Cited by 52Zebrafish Biomedical Research ApplicationsNeuroscience and Neuropharmacology ResearchNeurobiology and Insect Physiology Research

Functional diversity of excitatory commissural interneurons in adult zebrafish

Open access
Björnfors, E Rebecka, El Manira, Abdeljabbar·2016·eLife

Abstract

Flexibility in the bilateral coordination of muscle contraction underpins variable locomotor movements or gaits. While the locomotor rhythm is generated by ipsilateral excitatory interneurons, less is known about the commissural excitatory interneurons. Here we examined how the activity of the V0v interneurons – an important commissural neuronal class – varies with the locomotor speed in adult zebrafish. Although V0v interneurons are molecularly homogenous, their activity pattern during locomotion is not uniform. They consist of two distinct types dependent on whether they display rhythmicity or not during locomotion. The rhythmic V0v interneurons were further subdivided into three sub-classes engaged sequentially, first at slow then intermediate and finally fast locomotor speeds. Their order of recruitment is defined by scaling their synaptic current with their input resistance. Thus we uncover, in an adult vertebrate, a novel organizational principle for a key class of commissural interneurons and their recruitment pattern as a function of locomotor speed.

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 · 10.7554/elife.18579

Cites

5 of 5 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?

  • In adult zebrafish, V0v commissural excitatory neurons have bifurcating axons with shorter ascending branches and longer descending branches.

    “in adult zebrafish, V0v commissural excitatory neurons have been shown to have bifurcating axons with shorter ascending branches and longer descending branches (Björnfors and El Manira, 2016).”

    From Modeling spinal locomotor circuits for movements in developing zebrafish (2021) · cites this paper as Björnfors and El Manira, 2016

    The Results section, “Morphological diversity of V0v interneurons” (page unavailable), reports bifurcating commissural V0v neurons in adult zebrafish, with projections extending in both ascending and descending directions. It does not say that their ascending branches are shorter than their descending branches; it also describes descending, ascending, and local neurons, rather than bifurcation as a feature of all V0v neurons. (LLM, conf=0.88)

    Experimental — accuracy not yet measured
  • Commissural excitation is necessary to repeatedly activate the silent contralateral side during ongoing swimming to ensure successive left-right alternating tail beats and longer swim episodes.

    “These simulations suggest that commissural excitation is necessary to repeatedly activate the silent contralateral side during ongoing swimming to ensure successive left-right alternating tail beats and longer swim episodes (Björnfors and El Manira, 2016; Saint-Amant, 2010).”

    From Modeling spinal locomotor circuits for movements in developing zebrafish (2021) · cites this paper as Björnfors and El Manira, 2016

    The Introduction (page unavailable) describes commissural interneurons as important for left-right coordination during swimming, and the Results report rhythmic activity in excitatory V0v interneurons during swim episodes. The paper does not establish that commissural excitation is necessary to repeatedly activate a silent contralateral side or to produce longer swim episodes; the cited sentence frames those as conclusions from the citing authors’ simulations. (LLM, conf=0.84)

    Experimental — accuracy not yet measured
  • Different subgroups of V0v neurons are probably involved in coiling versus swimming.

    “While V0v neurons are the likely candidate to mediate the activation of contralateral movements, different subgroups of V0v neurons are probably involved in coiling versus swimming (Björnfors and El Manira, 2016; Jay and McLean, 2019) considering the two different targets of contralateral excitation involved, namely ICs in coiling and V2as in swimming.”

    From Modeling spinal locomotor circuits for movements in developing zebrafish (2021) · cites this paper as Björnfors and El Manira, 2016

    The Introduction and Discussion (‘The functional role of V0v interneurons during locomotion’; page unavailable) identify distinct V0v subgroups recruited at slow, intermediate, and fast swimming speeds. The paper does not address coiling or establish that different subgroups participate in coiling versus swimming. (LLM, conf=0.85)

    Experimental — accuracy not yet measured
  • Subgroups for vigor seem to be present within the V2a and V0v populations.

    “Subgroups for vigor seem to be present within the V2a (Menelaou and McLean, 2019; Song et al., 2018) and V0v (Björnfors and El Manira, 2016; Jay and McLean, 2019; McLean et al., 2007) populations.”

