CoChat
Sign Up
Cited by 128Advanced Fluorescence Microscopy TechniquesNeurobiology and Insect Physiology ResearchNeuroscience and Neuropharmacology Research

An Image-Free Opto-Mechanical System for Creating Virtual Environments and Imaging Neuronal Activity in Freely Moving Caenorhabditis elegans

Open access
Faumont, Serge, Rondeau, Gary, Thiele, Tod R., Lawton, Kristy J., McCormick, Kathryn E., Sottile, Matthew, Griesbeck, Oliver, Heckscher, Ellie S., Roberts, William M., Doe, Chris Q., Lockery, Shawn R.·2011·PLoS ONE
DOI 10.1371/journal.pone.0024666PMC PMC3182168
Open this paper in CoChat — free accountOpen PDF

Abstract

Non-invasive recording in untethered animals is arguably the ultimate step in the analysis of neuronal function, but such recordings remain elusive. To address this problem, we devised a system that tracks neuron-sized fluorescent targets in real time. The system can be used to create virtual environments by optogenetic activation of sensory neurons, or to image activity in identified neurons at high magnification. By recording activity in neurons of freely moving C. elegans, we tested the long-standing hypothesis that forward and reverse locomotion are generated by distinct neuronal circuits. Surprisingly, we found motor neurons that are active during both types of locomotion, suggesting a new model of locomotion control in C. elegans. These results emphasize the importance of recording neuronal activity in freely moving animals and significantly expand the potential of imaging techniques by providing a mean to stabilize fluorescent targets.

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.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1371/journal.pone.0024666

Cites

1 of 1 references verified0 citation errors · 0 not checkable

Statistics

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.

A few free checks a day · papers already verified open instantly · results are public

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 C. elegans locomotion pattern is characterized by dorsal and ventral oscillations in each class of cells occurring in antiphase.

    “(2) phase criterion: the dorsal and ventral oscillations in each class of cells occur in antiphase in order to drive the alternating dorsoventral bends responsible for locomotion (Faumont et al., 2011; Kawano et al., 2011);”

    From Potential role of a ventral nerve cord central pattern generator in forward and backward locomotion in<i>Caenorhabditis elegans</i> (2018) · cites this paper as Faumont et al., 2011

    The Results section ('Dedicated circuits for locomotion control in C. elegans'; page unavailable) says dorsal and ventral motor-neuron oscillations in each circuit are presumed to be antiphasic. A later Results section reports recordings consistent with opposite-phase activity, but does not establish the categorical claim for every class of cells. (LLM, conf=0.84)

    Experimental — accuracy not yet measured

  • The fitness function's three components capture the main three features of the in vivo calcium recordings for these motorneurons during forward and backward locomotion.

    “For each locomotion direction, neural traces were evaluated using three components that capture the main three features of the in vivo calcium recordings for these motorneurons during forward and backward locomotion (Faumont et al., 2011; Kawano et al., 2011).”

    From Potential role of a ventral nerve cord central pattern generator in forward and backward locomotion in<i>Caenorhabditis elegans</i> (2018) · cites this paper as Faumont et al., 2011

    The Results section on motor-neuron recordings reports calcium traces during forward and reverse locomotion, including oscillations in A-type neurons during forward movement and B-type neurons during reverse movement. It does not identify a set of three main recording features or establish that three fitness-function components capture them. (LLM, conf=0.82)

    Experimental — accuracy not yet measured

  • 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<i>Caenorhabditis elegans</i> (2018) · cites this paper as Faumont et al., 2011

