Diversity and Wiring Variability of Olfactory Local Interneurons in the Drosophila Antennal Lobe

Local interneurons play essential roles in information processing by neural circuits. Here we present a comprehensive genetic, anatomical, and electrophysiological analysis of local interneurons (LNs) in the Drosophila antennal lobe, the first olfactory processing center in the brain. We find that LNs are diverse in their neurotransmitter profiles, connectivity, and physiological properties. Analysis of >1500 individual LNs reveals major morphological classes characterized by coarsely stereotyped glomerular innervation patterns. Some of these morphological classes exhibit distinct physiological properties. However, the finer-scale connectivity of an individual LN varies considerably across brains and there is notable physiological variability within each morphological or genetic class. Finally, we show that LN innervation requires interaction with olfactory receptor neurons during development, and some individual variability also likely reflects LN-LN interactions. Our results reveal an unexpected degree of complexity and individual variation in an invertebrate neural circuit, a result that creates challenges for solving the Drosophila connectome.