Extraocular motoneuron pools develop along a dorsoventral axis in zebrafish, Danio rerio

J Comp Neurol. 2017 Jan 1;525(1):65-78. doi: 10.1002/cne.24042. Epub 2016 Jun 1.

Abstract

Both spatial and temporal cues determine the fate of immature neurons. A major challenge at the interface of developmental and systems neuroscience is to relate this spatiotemporal trajectory of maturation to circuit-level functional organization. This study examined the development of two extraocular motor nuclei (nIII and nIV), structures in which a motoneuron's identity, or choice of muscle partner, defines its behavioral role. We used retro-orbital dye fills, in combination with fluorescent markers for motoneuron location and birthdate, to probe spatial and temporal organization of the oculomotor (nIII) and trochlear (nIV) nuclei in the larval zebrafish. We describe a dorsoventral organization of the four nIII motoneuron pools, in which inferior and medial rectus motoneurons occupy dorsal nIII, while inferior oblique and superior rectus motoneurons occupy distinct divisions of ventral nIII. Dorsal nIII motoneurons are, moreover, born before motoneurons of ventral nIII and nIV. The order of neurogenesis can therefore account for the dorsoventral organization of nIII and may play a primary role in determining motoneuron identity. We propose that the temporal development of extraocular motoneurons plays a key role in assembling a functional oculomotor circuit. J. Comp. Neurol. 525:65-78, 2017. © 2016 The Authors The Journal of Comparative Neurology Published by Wiley Periodicals, Inc.

Keywords: RRID:SCR_002285; RRID:SCR_010279; RRID:ZFIN_ZDB-GENO-030919-1; RRID:ZFIN_ZDB-GENO-060619-2; cranial nerve; cranial nucleus; development; nIII; nucleogenesis; oculomotor.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Animals
  • Animals, Genetically Modified
  • Green Fluorescent Proteins / genetics
  • Green Fluorescent Proteins / metabolism
  • Larva
  • Microphthalmia-Associated Transcription Factor / genetics
  • Microphthalmia-Associated Transcription Factor / metabolism
  • Microscopy, Fluorescence
  • Motor Neurons / cytology*
  • Motor Neurons / metabolism
  • Neuroanatomical Tract-Tracing Techniques
  • Neurogenesis
  • Zebrafish / anatomy & histology*
  • Zebrafish / growth & development*
  • Zebrafish / metabolism
  • Zebrafish Proteins / genetics
  • Zebrafish Proteins / metabolism

Substances

  • Microphthalmia-Associated Transcription Factor
  • Zebrafish Proteins
  • mitfa protein, zebrafish
  • Green Fluorescent Proteins