The Order and Place of Neuronal Differentiation Establish the Topography of Sensory Projections and the Entry Points within the Hindbrain

J Neurosci. 2015 May 13;35(19):7475-86. doi: 10.1523/JNEUROSCI.3743-14.2015.

Abstract

Establishing topographical maps of the external world is an important but still poorly understood feature of the vertebrate sensory system. To study the selective innervation of hindbrain regions by sensory afferents in the zebrafish embryo, we mapped the fine-grained topographical representation of sensory projections at the central level by specific photoconversion of sensory neurons. Sensory ganglia located anteriorly project more medially than do ganglia located posteriorly, and this relates to the order of sensory ganglion differentiation. By single-plane illumination microscopy (SPIM) in vivo imaging, we show that (1) the sequence of arrival of cranial ganglion inputs predicts the topography of central projections, and (2) delaminated neuroblasts differentiate in close contact with the neural tube, and they never loose contact with the neural ectoderm. Afferent entrance points are established by plasma membrane interactions between primary differentiated peripheral sensory neurons and neural tube border cells with the cooperation of neural crest cells. These first contacts remain during ensuing morphological growth to establish pioneer axons. Neural crest cells and repulsive slit1/robo2 signals then guide axons from later-differentiating neurons toward the neural tube. Thus, this study proposes a new model by which the topographical representation of cranial sensory ganglia is established by entrance order, with the entry points determined by cell contact between the sensory ganglion cell bodies and the hindbrain.

Keywords: axon navigation; inner ear; neural crest cells; neuron differentiation; sensory systems; somatotopy.

Publication types

  • Research Support, Non-U.S. Gov't
  • Video-Audio Media

MeSH terms

  • Afferent Pathways / drug effects
  • Afferent Pathways / physiology*
  • Animals
  • Animals, Genetically Modified
  • Basic Helix-Loop-Helix Transcription Factors / genetics
  • Basic Helix-Loop-Helix Transcription Factors / metabolism
  • Brain Mapping*
  • Cell Differentiation / genetics
  • Cell Differentiation / physiology*
  • Chemokine CXCL12 / metabolism
  • DNA-Binding Proteins / genetics
  • DNA-Binding Proteins / metabolism
  • Embryo, Nonmammalian
  • Enzyme Inhibitors / pharmacology
  • Female
  • Gene Expression Regulation, Developmental / genetics
  • Gene Expression Regulation, Developmental / physiology*
  • Isoxazoles / pharmacology
  • LIM-Homeodomain Proteins / genetics
  • LIM-Homeodomain Proteins / metabolism
  • Leflunomide
  • Male
  • Morpholinos / pharmacology
  • Nerve Tissue Proteins / genetics
  • Nerve Tissue Proteins / metabolism
  • Neural Tube / cytology
  • Rhombencephalon / anatomy & histology*
  • Rhombencephalon / drug effects
  • Rhombencephalon / embryology
  • Sensory Receptor Cells / drug effects
  • Sensory Receptor Cells / physiology*
  • Signal Transduction / genetics
  • Signal Transduction / physiology
  • Transcription Factors / genetics
  • Transcription Factors / metabolism
  • Zebrafish
  • Zebrafish Proteins / genetics
  • Zebrafish Proteins / metabolism

Substances

  • Basic Helix-Loop-Helix Transcription Factors
  • Chemokine CXCL12
  • DNA-Binding Proteins
  • Enzyme Inhibitors
  • Gal4 protein, zebrafish
  • Isoxazoles
  • LIM-Homeodomain Proteins
  • Morpholinos
  • Nerve Tissue Proteins
  • Transcription Factors
  • Zebrafish Proteins
  • isl2b protein, zebrafish
  • NeuroD protein
  • Leflunomide