The irre Cell Recognition Module (IRM) Protein Kirre Is Required to Form the Reciprocal Synaptic Network of L4 Neurons in the Drosophila Lamina

Abstract

Each neuropil module, or cartridge, in the fly's lamina has a fixed complement of cells. Of five types of monopolar cell interneurons, only L4 has collaterals that invade neighboring cartridges. In the proximal lamina, these collaterals form reciprocal synapses with both the L2 of their own cartridge and the L4 collateral branches from two other neighboring cartridges. During synaptogenesis, L4 collaterals strongly express the cell adhesion protein Kirre, a member of the irre cell recognition module (IRM) group of proteins (, J Neurogenet, 23, 48–67). The authors show by mutant analysis and gene knockdown techniques that L4 neurons develop their lamina collaterals in the absence of this cell adhesion protein. Using electron microscopy (EM), the authors demonstrate, however, that without Kirre protein these L4 collaterals selectively form fewer synapses. The collaterals of L4 neurons of various genotypes reconstructed from serial-section EM revealed that the number of postsynaptic sites was dramatically reduced in the absence of Kirre, almost eliminating any synaptic input to L4 neurons. A significant reduction of presynaptic sites was also detected in kirre⁰ mutants and gene knockdown flies using RNA interference. L4 neuron reciprocal synapses are thus almost eliminated. A presynaptic marker, Brp-short^GFP confirmed these data using confocal microscopy. This study reveals that removing Kirre protein specifically disrupts the functional L4 synaptic network in the Drosophila lamina.

Keywords::

• cell adhesion
• cell recognition
• connectivity
• Neph proteins
• neural circuit
• optic lobe
• synapse
• visual system

ACKNOWLEDGMENTS

This work was supported by grants from the DFG (Fi 336/8-1 to KFF) and NIH (EY-03592 to IAM). We thank Margit Böhler, Martin Piringer, and Tanja Zöller (Freiburg) and Jolanta Borycz (Halifax) for technical support and Mar Ruiz-Gómez (Madrid) for supplying kirre⁰ mutant flies.

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