    From Modeling spinal locomotor circuits for movements in developing zebrafish (2021) · cites this paper as Björnfors and El Manira, 2016

  • Swim frequency modules likely include commissural excitatory V0v INs and commissural inhibitory INs belonging to either the dI6 or V0d populations.

    “Swim frequency modules likely include commissural excitatory V0v INs (Björnfors and El Manira, 2016; McLean et al., 2008) and commissural inhibitory INs belonging to either the dI6 or V0d populations (Satou et al., 2020).”

    From Modeling spinal locomotor circuits for movements in developing zebrafish (2021) · cites this paper as Björnfors and El Manira, 2016

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: 27

  1. Ampatzis K Song J Ausborn J El Manira A 2013 Pattern of innervation and recruitment of different classes of motoneurons in adult zebrafish Journal of Neuroscience 33 10875 10886 10.1523/JNEUROSCI.0896-13.2013 23804107 PMC6618491 · DOI · Paper page
  2. Arber S 2012 Motor circuits in action: specification, connectivity, and function Neuron 74 975 989 10.1016/j.neuron.2012.05.011 22726829 · DOI
  3. Ausborn J Mahmood R El Manira A 2012 Decoding the rules of recruitment of excitatory interneurons in the adult zebrafish locomotor network PNAS 109 E3631 E3639 10.1073/pnas.1216256110 23236181 PMC3535644 · DOI
  4. Buchanan JT 1999a Commissural interneurons in rhythm generation and intersegmental coupling in the lamprey spinal cord Journal of Neurophysiology 81 2037 2045 10322045
  5. Buchanan JT 1999b The roles of spinal interneurons and motoneurons in the lamprey locomotor network Progress in Brain Research 123 311 321 10.1016/s0079-6123(08)62866-6 10635726 · DOI
  6. Butt SJ Kiehn O 2003 Functional identification of interneurons responsible for left-right coordination of hindlimbs in mammals Neuron 38 953 963 10.1016/S0896-6273(03)00353-2 12818180 · DOI
  7. Dale N 1985 Reciprocal inhibitory interneurones in the Xenopus embryo spinal cord Journal of Physiology 363 61 70 10.1113/jphysiol.1985.sp015695 4020706 PMC1192914 · DOI
  8. Fetcho JR McLean DL 2010 Some principles of organization of spinal neurons underlying locomotion in zebrafish and their implications Annals of the New York Academy of Sciences 1198 94 104 10.1111/j.1749-6632.2010.05539.x 20536924 PMC3579554 · DOI
  9. Fidelin K Djenoune L Stokes C Prendergast A Gomez J Baradel A Del Bene F Wyart C 2015 State-Dependent Modulation of Locomotion by GABAergic Spinal Sensory Neurons Current Biology 25 3035 3047 10.1016/j.cub.2015.09.070 26752076 · DOI
  10. Gabriel JP Ausborn J Ampatzis K Mahmood R Eklöf-Ljunggren E El Manira A 2011 Principles governing recruitment of motoneurons during swimming in zebrafish Nature Neuroscience 14 93 99 10.1038/nn.2704 21113162 · DOI
  11. Griener A Zhang W Kao H Wagner C Gosgnach S 2015 Probing diversity within subpopulations of locomotor-related V0 interneurons Developmental Neurobiology 75 1189 1203 10.1002/dneu.22277 25649879 · DOI
  12. Grillner S Jessell TM 2009 Measured motion: searching for simplicity in spinal locomotor networks Current Opinion in Neurobiology 19 572 586 10.1016/j.conb.2009.10.011 19896834 PMC2951840 · DOI
  13. Kimura Y Satou C Higashijima S 2008 V2a and V2b neurons are generated by the final divisions of pair-producing progenitors in the zebrafish spinal cord Development 135 3001 3005 10.1242/dev.024802 18684740 · DOI
  14. Kyriakatos A Mahmood R Ausborn J Porres CP Büschges A El Manira A 2011 Initiation of locomotion in adult zebrafish Journal of Neuroscience 31 8422 8431 10.1523/JNEUROSCI.1012-11.2011 21653846 PMC6623330 · DOI
  15. Lanuza GM Gosgnach S Pierani A Jessell TM Goulding M 2004 Genetic identification of spinal interneurons that coordinate left-right locomotor activity necessary for walking movements Neuron 42 375 386 10.1016/S0896-6273(04)00249-1 15134635 · DOI
