Multiple Strategies Establish and Maintain Sex-Specific Neural Circuit Identities in Olfactory Neurons

Abstract

During development, sensory neurons must choose identities that allow them to detect specific signals and connect with appropriate target neurons. Ultimately, these sensory neurons will successfully integrate into appropriate neural circuits togenerate defined motor outputs, or behavior. This integration requires developmental coordination between the identity of the neuron and the identity of the circuit. The mechanisms that underlie this coordination are currently unknown. Here we describe two modes of regulation that coordinate the sensory identities of Drosophila melanogaster olfactory receptor neurons (ORNs) involved in sex-specific behaviors with the sex-specific behavioral circuit identity marker fruitless. During development, the putative chromatin modulator Alhambra (Alh) represses the expression of both fru and of specific olfactory receptors, helping to coordinate and establish both the sensory and circuit identities of the ORNs involved in sex-specific behaviors. In contrast, the maintenance of fru expression and thus the identities ofthese ORNs in adults utilize signaling from olfactory receptors through Cam Kinases and the histone acetyl transferase p300/CBP. Our results highlight feed-forward regulatory mechanisms with both developmentally hardwired and olfactory receptor activity-dependent components that establish and maintain fru expression in ORNs.These mechanisms might underlie innate and adaptable aspects of odor-guided sex- specific behaviors.