Differential adhesion determines the organization of synaptic fascicles in the Drosophila visual system

Curr Biol. 2014 Jun 16;24(12):1304-1313. doi: 10.1016/j.cub.2014.04.047. Epub 2014 May 29.

Abstract

Background: Neuronal circuits in worms, flies, and mammals are organized so as to minimize wiring length for a functional number of synaptic connections, a phenomenon called wiring optimization. However, the molecular mechanisms that establish optimal wiring during development are unknown. We addressed this question by studying the role of N-cadherin in the development of optimally wired neurite fascicles in the peripheral visual system of Drosophila.

Results: Photoreceptor axons surround the dendrites of their postsynaptic targets, called lamina cells, within a concentric fascicle called a cartridge. N-cadherin is expressed at higher levels in lamina cells than in photoreceptors, and all genetic manipulations that invert these relative differences displace lamina cells to the periphery and relocate photoreceptor axon terminals into the center.

Conclusions: Differential expression of a single cadherin is both necessary and sufficient to determine cartridge structure because it positions the most-adhesive elements that make the most synapses at the core and the less-adhesive elements that make fewer synapses at the periphery. These results suggest a general model by which differential adhesion can be utilized to determine the relative positions of axons and dendrites to establish optimal wiring.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cadherins / genetics*
  • Cadherins / metabolism
  • Drosophila Proteins / genetics*
  • Drosophila Proteins / metabolism
  • Drosophila melanogaster / genetics
  • Drosophila melanogaster / growth & development
  • Drosophila melanogaster / physiology*
  • Larva / growth & development
  • Larva / physiology
  • Neurites / metabolism
  • Photoreceptor Cells, Invertebrate / cytology*
  • Photoreceptor Cells, Invertebrate / physiology
  • Pupa / growth & development
  • Pupa / physiology
  • Synapses / physiology
  • Visual Pathways / growth & development
  • Visual Pathways / physiology

Substances

  • CadN protein, Drosophila
  • Cadherins
  • Drosophila Proteins