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

Flagged first, then by citations

Research works printed but not linked: 35

  1. [1]Schregardus DS Pieneman AW Ter Maat A Jansen RF Brouwer TJ 2006 A lightweight telemetry system for recording neuronal activity in freely behaving small animals. J Neurosci Methods 155 62 71 16490257
  2. [2]Naumann EA Kampff AR Prober DA Schier AF Engert F 2010 Monitoring neural activity with bioluminescence during natural behavior. Nat Neurosci 13 513 520 20305645 PMC2846983
  3. [3]Clark DA Gabel CV Gabel H Samuel AD 2007 Temporal activity patterns in thermosensory neurons of freely moving Caenorhabditis elegans encode spatial thermal gradients. J Neurosci 27 6083 6090 17553981 PMC6672141
  4. [4]Ben Arous J Tanizawa Y Rabinowitch I Chatenay D Schafer WR 2010 Automated imaging of neuronal activity in freely behaving Caenorhabditis elegans. J Neurosci Methods 187 229 234 20096306
  5. [5]Pierce-Shimomura JT Morse TM Lockery SR 1999 The fundamental role of pirouettes in Caenorhabditis elegans chemotaxis. J Neurosci 19 9557 9569 10531458 PMC6782915
  6. [6]Chalfie M Sulston JE White JG Southgate E Thomson JN 1985 The neural circuit for touch sensitivity in Caenorhabditis elegans. J Neurosci 5 956 964 3981252 PMC6565008
  7. [7]Nagai T Yamada S Tominaga T Ichikawa M Miyawaki A 2004 Expanded dynamic range of fluorescent indicators for Ca(2+) by circularly permuted yellow fluorescent proteins. Proc Natl Acad Sci U S A 101 10554 10559 15247428 PMC490022
  8. [8]Mank M Reiff DF Heim N Friedrich MW Borst A 2006 A FRET-based calcium biosensor with fast signal kinetics and high fluorescence change. Biophys J 90 1790 1796 16339891 PMC1367327
  9. [9]Mank M Santos AF Direnberger S Mrsic-Flogel TD Hofer SB 2008 A genetically encoded calcium indicator for chronic in vivo two-photon imaging. Nat Methods 5 805 811 19160515 PMC7618336
  10. [10]Nakai J Ohkura M Imoto K 2001 A high signal-to-noise Ca(2+) probe composed of a single green fluorescent protein. Nat Biotechnol 19 137 141 11175727
  11. [11]Suster ML Martin JR Sung C Robinow S 2003 Targeted expression of tetanus toxin reveals sets of neurons involved in larval locomotion in Drosophila. J Neurobiol 55 233 246 12672020
  12. [12]Lockery SR Lawton KJ Doll JC Faumont S Coulthard SM 2008 Artificial dirt: microfluidic substrates for nematode neurobiology and behavior. J Neurophysiol 99 3136 3143 18337372 PMC2693186
  13. [13]Nagel G Szellas T Huhn W Kateriya S Adeishvili N 2003 Channelrhodopsin-2, a directly light-gated cation-selective membrane channel. Proc Natl Acad Sci U S A 100 13940 13945 14615590 PMC283525
  14. [14]Culotti JG Russell RL 1978 Osmotic avoidance defective mutants of the nematode Caenorhabditis elegans. Genetics 90 243 256 730048 PMC1213887
  15. [15]Bargmann CI Thomas JH Horvitz HR 1990 Chemosensory cell function in the behavior and development of Caenorhabditis elegans. Cold Spring Harb Symp Quant Biol 55 529 538 2132836
  16. [16]Hart AC Sims S Kaplan JM 1995 Synaptic code for sensory modalities revealed by C. elegans GLR-1 glutamate receptor. Nature 378 82 85 7477294
  17. [17]Chen BL Hall DH Chklovskii DB 2006 Wiring optimization can relate neuronal structure and function. Proc Natl Acad Sci U S A 103 4723 4728 16537428 PMC1550972
  18. [18]White JG Southgate E Thomson JN 1992 Mutations in the Caenorhabditis elegans unc-4 gene alter the synaptic input to ventral cord motor neurons. Nature 355 838 841 1538764
  19. [19]White JG Southgate E Thomson JN Brenner S 1986 The structure of the nervous system of the nematode C. elegans. Philos Trans R Soc Lond B Biol Sci 341 1 340 22462104
  20. [20]Haspel G O'Donovan MJ Hart AC 2010 Motoneurons dedicated to either forward or backward locomotion in the nematode Caenorhabditis elegans. J Neurosci 30 11151 11156 20720122 PMC2945236
  21. [21]Chronis N Zimmer M Bargmann CI 2007 Microfluidics for in vivo imaging of neuronal and behavioral activity in Caenorhabditis elegans. Nat Methods 4 727 731 17704783
  22. [22]Reiff DF Ihring A Guerrero G Isacoff EY Joesch M 2005 In vivo performance of genetically encoded indicators of neural activity in flies. J Neurosci 25 4766 4778 15888652 PMC1464576
  23. [23]Chalasani SH Chronis N Tsunozaki M Gray JM Ramot D 2007 Dissecting a circuit for olfactory behaviour in Caenorhabditis elegans. Nature 450 63 70 17972877
  24. [24]Sawin ER Ranganathan R Horvitz HR 2000 C. elegans locomotory rate is modulated by the environment through a dopaminergic pathway and by experience through a serotonergic pathway. Neuron 26 619 631 10896158
  25. [25]Goodman MB 2005 Mechanosensation. In: (June 25, WormBook, ed. The C. elegans Research Community, WormBook, doi/10.1895/wormbook.1.7.1, http://www.wormbook.org., editor · DOI
  26. [26]Marder E Bucher D Schulz DJ Taylor AL 2005 Invertebrate central pattern generation moves along. Curr Biol 15 R685 699 16139202
  27. [27]Mullins OJ Hackett JT Buchanan JT Friesen WO Neuronal control of swimming behavior: comparison of vertebrate and invertebrate model systems. Prog Neurobiol 93 244 269 21093529 PMC3034781
  28. [28]Li W Feng Z Sternberg PW Xu XZ 2006 A C. elegans stretch receptor neuron revealed by a mechanosensitive TRP channel homologue. Nature 440 684 687 16572173 PMC2865900
  29. [29]Tavernarakis N Shreffler W Wang S Driscoll M 1997 unc-8, a DEG/ENaC family member, encodes a subunit of a candidate mechanically gated channel that modulates C. elegans locomotion. Neuron 18 107 119 9010209
  30. [30]Leifer AM Fang-Yen C Gershow M Alkema MJ Samuel AD 2011 Optogenetic manipulation of neural activity in freely moving Caenorhabditis elegans. Nat Methods 8 147 152 21240279 PMC3032981
  31. [31]Stirman JN Crane MM Husson SJ Wabnig S Schultheis C 2011 Real-time multimodal optical control of neurons and muscles in freely behaving Caenorhabditis elegans. Nat Methods 8 153 158 21240278 PMC3189501
  32. [32]Brenner S 1974 The genetics of Caenorhabditis elegans. Genetics 77 71 94 4366476 PMC1213120
  33. [33]Stiernagle T The C. elegans Research Community W, ed 2006 Maintenance of C. elegans. doi/10.1895/wormbook.1.101.1. http://www.wormbook.org. editor. WormBook · DOI
  34. [34]Hendel T Mank M Schnell B Griesbeck O Borst A 2008 Fluorescence changes of genetic calcium indicators and OGB-1 correlated with neural activity and calcium in vivo and in vitro. J Neurosci 28 7399 7411 18632944 PMC6670390
  35. [35]Mahr A Aberle H 2006 The expression pattern of the Drosophila vesicular glutamate transporter: a marker protein for motoneurons and glutamatergic centers in the brain. Gene Expr Patterns 6 299 309 16378756

