Peripheral non-synaptic inhibition facilitates odor processing in fly brains

In insects, Olfactory Receptor Neurons ('ORNs') are grouped together into sensory hairs ('sensilla') in a stereotypical manner. Grouped ORNs: (i) antagonistically regulate the same behaviors, (ii) mutually inhibit each other via electrical interactions, and (iii) have a systematic size-asymmetry, resulting in asymmetric inhibitory interactions. The functional significance of this highly conserved organization is not known. We constructed a phenomenological model of nonlinearly coupled ORNs, which shows that inhibition between ORNs transiently amplifies the hedonic value ('valence') of an odor stimulus, as conveyed by ORN responses. Our analysis suggests that through this peripheral 'pre-processing' step, olfactory signals are prepared to be read-out effectively by central brain circuits. Specifically, in order to leverage the stimulus-specific valence amplification, downstream readouts of ORN activity must reflect peripheral sensory structure. Our analysis of Antennal Lobe (AL) to Lateral Horn (LH) connections in the fly connectome confirms these predictions: biases in AL to LH projections are consistent with interaction asymmetries of coupled ORNs. Further, using a population level model of coupled ORNs, we show that peripheral interactions modify the structure of AL responses. This modification is essential for the classification of high-dimensional stimuli in the Mushroom Body (MB), facilitated by random and expansive AL to MB projections. Taken together, stereotyped electrical inhibition between ORNs at the sensory periphery is crucial for odor processing in the fly brain.