Untangling the wiring of the Drosophila visual system: developmental principles and molecular strategies

Abstract

The assembly of neural circuits relies on the accurate establishment of connections between synaptic partners. Precise wiring results from responses that neurons elicit to environmental cues and cell–cell contact events during development. A common design principle in both invertebrate and vertebrate adult nervous systems is the orderly array of columnar and layered synaptic units of certain neuropils. This similarity is particularly striking in the visual system, both at the structural and cell-type levels. Given the powerful genetic approaches and tools available in Drosophila, the fly visual system has been extensively used to probe how specific wiring patterns are achieved during development. In this review, we cover the developmental principles and molecular strategies that govern the assembly of columnar units (lamina cartridges and medulla columns), the formation of layers, afferent specific layer selection, and synaptogenesis in Drosophila. The mechanisms include: sequential developmental steps that ensure coordinated assembly of synaptic partners; anterograde and autocrine signaling; interactions between cell-surface molecules, or secreted molecules and their receptors that take place among neurons; and glia signaling to neurons.

Keywords:

• Neural circuits
• wiring specificity
• synaptic partners
• columns and layers
• cell surface and secreted molecules

Acknowledgements

We apologize to our colleagues whose work was not included due to space limitations. We thank C-H. Lee and P.R. Hiesinger for critical reading and insightful comments on the manuscript.

Disclosure statement

No potential conflict of interest was reported by the authors.

Additional information

Funding

This work was supported by an APIF fellowship from the University of Barcelona (to H. P-S.), a FPI fellowship (BES-2013-065103) from the Spanish Ministerio de Economía y Competitividad (to A. F-P.); a Ramón y Cajal contract (RYC-2011-09479); and a Spanish Ministerio de Economía y Competitividad grant (BFU2015-69689-P) (to M. M.).