From Unisensory to Multisensory Processing in the Early Olfactory System of the Drosophila Larva

Abstract

The brain detects sensory stimuli through distinct modalities, extracts and encodes relevant stimulus features, and integrates this information within and across modalities. For most animals, food-seeking behavior entails identifying odors across a wide range of concentrations, detecting changes in odor concentration, and integrating olfactory and gustatory information. How neural representations at the early sensory level are structured and organized to allow for these distinct functions is not yet fully understood. Here, we use the fruit fly larva to study how individual and populations of neurons represent distinct olfactory features as well as integrate olfactory and gustatory information at the physiological and behavioral levels. First, we investigated how the olfactory receptor neurons (ORNs) disentangle odorant identity and intensity representations. We studied the complete larval ORN population in response to a broad range of odorants types and intensities. We found that odor representations form vector-like trajectories in neuronal activity space. The distance along these trajectories correlates with concentration whereas direction correlates with odor type. Closer examination revealed that the activity of each ORN scales with odor concentration along a fixed dose-response curve with only one free variable, namely an odor dependent sensitivity. Moreover, these sensitivity values follow a statistical structure, a long-tailed distribution. Thus, several quantitative structures contribute to a low-dimensional representation of important olfactory features animals need to extract. Second, we examined olfactory and gustatory integration during navigation behavior and within the early olfactory circuit. We find that larvae show sub-additive enhancement in their orientation towards the most attractive cue when navigating combined attractive olfactory and gustatory gradients in parallel, compared to pure sensory gradients. Examination of neural circuits revealed that several local and projection neurons in the larval antennal lobe, the first olfactory processing center in the fly, show responses to both olfactory and gustatory cues and/or can be modulated by mixtures of the two stimuli. We conclude that multisensory integration begins at the earliest stages of olfactory processing.