title: A hybrid electrical/chemical circuit in the spinal cord generates a transient embryonic motor behavior.
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.
authors.affiliation: Departments of Pathology and Cell Biology and Neuroscience, Research Centre of the University of Montréal Hospital Centre and Groupe de Recherche sur le Systeme Nerveux Central, Université de Montréal, Montréal, Québec H3T 1J4, Canada.
authors.forename: Laura D
authors.identifier: http://orcid.org/0000-0001-7111-9832
authors.initials: LD
authors.lastname: Knogler
authors.affiliation: Departments of Pathology and Cell Biology and.
authors.forename: Joel
authors.initials: J
authors.lastname: Ryan
authors.affiliation: Departments of Pathology and Cell Biology and.
authors.forename: Louis
authors.initials: L
authors.lastname: Saint-Amant
authors.affiliation: Departments of Pathology and Cell Biology and Neuroscience, Research Centre of the University of Montréal Hospital Centre and Groupe de Recherche sur le Systeme Nerveux Central, Université de Montréal, Montréal, Québec H3T 1J4, Canada p.drapeau@umontreal.ca.
authors.forename: Pierre
authors.initials: P
authors.lastname: Drapeau
mesh_terms: D018750:6-Cyano-7-nitroquinoxaline-2,3-dione / Q000494:pharmacology; D000200:Action Potentials / Q000187:drug effects / Q000502:physiology; D000818:Animals; D030801:Animals, Genetically Modified; D004268:DNA-Binding Proteins / Q000235:genetics; D004305:Dose-Response Relationship, Drug; D004558:Electric Stimulation; D004625:Embryo, Nonmammalian; D018691:Excitatory Amino Acid Antagonists / Q000494:pharmacology; D018698:Glutamic Acid / Q000378:metabolism / Q000494:pharmacology; D049452:Green Fluorescent Proteins / Q000235:genetics / Q000378:metabolism; D009043:Motor Activity / Q000187:drug effects / Q000502:physiology*; D009046:Motor Neurons / Q000187:drug effects / Q000502:physiology*; D009415:Nerve Net / Q000187:drug effects / Q000502:physiology*; D009434:Neural Pathways / Q000187:drug effects / Q000196:embryology; D012249:Rhombencephalon / Q000502:physiology; D013116:Spinal Cord / Q000166:cytology* / Q000196:embryology; D013569:Synapses / Q000145:classification / Q000187:drug effects / Q000502:physiology*; D014157:Transcription Factors / Q000235:genetics; D014633:Valine / Q000031:analogs & derivatives / Q000494:pharmacology; D015027:Zebrafish; D029961:Zebrafish Proteins / Q000235:genetics
chemical_list: D004268:DNA-Binding Proteins; D018691:Excitatory Amino Acid Antagonists; C542436:Gal4 protein, zebrafish; D014157:Transcription Factors; D029961:Zebrafish Proteins; D049452:Green Fluorescent Proteins; D018698:Glutamic Acid; D018750:6-Cyano-7-nitroquinoxaline-2,3-dione; C056639:2-amino-5-phosphopentanoic acid; D014633:Valine
keywords: V2a interneurons; glutamate; locomotor development; motoneurons; spinal cord; zebrafish embryo