Cited by

Sorted by citations

Authors
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., & Lockery, S. R.
Affiliations
  • University of Oregon (US)
  • University of California, San Francisco (US)
  • Cornell University (US)
  • Galois (United States) (US)
  • Max Planck Institute of Neurobiology (DE)
  • Howard Hughes Medical Institute (US)
Corresponding author
Lockery, Shawn R.
ORCID
Venue
PLoS ONE
Publisher
Public Library of Science (PLoS)
Published
2011-09-28
Volume
6
Issue
9
Pages
e24666
ISSN
1932-6203 (ISSN-L)
DOI
10.1371/journal.pone.0024666
PMC
PMC3182168
OpenAlex
W2157127963
Cited by
128
References
1
Citations by year
2026: 3 · 2025: 3 · 2024: 5 · 2023: 8 · 2022: 6 · 2021: 11 · 2020: 4 · 2019: 8 · 2018: 11 · 2017: 7 · 2016: 9 · 2015: 14 · 2014: 11 · 2013: 14 · 2012: 12
FWCI
7.20
Type
journal article
Language
en
Open access
Licence
Locations
  • PLoS ONE (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • Max Planck Digital Library (submittedVersion, other-oa)
  • Figshare (submittedVersion, cc-by)
  • MPG.PuRe (Max Planck Society) (submittedVersion, other-oa)
Funders
  • Howard Hughes Medical Institute
  • National Institutes of Health
  • National Institute of Mental Health (R21MH112105, R29MH051383, MH051383-13, R01MH051383)
  • National Center for Research Resources
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Biophysics › Advanced Fluorescence Microscopy Techniques
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurobiology and Insect Physiology Research
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Keywords
optomechanical systems, neuronal activity imaging, optogenetic stimulation, virtual worlds, locomotion control, motor neurons, non-invasive recording
MeSH terms
Animals, Behavior, Animal, Calcium, Electrophysiology, Fluorescent Dyes, Locomotion, Models, Neurological, Motor Activity, Motor Neurons, Movement, Neurons, Osmosis, Signal Processing, Computer-Assisted, Caenorhabditis elegans

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