RRC ID 33654
Author Knogler LD, Ryan J, Saint-Amant L, Drapeau P.
Title A hybrid electrical/chemical circuit in the spinal cord generates a transient embryonic motor behavior.
Journal J Neurosci
Abstract 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.
Volume 34(29)
Pages 9644-55
Published 2014-7-16
DOI 10.1523/JNEUROSCI.1225-14.2014
PII 34/29/9644
PMID 25031404
PMC PMC6608330
MeSH 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
IF 6.074
Times Cited 12
Zebrafish Tg[chx10:Gal4]