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Cell. 2015 Jul 2;162(1):120-33. doi: 10.1016/j.cell.2015.05.055. Epub 2015 Jun 25.

The Developmental Rules of Neural Superposition in Drosophila.

Author information

1
Green Center for Systems Biology, UT Southwestern Medical Center, Dallas, TX 75390, USA; Department of Pharmaceutical Chemistry, University of California, San Francisco, San Francisco, CA 94158, USA.
2
Department of Physiology, UT Southwestern Medical Center, Dallas, TX 75390, USA; Division of Neurobiology, Institute for Biology, Freie Universität Berlin, 14195 Berlin, Germany; NeuroCure Cluster of Excellence, Charité Universitätsmedizin Berlin, 10117 Berlin, Germany.
3
Green Center for Systems Biology, UT Southwestern Medical Center, Dallas, TX 75390, USA.
4
Green Center for Systems Biology, UT Southwestern Medical Center, Dallas, TX 75390, USA; Department of Pharmaceutical Chemistry, University of California, San Francisco, San Francisco, CA 94158, USA. Electronic address: steven.altschuler@ucsf.edu.
5
Green Center for Systems Biology, UT Southwestern Medical Center, Dallas, TX 75390, USA; Department of Physiology, UT Southwestern Medical Center, Dallas, TX 75390, USA; Division of Neurobiology, Institute for Biology, Freie Universität Berlin, 14195 Berlin, Germany; NeuroCure Cluster of Excellence, Charité Universitätsmedizin Berlin, 10117 Berlin, Germany. Electronic address: robin.hiesinger@fu-berlin.de.

Abstract

Complicated neuronal circuits can be genetically encoded, but the underlying developmental algorithms remain largely unknown. Here, we describe a developmental algorithm for the specification of synaptic partner cells through axonal sorting in the Drosophila visual map. Our approach combines intravital imaging of growth cone dynamics in developing brains of intact pupae and data-driven computational modeling. These analyses suggest that three simple rules are sufficient to generate the seemingly complex neural superposition wiring of the fly visual map without an elaborate molecular matchmaking code. Our computational model explains robust and precise wiring in a crowded brain region despite extensive growth cone overlaps and provides a framework for matching molecular mechanisms with the rules they execute. Finally, ordered geometric axon terminal arrangements that are not required for neural superposition are a side product of the developmental algorithm, thus elucidating neural circuit connectivity that remained unexplained based on adult structure and function alone.

PMID:
26119341
PMCID:
PMC4646663
DOI:
10.1016/j.cell.2015.05.055
[Indexed for MEDLINE]
Free PMC Article

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