CoChat
Sign Up
Cited by 8Neurobiology and Insect Physiology ResearchMotor Control and AdaptationNeuroscience and Neuropharmacology Research

Reconciling the functions of even-skipped interneurons during crawling, swimming, and walking

Open access
Jay, Michael, McLean, David L·2019·Current Opinion in Physiology
DOI 10.1016/j.cophys.2019.02.003PMC PMC6820970
Open this paper in CoChat — free account

Abstract

In all bilaterally symmetric animals, movements across the body are coordinated by interneurons that traverse the midline. Recent work is beginning to tease apart the functional complexity of interneurons labeled by the homeodomain transcription factor even-skipped, which provide a phylogenetically-conserved source of commissural excitation during locomotion in both vertebrates and invertebrates. Here we review recent studies of the roles of even-skipped neurons during locomotion in flies (EL neurons), fishes, frogs, and mice (V0v neurons). Comparisons across species reveal commonalities, which include the functional organization of even-skipped circuits based on birth order, the link between increased muscular complexity and even-skipped neuron diversity, and the hierarchical organization of even-skipped circuits based on their control of escape versus exploratory movements. We discuss how stronger links between different species enable testable predictions to further the discovery of principles of locomotor network organization.

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 · 10.1016/j.cophys.2019.02.003

Cites

4 of 4 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?

  • 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 Jay and McLean, 2019

    The ‘Even-skipped interneurons and swimming’ section describes early-born ascending V0v neurons recruited during spontaneous whole-body bends and later-born MCoDs participating in exploratory swimming. This supports the idea that different V0v subgroups serve different movements, but the paper does not explicitly identify those bends as coiling or establish the proposed IC-versus-V2a targets. Page numbers are unavailable in our copy. (LLM, conf=0.82)

    Experimental — accuracy not yet measured

  • V0v neurons are a population of glutamatergic commissural INs, some of which may be involved in larger amplitude locomotor movements such as coiling.

    “V0v neurons are a population of glutamatergic commissural INs, some of which may be involved in larger amplitude locomotor movements such as coiling (Jay and McLean, 2019).”

    From Modeling spinal locomotor circuits for movements in developing zebrafish (2021) · cites this paper as Jay and McLean, 2019

