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Diversity and wiring variability of olfactory local interneurons in the Drosophila antennal lobe


Local interneurons are essential in information processing by neural circuits. Here we present a comprehensive genetic, anatomical and electrophysiological analysis of local interneurons (LNs) in the Drosophila melanogaster antennal lobe, the first olfactory processing center in the brain. We found LNs to be diverse in their neurotransmitter profiles, connectivity and physiological properties. Analysis of >1,500 individual LNs revealed principal morphological classes characterized by coarsely stereotyped glomerular innervation patterns. Some of these morphological classes showed distinct physiological properties. However, the finer-scale connectivity of an individual LN varied considerably across brains, and there was notable physiological variability within each morphological or genetic class. Finally, LN innervation required interaction with olfactory receptor neurons during development, and some individual variability also likely reflected 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.

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Figure 1: Antennal lobe LNs.
Figure 2: Diversity of LN morphology.
Figure 3: Statistical analysis of glomerular innervation patterns.
Figure 4: Functional stereotypy and diversity among genetic classes.
Figure 5: Functional differences between morphological classes.
Figure 6: Variability and stereotypy of line 6 LNs.
Figure 7: Variability of patchy LNs.
Figure 8: Development but not maintenance of LN arborization depends on ORNs.


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We thank U. Heberlein (University of California, San Francisco) and E. Marin for respectively providing and screening unpublished Gal4 lines, which lead to identification of line 1 and line 6; J. Simpson (Janelia Farm, Howard Hughes Medical Institute) for providing unpublished LCCH3 (line 7) Gal4; K. Wehner (Stanford University) for mouse anti-HA; A. DiAntonio (Washington University) for rabbit anti-DVGLUT; and the Bloomington Stock Center, Kyoto Stock Center, Drosophila Genetic Resource Center, Gal4 Enhancer Trap Insertion Database (GETDB), and Developmental Studies Hybridoma Bank for other reagents. M.L.S. is grateful for the help of J. Brooks in data collection. We thank the Stanford Department of Statistics Consulting Service for technical help with statistical analyses. We thank T. Clandinin, G. Jefferis and members of the Luo and Wilson laboratories for helpful comments on the manuscript. This work was supported by US National Institutes of Health grants to L.L. (R01-DC005982) and R.I.W. (R01-DC008174), a Pew Scholar award, a McKnight Scholar award, a Sloan Foundation research fellowship, and a Beckman Young Investigator award (to R.I.W). M.L.S. is supported by a US National Research Service predoctoral award. E.Y. is supported by a Human Frontiers Science Program Long Term Fellowship. J.C.S.L. is supported by the Medical Scientist Training Program at Stanford University. L.L. receives investigator support from the Howard Hughes Medical Institute.

Author information




Y.-H.C. and M.L.S. performed the anatomical and developmental experiments. E.Y. performed the physiological experiments. J.C.S.L. helped with statistical analysis. L.L. and R.I.W. supervised the project and wrote the paper.

Corresponding authors

Correspondence to Rachel I Wilson or Liqun Luo.

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The authors declare no competing financial interests.

Supplementary information

Supplementary Text and Figures

Supplementary Tables 1 and 4, Supplementary Figures 1–11 (PDF 1737 kb)

Supplementary Table 2

Raw data for ipsilateral glomerular innervation patterns (XLS 639 kb)

Supplementary Table 3

Raw data for contralateral glomerular innervation patterns of bilateral projection LNs (XLS 52 kb)

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Chou, YH., Spletter, M., Yaksi, E. et al. Diversity and wiring variability of olfactory local interneurons in the Drosophila antennal lobe. Nat Neurosci 13, 439–449 (2010).

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