PMC4442482
- [39]K. C. Bittner, A. D. Milstein, C. Grienberger, S. Romani, J. C. Magee, Behavioral time scale synaptic plasticity underlies CA1 place fields. Science 357, 1033– 1036 (2017). 28883072 PMC7289271
- [40]J. I. Kass, I. M. Mintz, Silent plateau potentials, rhythmic bursts, and pacemaker firing: Three patterns of activity that coexist in quadristable subthalamic neurons. Proc. Natl. Acad. Sci. U.S.A. 103, 183– 188 (2006). 16373507 PMC1324981
- [41]E. S. Nisenbaum, C. J. Wilson, Potassium currents responsible for inward and outward rectification in rat neostriatal spiny projection neurons. J. Neurosci. 15, 4449– 4463 (1995). 7790919 PMC6577733
- [42]R. W. Berg, A. Alaburda, J. Hounsgaard, Balanced inhibition and excitation drive spike activity in spinal half-centers. Science 315, 390– 393 (2007). 17234950
- [43]E. Salinas, T. J. Sejnowski, Impact of correlated synaptic input on output firing rate and variability in simple neuronal models. J. Neurosci. 20, 6193– 6209 (2000). 10934269 PMC6772574
- [44]D. J. Bennett, Y. Li, P. J. Harvey, M. Gorassini, Evidence for plateau potentials in tail motoneurons of awake chronic spinal rats with spasticity. J. Neurophysiol. 86, 1972– 1982 (2001). 11600654
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A feature and not a bug: Replication failures can lead to new biology
Marder, E. (2026) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2026.103268
Self-citation
- Authors
- Kenngott, M., Sengupta, P., Lockery, S., & Marder, E.
- Affiliations
- Brandeis University (US)
- University of Oregon (US)
- Corresponding author
- Marder, Eve
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2025-04-03
- Volume
- 122
- Issue
- 14
- Pages
- e2422709122-e2422709122
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC12002347
- OpenAlex
- W4409126850
- Cited by
- 1
- References
- 2
- Citations by year
- 2026: 1
- FWCI
- 0.30
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Funders
- HHS | NIH | National Institute of Neurological Disorders and Stroke (R35 NS 097343-08)
- Kavli Foundation (LS-2024 GR-41-3017)
- NSF | BIO | Division of Biological Infrastructure (NiCE: IOS-2426394)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Ion channel regulation and function
- Physical Sciences › Physics and Astronomy › Statistical and Nonlinear Physics › stochastic dynamics and bifurcation
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Keywords
- pharyngeal muscles, potassium conductance, noise robustness, computational model, Caenorhabditis elegans
- MeSH terms
- Animals, Models, Biological, Muscle Contraction, Pharyngeal Muscles, Pharynx, Potassium, Caenorhabditis elegans
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