The Evolution and Development of Neural Superposition

Abstract

Visual systems have a rich history as model systems for the discovery and understanding of basic principles underlying neuronal connectivity. The compound eyes of insects consist of up to thousands of small unit eyes that are connected by photoreceptor axons to set up a visual map in the brain. The photoreceptor axon terminals thereby represent neighboring points seen in the environment in neighboring synaptic units in the brain. Neural superposition is a special case of such a wiring principle, where photoreceptors from different unit eyes that receive the same input converge upon the same synaptic units in the brain. This wiring principle is remarkable, because each photoreceptor in a single unit eye receives different input and each individual axon, among thousands others in the brain, must be sorted together with those few axons that have the same input. Key aspects of neural superposition have been described as early as 1907. Since then neuroscientists, evolutionary and developmental biologists have been fascinated by how such a complicated wiring principle could evolve, how it is genetically encoded, and how it is developmentally realized. In this review article, we will discuss current ideas about the evolutionary origin and developmental program of neural superposition. Our goal is to identify in what way the special case of neural superposition can help us answer more general questions about the evolution and development of genetically “hard-wired” synaptic connectivity in the brain.

Keywords::

• Drosophila
• Visual System
• synapse
• brain wiring

ACKNOWLEDGEMENTS

We would like to thank all members of the Hiesinger lab, Tom Clandinin, Ian Meinertzhagen, Claude Desplan, and Roland Melzer for discussion.

Declaration of interest: The authors report no conflicts of interest. The authors alone are responsible for the content and writing of the paper.

The work was supported by grants from the National Institute of Health to PRH (RO1EY018884, RO1EY02 3333) and the Welch Foundation to PRH (I-1657). This work was further supported by grant from the National Institute of Health to SJA (R01CA133253) and LFW (R01GM071794) and the Welch Foundation to SJA (I-1619) and LFW (I-1644). ML was supported by a Green Center for Systems Biology Postdoctoral Fellowship.