A hybrid electrical/chemical circuit in the spinal cord generates a transient embryonic motor behavior

Knogler, L.D., Ryan, J., Saint-Amant, L., Drapeau, P.
The Journal of neuroscience : the official journal of the Society for Neuroscience   34: 9644-55 (Journal)
Registered Authors
Drapeau, Pierre, Saint-Amant, Louis
V2a interneurons, glutamate, locomotor development, motoneurons, spinal cord, zebrafish embryo
MeSH Terms
  • 6-Cyano-7-nitroquinoxaline-2,3-dione/pharmacology
  • Action Potentials/drug effects
  • Action Potentials/physiology
  • Animals
  • Animals, Genetically Modified
  • DNA-Binding Proteins/genetics
  • Dose-Response Relationship, Drug
  • Electric Stimulation
  • Embryo, Nonmammalian
  • Excitatory Amino Acid Antagonists/pharmacology
  • Glutamic Acid/metabolism
  • Glutamic Acid/pharmacology
  • Green Fluorescent Proteins/genetics
  • Green Fluorescent Proteins/metabolism
  • Motor Activity/drug effects
  • Motor Activity/physiology*
  • Motor Neurons/drug effects
  • Motor Neurons/physiology*
  • Nerve Net/drug effects
  • Nerve Net/physiology*
  • Neural Pathways/drug effects
  • Neural Pathways/embryology
  • Rhombencephalon/physiology
  • Spinal Cord/cytology*
  • Spinal Cord/embryology
  • Synapses/classification
  • Synapses/drug effects
  • Synapses/physiology*
  • Transcription Factors/genetics
  • Valine/analogs & derivatives
  • Valine/pharmacology
  • Zebrafish
  • Zebrafish Proteins/genetics
25031404 Full text @ J. Neurosci.
Spontaneous network activity is a highly stereotyped early feature of developing circuits throughout the nervous system, including in the spinal cord. Spinal locomotor circuits produce a series of behaviors during development before locomotion that reflect the continual integration of spinal neurons into a functional network, but how the circuitry is reconfigured is not understood. The first behavior of the zebrafish embryo (spontaneous coiling) is mediated by an electrical circuit that subsequently generates mature locomotion (swimming) as chemical neurotransmission develops. We describe here a new spontaneous behavior, double coiling, that consists of two alternating contractions of the tail in rapid succession. Double coiling was glutamate-dependent and required descending hindbrain excitation, similar to but preceding swimming, making it a discrete intermediary developmental behavior. At the cellular level, motoneurons had a distinctive glutamate-dependent activity pattern that correlated with double coiling. Two glutamatergic interneurons, CoPAs and CiDs, had different activity profiles during this novel behavior. CoPA neurons failed to show changes in activity patterns during the period in which double coiling appears, whereas CiD neurons developed a glutamate-dependent activity pattern that correlated with double coiling and they innervated motoneurons at that time. Additionally, double coils were modified after pharmacological reduction of glycinergic neurotransmission such that embryos produced three or more rapidly alternating coils. We propose that double coiling behavior represents an important transition of the motor network from an electrically coupled spinal cord circuit that produces simple periodic coils to a spinal network driven by descending chemical neurotransmission, which generates more complex behaviors.
Genes / Markers
Mutations / Transgenics
Human Disease / Model
Sequence Targeting Reagents
Engineered Foreign Genes