  16. Liu DW Westerfield M 1988 Function of identified motoneurones and co-ordination of primary and secondary motor systems during zebra fish swimming Journal of Physiology 403 73 89 10.1113/jphysiol.1988.sp017239 3253426 PMC1190703 · DOI · Paper page
  17. McLean DL Fan J Higashijima S Hale ME Fetcho JR 2007 A topographic map of recruitment in spinal cord Nature 446 71 75 10.1038/nature05588 17330042 · DOI · Paper page
  18. McLean DL Fetcho JR 2009 Spinal interneurons differentiate sequentially from those driving the fastest swimming movements in larval zebrafish to those driving the slowest ones Journal of Neuroscience 29 13566 13577 10.1523/JNEUROSCI.3277-09.2009 19864569 PMC2796107 · DOI
  19. McLean DL Masino MA Koh IY Lindquist WB Fetcho JR 2008 Continuous shifts in the active set of spinal interneurons during changes in locomotor speed Nature Neuroscience 11 1419 1429 10.1038/nn.2225 18997790 PMC2735137 · DOI · Paper page
  20. Mentel T Cangiano L Grillner S Büschges A 2008 Neuronal substrates for state-dependent changes in coordination between motoneuron pools during fictive locomotion in the lamprey spinal cord Journal of Neuroscience 28 868 879 10.1523/JNEUROSCI.4250-07.2008 18216195 PMC6671005 · DOI
  21. Moran-Rivard L Kagawa T Saueressig H Gross MK Burrill J Goulding M 2001 Evx1 is a postmitotic determinant of v0 interneuron identity in the spinal cord Neuron 29 385 399 10.1016/S0896-6273(01)00213-6 11239430 · DOI
  22. Moult PR Cottrell GA Li WC 2013 Fast silencing reveals a lost role for reciprocal inhibition in locomotion Neuron 77 129 140 10.1016/j.neuron.2012.10.040 23312521 PMC3542422 · DOI
  23. Pierani A Moran-Rivard L Sunshine MJ Littman DR Goulding M Jessell TM 2001 Control of interneuron fate in the developing spinal cord by the progenitor homeodomain protein Dbx1 Neuron 29 367 384 10.1016/S0896-6273(01)00212-4 11239429 · DOI
  24. Satou C Kimura Y Higashijima S 2012 Generation of multiple classes of V0 neurons in zebrafish spinal cord: progenitor heterogeneity and temporal control of neuronal diversity Journal of Neuroscience 32 1771 1783 10.1523/JNEUROSCI.5500-11.2012 22302816 PMC6703360 · DOI
  25. Satou C Kimura Y Hirata H Suster ML Kawakami K Higashijima S 2013 Transgenic tools to characterize neuronal properties of discrete populations of zebrafish neurons Development 140 3927 3931 10.1242/dev.099531 23946442 · DOI
  26. Soffe SR Clarke JD Roberts A 1984 Activity of commissural interneurons in spinal cord of Xenopus embryos Journal of Neurophysiology 51 1257 1267 6737030
  27. Talpalar AE Bouvier J Borgius L Fortin G Pierani A Kiehn O 2013 Dual-mode operation of neuronal networks involved in left-right alternation Nature 500 85 88 10.1038/nature12286 23812590 · DOI

Cited by

Sorted by citations

Authors
Björnfors, E. R., & El Manira, A.
Affiliations
  • Karolinska Institutet (SE)
  • Department of Neuroscience, Karolinska Institute, Stockholm, Sweden
Venue
eLife
Published
2016-08-25
Volume
5
ISSN
2050-084X (ISSN-L)
OpenAlex
W2516102782
Cited by
52
References
5
Citations by year
2026: 4 · 2025: 3 · 2024: 3 · 2023: 9 · 2022: 3 · 2021: 6 · 2020: 7 · 2019: 9 · 2018: 5 · 2017: 3
FWCI
3.90
Type
journal article
Language
en
Open access
Locations
  • eLife (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders
  • Karolinska Institutet
  • Swedish Brain Foundation
  • Swedish Research Council
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Zebrafish Biomedical Research Applications
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurobiology and Insect Physiology Research
Keywords
commissural interneurons, locomotion speed, locomotor rhythm, bilateral coordination, interneuron subtypes, synaptic currents, input resistance, zebrafish, spinal cord

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