Neural Network Organization for Courtship Song Feature Detection in Drosophila

Abstract

Animals communicate using sounds in a wide range of contexts, and auditory systems must encode behaviorally relevant acoustic features to drive appropriate reactions. How feature detection emerges along auditory pathways has been difficult to solve due to challenges in mapping the underlying circuits and characterizing responses to behaviorally relevant features. Here, we study auditory activity in the Drosophila melanogaster brain and investigate feature selectivity for the two main modes of fly courtship song, sinusoids and pulse trains. We identify 24 new cell types of the intermediate layers of the auditory pathway, and using a new connectomic resource, FlyWire, we map all synaptic connections between these cell types, in addition to connections to known early and higher-order auditory neurons - this represents the first map of the auditory pathway. We additionally determine the sign (excitatory or inhibitory) of most synapses in this auditory connectome. We find that auditory neurons display a continuum of preferences for courtship song modes, and that neurons with different song mode preferences are highly interconnected in a network that lacks hierarchical structure. Among this network, frequency tuning is centered on the range of frequencies present in song, whereas pulse rate tuning extends to rates outside of song, suggesting that these neurons form a basis set for downstream processing. Our study provides new insights into the organization of auditory coding within the Drosophila brain.