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Summary: Emerging evidence suggests that long non-coding RNAs (lncRNAs) play diverse and critical roles in neural development, function, and disease. Here, we examine neuronal lncRNAs in a model system that offers enormous advantages for deciphering their functions: the Drosophila olfactory system. This system is numerically simple, its neurons are exquisitely well defined, and it drives multiple complex behaviors. We undertake a comprehensive survey of linear and circular lncRNAs in the Drosophila antenna and identify a wealth of lncRNAs enriched in it. We generate an unprecedented lncRNA-to-neuron map, which reveals that olfactory receptor neurons are defined not only by their receptors but also by the combination of lncRNAs they express. We identify species-specific lncRNAs, including many that are expressed primarily in pheromone-sensing neurons and that may act in modulation of pheromonal responses or in speciation. This resource opens many new opportunities for investigating the roles of lncRNAs in the nervous system.