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: 36

  1. [2]Suster ML, Kania A, Liao M, Asakawa K, Charron F, Kawakami K, Drapeau P: A novel conserved evx1 enhancer links spinal interneuron morphology and cis-regulation from fish to mammals. Dev Biol 2009, 325: 422– 433. 18992237
  2. [3]Duman-Scheel M, Patel NH: Analysis of molecular marker expression reveals neuronal homology in distantly related arthropods. Development 1999, 126: 2327– 2334. 10225992
  3. [4]Doe CQ, Smouse D, Goodman CS: Control of neuronal fate by the Drosophila segmentation gene even-skipped. Nature 1988, 333: 376– 378. 3374572
  4. [5]Clark MQ, Zarin AA, Carreira-Rosario A, Doe CQ: Neural circuits driving larval locomotion in Drosophila. Neural Dev 2018, 13: 6. 29673388 PMC5907184
  5. [6]Pulver SR, Bayley TG, Taylor AL, Berni J, Bate M, Hedwig B: Imaging fictive locomotor patterns in larval Drosophila. J Neurophysiol 2015, 114: 2564– 2577. 26311188 PMC4637366
  6. [8]Wreden CC, Meng JL, Feng W, Chi W, Marshall ZD, Heckscher ES: Temporal cohorts of lineage-related neurons perform analogous functions in distinct sensorimotor circuits. Curr Biol 2017, 27: 1521– 1528 e1524. 28502656 ** The authors establish developmentally distinct cohorts of Eve-positive interneurons contribute to distinct motor circuits. Eve-positive interneurons integrate different sensory modalities to drive slow and fast modes of motor output.
  7. [9]Ohyama T, Schneider-Mizell CM, Fetter RD, Aleman JV, Franconville R, Rivera-Alba M, Mensh BD, Branson KM, Simpson JH, Truman JW,: A multilevel multimodal circuit enhances action selection in Drosophila. Nature 2015, 520: 633– 639. 25896325
  8. [10]Brustein E, Saint-Amant L, Buss RR, Chong M, McDearmid JR, Drapeau P: Steps during the development of the zebrafish locomotor network. J Physiol Paris 2003, 97: 77– 86. 14706693
  9. [11]Hale ME: Developmental change in the function of movement systems: transition of the pectoral fins between respiratory and locomotor roles in zebrafish. Integr Comp Biol 2014, 54: 238– 249. 24748600 PMC4097112
  10. [12]Siomava N, Shkil F, Voronezhskaya E, Diogo R: Development of zebrafish paired and median fin musculature: basis for comparative, developmental, and macroevolutionary studies. Sci Rep 2018, 8: 14187. 30242203 PMC6155031
  11. [13]Lanuza GM, Gosgnach S, Pierani A, Jessell TM, Goulding M: Genetic identification of spinal interneurons that coordinate left-right locomotor activity necessary for walking movements. Neuron 2004, 42: 375– 386. 15134635
  12. [14]Moran-Rivard L, Kagawa T, Saueressig H, Gross MK, Burrill J, Goulding M: Evx1 is a postmitotic determinant of v0 interneuron identity in the spinal cord. Neuron 2001, 29: 385– 399. 11239430
  13. [15]Satou C, Kimura Y, Higashijima S: Generation of multiple classes of V0 neurons in zebrafish spinal cord: progenitor heterogeneity and temporal control of neuronal diversity. J Neurosci 2012, 32: 1771– 1783. 22302816 PMC6703360
  14. [16]Knogler LD, Drapeau P: Sensory gating of an embryonic zebrafish interneuron during spontaneous motor behaviors. Front Neural Circuits 2014, 8: 121. 25324729 PMC4179717
  15. [17]Juarez-Morales JL, Martinez-De Luna RI, Zuber ME, Roberts A, Lewis KE: Zebrafish transgenic constructs label specific neurons in Xenopus laevis spinal cord and identify frog V0v spinal neurons. Dev Neurobiol 2017, 77: 1007– 1020. 28188691 PMC5513754
  16. [18]Juarez-Morales JL, Schulte CJ, Pezoa SA, Vallejo GK, Hilinski WC, England SJ, de Jager S, Lewis KE: Evx1 and Evx2 specify excitatory neurotransmitter fates and suppress inhibitory fates through a Pax2-independent mechanism. Neural Dev 2016, 11: 5. 26896392 PMC4759709
  17. [19]Roberts A, Hill NA, Hicks R: Simple mechanisms organise orientation of escape swimming in embryos and hatchling tadpoles of Xenopus laevis. J Exp Biol 2000, 203: 1869– 1885. 10821744
  18. [20]Sillar KT, Robertson RM: Thermal activation of escape swimming in post-hatching Xenopus laevis frog larvae. J Exp Biol 2009, 212: 2356– 2364. 19617428 PMC2712414
  19. [21]McLean DL, Fetcho JR: Spinal interneurons differentiate sequentially from those driving the fastest swimming movements in larval zebrafish to those driving the slowest ones. J Neurosci 2009, 29: 13566– 13577. 19864569 PMC2796107
  20. [22]McLean DL, Masino MA, Koh IY, Lindquist WB, Fetcho JR: Continuous shifts in the active set of spinal interneurons during changes in locomotor speed. Nat Neurosci 2008, 11: 1419– 1429. 18997790 PMC2735137
  21. [23]Green MH, Hale ME: Activity of pectoral fin motoneurons during two swimming gaits in the larval zebrafish (Danio rerio) and localization of upstream circuit elements. J Neurophysiol 2012, 108: 3393– 3402. 23034362
  22. [24]McLean DL, Fan J, Higashijima S, Hale ME, Fetcho JR: A topographic map of recruitment in spinal cord. Nature 2007, 446: 71– 75. 17330042
  23. [25]Bjornfors ER, El Manira A: Functional diversity of excitatory commissural interneurons in adult zebrafish. Elife 2016, 5. PMC5039025 27559611 ** The authors provide a detailed characterization of the morphological and electrophysiological properties of V0v interneurons at juvenile/adult stages in zebrafish. The majority of V0v types are not active during low-frequency exploratory locomotion, consistent with studies at larval stages.
  24. [26]Kyriakatos A, Mahmood R, Ausborn J, Porres CP, Buschges A, El Manira A: Initiation of locomotion in adult zebrafish. J Neurosci 2011, 31: 8422– 8431. 21653846 PMC6623330
  25. [27]Gabriel JP, Mahmood R, Walter AM, Kyriakatos A, Hauptmann G, Calabrese RL, El Manira A: Locomotor pattern in the adult zebrafish spinal cord in vitro. J Neurophysiol 2008, 99: 37– 48. 17977928
  26. [28]Masino MA, Fetcho JR: Fictive swimming motor patterns in wild type and mutant larval zebrafish. J Neurophysiol 2005, 93: 3177– 3188. 15673549
  27. [29]McLean DL, Dougherty KJ: Peeling back the layers of locomotor control in the spinal cord. Curr Opin Neurobiol 2015, 33: 63– 70. 25820136 PMC4523447
  28. [31]Talpalar AE, Bouvier J, Borgius L, Fortin G, Pierani A, Kiehn O: Dual-mode operation of neuronal networks involved in left-right alternation. Nature 2013, 500: 85– 88. 23812590
  29. [32]Ruder L, Takeoka A, Arber S: Long-distance descending spinal neurons ensure quadrupedal locomotor stability. Neuron 2016, 92: 1063– 1078. 27866798 * By retrograde labeling, the authors demonstrated the presence of long-range descending V0vs linking cervical and lumbar regions in the mouse spinal cord. Ablation of these cells revealed a role for long-range projecting V0vs during motor output which was previously not appreciated.
  30. [33]Griener A, Zhang W, Kao H, Wagner C, Gosgnach S: Probing diversity within subpopulations of locomotor-related V0 interneurons. Dev Neurobiol 2015, 75: 1189– 1203. 25649879
  31. [34]Danner SM, Shevtsova NA, Frigon A, Rybak IA: Computational modeling of spinal circuits controlling limb coordination and gaits in quadrupeds. Elife 2017, 6. PMC5726855 29165245 * In this study, the authors provide a computational model of quadrupedal spinal circuits. By incorporating recent results, the authors were able to successfully recapitulate the behavioural results of experimental manipulations of different cell populations. The model also suggests unique roles for local and long-range V0vs.
  32. [35]Jung H, Baek M, D’Elia KP, Boisvert C, Currie PD, Tay BH, Venkatesh B, Brown SM, Heguy A, Schoppik D,: The Ancient Origins of Neural Substrates for Land Walking. Cell 2018, 172: 667– 682 e615. 29425489 PMC5808577 ** The authors demonstrate that the molecular program underpinning the specification of fin and limb motor neuron pools is conserved between tetrapods and fish that use their pelvic fins to locomote. These results suggest the basic spinal networks coordinating locomotion are highly conserved.
  33. [36]Bevan S, Burrows M: Localisation of Even-skipped in the mature CNS of the locust, Schistocerca gregaria. Cell Tissue Res 2003, 313: 237– 244. 12883992
  34. [37]Bohm UL, Prendergast A, Djenoune L, Nunes Figueiredo S, Gomez J, Stokes C, Kaiser S, Suster M, Kawakami K, Charpentier M,: CSF-contacting neurons regulate locomotion by relaying mechanical stimuli to spinal circuits. Nat Commun 2016, 7: 10866. 26946992 PMC4786674
  35. [38]Fidelin K, Djenoune L, Stokes C, Prendergast A, Gomez J, Baradel A, Del Bene F, Wyart C: State-dependent modulation of locomotion by GABAergic spinal sensory neurons. Curr Biol 2015, 25: 3035– 3047. 26752076 ** This study is the first to demonstrate V0v interneurons receive synaptic inputs from a unique class of cerebrospinal fluid-contacting mechanosensitive interneuron, thus further demonstrating conserved sensory integration functions across species.
  36. [39]Caggiano V, Leiras R, Goni-Erro H, Masini D, Bellardita C, Bouvier J, Caldeira V, Fisone G, Kiehn O: Midbrain circuits that set locomotor speed and gait selection. Nature 2018, 553: 455– 460. 29342142 PMC5937258 * The authors identify two key midbrain structures which comprise the mesencephalic locomotor region and examine how these structures contribute to different modes of motor output.

