Conserved and divergent development of brainstem vestibular and auditory nuclei

Elife. 2018 Dec 19:7:e40232. doi: 10.7554/eLife.40232.

Abstract

Vestibular function was established early in vertebrates and has remained, for the most part, unchanged. In contrast, each group of tetrapods underwent independent evolutionary processes to solve the problem of hearing on land, resulting in a remarkable mixture of conserved, divergent and convergent features that define extant auditory systems. The vestibuloacoustic nuclei of the hindbrain develop from a highly conserved ground plan and provide an ideal framework on which to address the participation of developmental processes to the evolution of neuronal circuits. We employed an electroporation strategy to unravel the contribution of two dorsoventral and four axial lineages to the development of the chick hindbrain vestibular and auditory nuclei. We compare the chick developmental map with recently established genetic fate-maps of the developing mouse hindbrain. Overall, we find considerable conservation of developmental origin for the vestibular nuclei. In contrast, a comparative analysis of the developmental origin of hindbrain auditory structures echoes the complex evolutionary history of the auditory system. In particular, we find that the developmental origin of the chick auditory interaural time difference circuit supports its emergence from an ancient vestibular network, unrelated to the analogous mammalian counterpart.

Keywords: auditory; chicken; development; developmental biology; evolution; hindbrain; mouse; neuroscience; vestibular.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Auditory Pathways / cytology
  • Auditory Pathways / embryology
  • Auditory Pathways / metabolism
  • Brain Stem / cytology
  • Brain Stem / embryology*
  • Brain Stem / metabolism
  • Chick Embryo
  • Chickens
  • Cochlear Nucleus / cytology
  • Cochlear Nucleus / embryology*
  • Cochlear Nucleus / metabolism
  • Electroporation
  • Gene Expression Regulation, Developmental
  • Mice
  • Mice, Transgenic
  • Neurons / metabolism
  • Rhombencephalon / cytology
  • Rhombencephalon / embryology
  • Rhombencephalon / metabolism
  • Species Specificity
  • Vestibular Nuclei / cytology
  • Vestibular Nuclei / embryology*
  • Vestibular Nuclei / metabolism
  • Vestibule, Labyrinth / cytology
  • Vestibule, Labyrinth / embryology*
  • Vestibule, Labyrinth / metabolism

Grants and funding

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.