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Cited by 53Zebrafish Biomedical Research ApplicationsNeuroscience and Neuropharmacology ResearchNeural dynamics and brain function

Pacemaker and Plateau Potentials Shape Output of a Developing Locomotor Network

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Tong, Huaxia, McDearmid, Jonathan Robert·2012·Current Biology
DOI 10.1016/j.cub.2012.10.025PMC PMC3525839
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Abstract

BACKGROUND: During development, spinal networks undergo an intense period of maturation in which immature forms of motor behavior are observed. Such behaviors are transient, giving way to more mature activity as development proceeds. The processes governing age-specific transitions in motor behavior are not fully understood. RESULTS: Using in vivo patch clamp electrophysiology, we have characterized ionic conductances and firing patterns of developing zebrafish spinal neurons. We find that a kernel of spinal interneurons, the ipsilateral caudal (IC) cells, generate inherent bursting activity that depends upon a persistent sodium current (I(NaP)). We further show that developmental transitions in motor behavior are accompanied by changes in IC cell bursting: during early life, these cells generate low frequency membrane oscillations that likely drive "coiling," an immature form of motor output. As fish mature to swimming stages, IC cells switch to a sustained mode of bursting that permits generation of high-frequency oscillations during locomotion. Finally, we find that perturbation of IC cell bursting disrupts motor output at both coiling and swimming stages. CONCLUSIONS: Our results suggest that neurons with unique bursting characteristics are a fundamental component of developing motor networks. During development, these may shape network output and promote stage-specific reconfigurations in motor behavior.

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  • Parameter values of ICs were chosen such that they exhibited a relatively depolarized threshold of action potentials and bursts of short action potentials lasting hundreds of milliseconds as seen in experimental recordings in embryonic zebrafish.

    “Parameter values of ICs (see Table 4 for all neuron parameters) were chosen such that they exhibited a relatively depolarized threshold of action potentials and bursts of short action potentials lasting hundreds of milliseconds as seen in experimental recordings in embryonic zebrafish (Tong and McDearmid, 2012).”

    From Modeling spinal locomotor circuits for movements in developing zebrafish (2021) · cites this paper as Tong and McDearmid, 2012

    The Results sections on coiling and early swimming report IC-cell bursting with small spikelets, supporting that aspect of the description. But the reported thresholds are for oscillations or sustained bursts, not explicitly for action potentials; the reported events last about 1.19 seconds at coiling stages and 1 to more than 20 seconds at early swimming stages, rather than hundreds of milliseconds. The cited copy provides no page numbers for these passages. (LLM, conf=0.87)

    Experimental — accuracy not yet measured

  • Rostrally located IC pacemaker spinal neurons drive periodic depolarizations (PDs) of ipsilateral MNs via electrical synapses.

    “It has been proposed that rostrally located IC pacemaker spinal neurons (Tong and McDearmid, 2012) drive periodic depolarizations (PDs) of ipsilateral MNs via electrical synapses (Drapeau et al., 2002; Saint-Amant and Drapeau, 2001).”

    From Modeling spinal locomotor circuits for movements in developing zebrafish (2021) · cites this paper as Tong and McDearmid, 2012

    The Results section, “Inherent INaP-Dependent Bursting Activity at Coiling Stages” (page unavailable), identifies spinal IC cells as having pacemaker properties. The Results section, “INaP-Dependent Bursting Activity and Locomotion” (page unavailable), also reports that IC-cell bursts depolarized paired neurons, including motoneurons, through electrical coupling. The copy does not establish the specified rostral location, and its direct coupling observations concern the early swimming network rather than specifically identifying the source of motoneuron PDs during coiling. (LLM, conf=0.78)

    Experimental — accuracy not yet measured

  • The single coiling model predicts that IC and V0d are coupled together to facilitate the activation of V0ds, which are responsible for the glycinergic SBs observed in spinal neurons at this stage.

    “For instance, the single coiling model predicts that IC and V0d are coupled together to facilitate the activation of V0ds, which are responsible for the glycinergic SBs observed in spinal neurons at this stage (Saint-Amant and Drapeau, 2001; Tong and McDearmid, 2012).”

    From Modeling spinal locomotor circuits for movements in developing zebrafish (2021) · cites this paper as Tong and McDearmid, 2012

    The Results section on coiling-stage activity reports IC-cell pacemaker properties and describes synaptic bursts as volleys of glycine released from newly integrated secondary neurons (page unavailable). The Results section on locomotion finds electrical coupling between IC cells and other neurons, but at early swimming stages. Our copy does not identify V0d neurons or show IC–V0d coupling during single coiling, so it does not support that specific model prediction. (LLM, conf=0.86)

    Experimental — accuracy not yet measured

  • IC INs are thought to play an essential role in driving the rhythm of early locomotor behavior due to their endogenous bursting activity.

    “These include Ipsilateral Caudal (IC) INs that are thought to play an essential role in driving the rhythm of early locomotor behavior due to their endogenous bursting activity (Tong and McDearmid, 2012).”

    From Modeling spinal locomotor circuits for movements in developing zebrafish (2021) · cites this paper as Tong and McDearmid, 2012

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Authors
Tong, H., & McDearmid, J. R.
Affiliations
University of Leicester (GB)
Corresponding author
McDearmid, Jonathan Robert
Venue
Current Biology
Publisher
Elsevier BV
Published
2012-12
Volume
22
Issue
24
Pages
2285-2293
ISSN
0960-9822 (ISSN-L)
DOI
10.1016/j.cub.2012.10.025
PMC
PMC3525839
OpenAlex
W2016749689
Cited by
53
References
1
Citations by year
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FWCI
1.36
Type
journal article
Language
en
Open access
Licence
Locations
  • Current Biology (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
Funders
Biotechnology and Biological Sciences Research Council (BB/F01516X/1)
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 › Cognitive Neuroscience › Neural dynamics and brain function
Keywords
spinal cord development, burst firing, persistent sodium current, membrane potential oscillations, swimming, zebrafish, ionic conductance, pacemaker potential, plateau potentials
MeSH terms
Animals, Locomotion, Neurons, Patch-Clamp Techniques

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