Odour representations supporting ethology-relevant categorisation and discrimination in the Drosophila mushroom body

Abstract

Neural representations of sensory stimuli serve multiple distinct purposes, from the rapid recognition of familiar environments, to the precise identification of individual salient cues. In the insect mushroom body (MB), odours are encoded by the activity of Kenyon cells (KCs). The random wiring of olfactory projection neurons (PNs) and KCs in the MB calyx is thought to enhance odour discrimination. Here, we examined the impact of deviations from random wiring and demonstrated their significant roles in shaping odour representations. We confirm that different KC types have distinct PN input biases correlated with the contextual relevance of the odour information delivered by the PNs. By recording the functional responses of different KC types to ethologically defined odour categories, we found that the {beta} and {beta} KCs produce segregated representations of relevant odour groups, potentially enhancing the categorisation of odours based on ethological relevance. Simultaneously, these same KC types displayed distinct representations for food-related odours, supporting precise discrimination. In contrast, {gamma} KCs lacked significant segregation of odour representations by ethological category. Computational simulations refined with our functional data indicated that the specific PN input connection pattern of individual KC types largely accounts for the observed representations. Taken together, we propose that individual KC types process odour information with distinct objectives, supporting both ethological categorisation and discrimination.