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Motoneurons Dedicated to Either Forward or Backward Locomotion in the Nematode Caenorhabditis elegans
Open accessAbstract
Multifunctional motoneurons and muscles, which are active during forward and backward locomotion are ubiquitous in animal models. However, studies in the nematode Caenorhabditis elegans suggest that some locomotor motoneurons are necessary only for forward locomotion (dorsal B-motoneurons, DB), while others (dorsal A-motoneurons, DA) are necessary only for backward locomotion. We tested this hypothesis directly by recording the activity of these motoneurons during semirestrained locomotion. For this purpose, we used epifluorescence imaging of the genetically encoded calcium sensor cameleon, expressed in specific motoneurons, while monitoring locomotor behavior through the microscope condenser using a second camera. We found that ventral and dorsal B-motoneurons (DB and VB) were coactive during forward locomotion while ventral A-motoneurons (VA) were only active during backward locomotion. The signals we recorded correlated with the direction of locomotion but not with the faster undulatory cycles. To our knowledge, these are the first recordings of motoneuron activity in C. elegans and the only direction-dedicated motoneurons described to date.
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The C. elegans locomotion pattern is characterized by A- and B-class motorneurons oscillating.
“(1) Oscillation criterion: the A- and B-class motorneurons oscillate (Faumont et al., 2011; Haspel et al., 2010; Kawano et al., 2011);”
From Potential role of a ventral nerve cord central pattern generator in forward and backward locomotion in Caenorhabditis elegans (2018) · cites this paper as Haspel et al., 2010
The Abstract reports that A- and B-class motorneuron signals correlated with locomotion direction, not the faster undulatory cycles. The Results section, “No dorsoventral alternating activity was recorded in B-motorneurons,” likewise reports no detected activity correlated with the undulations. The Discussion cautions that the recordings cannot establish whether alternating activity is absent, but the paper does not characterize these motorneurons as oscillating. (LLM, conf=0.88)
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Experimental — accuracy not yet measuredThe C. elegans locomotion pattern is characterized by B-class activity exceeding A-class activity during forward locomotion, whereas A-class activity exceeds B-class activity during backward locomotion.
“(3) dominance criterion: B-class activity exceeds A-class activity during forward locomotion, whereas A-class activity exceeds B-class activity during backward locomotion (Haspel et al., 2010; Kawano et al., 2011).”
From Potential role of a ventral nerve cord central pattern generator in forward and backward locomotion in Caenorhabditis elegans (2018) · cites this paper as Haspel et al., 2010
DA and DB motor neurons drive backward and forward locomotion, respectively.
“It has been demonstrated that DA and DB motor neurons drive backward and forward locomotion, respectively (Haspel et al., 2010;Wen et al., 2012).”
From TMEM55B promotes anterograde transport and distal axonal distribution of LAMP1-positive organelles (2026) · cites this paper as Haspel et al., 2010
During backward locomotion in the full circuit, the minimum activity of VA remains quite high, as in the worm.
“As in the worm (Haspel et al., 2010; Kawano et al., 2011), during backward locomotion in the full circuit the minimum activity of VA remains quite high.”
From Potential role of a ventral nerve cord central pattern generator in forward and backward locomotion in Caenorhabditis elegans (2018) · cites this paper as Haspel et al., 2010
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“Both classes of motoneuron possess long undifferentiated posterior processes that may function as a stretch receptor (White et al., 1986).”
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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
Distributed rhythm generators underlie Caenorhabditis elegans forward locomotion
Fouad, A. D., Teng, S., Mark, J. R., Liu, A., Alvarez-Illera, P., Ji, H., Du, A., Bhirgoo, P. D., Cornblath, E., Guan, S. A., et al. (2018) · eLife · doi:10.7554/elife.29913 · Cited by 79
From head to tail: a neuromechanical model of forward locomotion in Caenorhabditis elegans
Izquierdo, E. J., & Beer, R. D. (2018) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2017.0374 · Cited by 56
Sherlekar, A. L., Janssen, A., Siehr, M. S., Koo, P. K., Caflisch, L., Boggess, M., & Lints, R. (2013) · PLoS ONE · doi:10.1371/journal.pone.0060597 · Cited by 46
Olivares, E. O., Izquierdo, E. J., & Beer, R. D. (2018) · Network Neuroscience · doi:10.1162/netn_a_00036 · Cited by 38
“…neural traces of this circuit for forward and backward locomotion, we observed traces that matched all the main features (Faumont et al., 2011; Haspel et al., 2010; Kawano et al., 2011) (Figure 2B): (1) A- and B-class motorneurons oscillate; (2) dorsal and ventral motorneurons oscillate in…”
BackgroundMethodInfluentialRosenbaum, P., Schmitz, J., Schmidt, J., & Büschges, A. (2015) · Journal of Neurophysiology · doi:10.1152/jn.00006.2015 · Cited by 15
TMEM55B promotes anterograde transport and distal axonal distribution of LAMP1-positive organelles
Rudnik, S., Li, C. H., Gottschling, D.-C., Veh, A., Barbosa, D. J., Richter, J., Stroobants, S., Schuster, B., Beck, I. M., Sedlack, R., et al. (2026) · doi:10.64898/2026.10.27.762112
Metadata
- Authors
- Haspel, G., O'Donovan, M. J., & Hart, A. C.
- Affiliations
- National Institutes of Health (US)
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2010-08-18
- Volume
- 30
- Issue
- 33
- Pages
- 11151-11156
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC2945236
- OpenAlex
- W1994557483
- Cited by
- 71
- References
- 1
- Citations by year
- 2026: 5 · 2025: 1 · 2024: 2 · 2023: 1 · 2022: 3 · 2021: 4 · 2020: 5 · 2019: 4 · 2018: 6 · 2017: 6 · 2016: 4 · 2015: 3 · 2014: 5 · 2013: 9 · 2012: 6
- FWCI
- 2.56
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- University of Oregon
- National Institutes of Health
- RIKEN
- National Institute of General Medical Sciences (R01GM057918)
- National Institute of Neurological Disorders and Stroke (ZIANS003022, R01NS055813)
- National Center for Research Resources
- 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 › Motor Control and Adaptation
- Keywords
- Caenorhabditis elegans, locomotion, motor neurons, forward locomotion, backward locomotion, motoneuron activity, calcium imaging, cameleon
- MeSH terms
- Animals, Larva, Locomotion, Motor Neurons, Muscles, Periodicity, Caenorhabditis elegans, Dermoscopy
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