Abstract
In Drosophila, 50 classes of olfactory receptor neurons (ORNs) connect to 50 class-specific and uniquely positioned glomeruli in the antennal lobe. Despite the identification of cell surface receptors regulating axon guidance, how ORN axons sort to form 50 stereotypical glomeruli remains unclear. Here we show that the heterophilic cell adhesion proteins, DIPs and Dprs, are expressed in ORNs during glomerular formation. Many ORN classes express a unique combination of DIPs/dprs, with neurons of the same class expressing interacting partners, suggesting a role in class-specific self-adhesion between ORN axons. Analysis of DIP/Dpr expression revealed that ORNs that target neighboring glomeruli have different combinations, and ORNs with very similar DIP/Dpr combinations can project to distant glomeruli in the antennal lobe. DIP/Dpr profiles are dynamic during development and correlate with sensilla type lineage for some ORN classes. Perturbations of DIP/dpr gene function result in local projection defects of ORN axons and glomerular positioning, without altering correct matching of ORNs with their target neurons. Our results suggest that context-dependent differential adhesion through DIP/Dpr combinations regulate self-adhesion and sort ORN axons into uniquely positioned glomeruli.
Highlights
One of the most complex biological systems in nature is the human brain, which contains an estimated 86 billion neurons wired to make approximately 100 trillion synaptic connections [1]
In Drosophila, 50 classes of olfactory receptor neurons (ORNs) connect to 50 class-specific and uniquely positioned glomeruli in the antennal lobe, providing a complex yet workable model to understand the organization of glomerular structures and morphology
We show that the heterophilic cell adhesion proteins, Dpr Interacting Proteins (DIPs) and Defective proboscis response (Dpr), are expressed in ORNs during glomerular formation
Summary
One of the most complex biological systems in nature is the human brain, which contains an estimated 86 billion neurons wired to make approximately 100 trillion synaptic connections [1]. The expression of genes, those encoding cell surface receptors (CSRs), relay attractive or repulsive cues to regulate each step of this wiring program. Mutations affecting these programs are associated with numerous neurodevelopmental and neuropsychiatric disorders, as well as many known brain cancers [4,5,6,7]. While individual examples of CSRs directing axon guidance and connectivity are well known and evolutionarily conserved, how they act in combinations to coordinate large scale organizational patterns among a diverse set of neurons within a circuit remains poorly understood
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