Cited by

Sorted by citations

Authors
Jay, M., & McLean, D. L.
Affiliations
Northwestern University (US)
Corresponding author
McLean, David L
ORCID
McLean, David L
Venue
Current Opinion in Physiology
Publisher
Elsevier BV
Published
2019-04
Volume
8
Pages
188-192
ISSN
2468-8673 (ISSN-L)
DOI
10.1016/j.cophys.2019.02.003
PMC
PMC6820970
OpenAlex
W2918921409
Cited by
8
References
4
Citations by year
2026: 1 · 2024: 2 · 2022: 2 · 2021: 1 · 2020: 2
FWCI
0.17
Type
journal article
Language
en
Open access
Licence
Locations
  • Current Opinion in Physiology (acceptedVersion)
  • PubMed (publishedVersion)
  • Europe PMC (PubMed Central) (acceptedVersion)
  • PubMed Central (acceptedVersion)
Funders
  • National Institutes of Health (R01-NS067299)
  • National Science Foundation (IOS-1456830)
Topics
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurobiology and Insect Physiology Research
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Motor Control and Adaptation
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Keywords
commissural interneurons, locomotor circuits, crawling, swimming, walking, birth order, escape behavior, exploratory behavior, Drosophila, zebrafish, frogs, mice, interneuron diversity

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