Laterality and interhemispheric integration in the larval Drosophila olfactory system

All animals with bilateral symmetry must integrate the sensory input from the left and right sides of their bodies to make coherent perceptual decisions. In Drosophila larvae, connectomic evidence suggests that olfactory signals from the two sides of the head are initially processed independently (as in the mammalian olfactory system) before being combined in the central brain. By pairing volumetric calcium imaging in intact larvae with microfluidic odor delivery and targeted laser ablation at the sensory periphery, we have mapped the propagation of olfactory signals between the two brain hemispheres, across successive layers of the larval olfactory system. This approach implicates the mushroom body (MB) as a key substrate for interhemispheric integration of odor representations. Whereas the two larval MBs appear to process odors largely independently at the level of their intrinsic neurons (Kenyon cells), the modulatory neurons of the MB show strongly symmetrized responses to asymmetric olfactory stimuli. Nevertheless, odor responses in some MB output neurons (MBONs), up to 5 synapses downstream from the sensory periphery, preserve information about stimulus laterality. Moreover, we show that asymmetric activation of these MBONs can modulate the animal’s turning behavior in a side-biased manner. These findings suggest that the deeply lateralized architecture of the larval olfactory system balances the need for interhemispheric integration with the advantages of parallel sensory processing.