Spatially anisotropic and isotropic lateral inhibition: Convergent circuit designs in the insect antennal lobe and vertebrate olfactory bulb

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Inhibitory neurons are an essential component of nervous systems, balancing and modulating the output from excitatory neural subnetworks. Across olfactory systems in the animal kingdom, inhibition is particularly dominant. Highly complex and dense inhibitory circuits control the impact of sensory neuron input. Yet more strikingly, inhibitory neurons are the main mediators of interactions between second order principal neurons that lack direct synaptic contacts with each other. These pathways are thought to regulate olfactory sensitivity in a state-dependent manner, provide gain control, synchronize the spiking activity of principal neuron ensembles, and enhance the contrast of representations of similar odorants via decorrelation of their response patterns. The architecture of the underlying network anatomy is astonishingly similar across insects and vertebrates - a prime example of convergent evolution. Here we aim to further clarify the cellular correlates of defined inhibitory interactions within early olfactory processing across phylae. More specifically, we will investigate the cellular basis and functional impact of dominant forms of inhibition within the fly antennal lobe and the rat olfactory bulb, namely recurrent inhibition and isotropic and anisotropic lateral inhibition, the latter allowing for directed interactions between individual glomerular channels that might be even hard-wired. Beyond the first phase of the SPP funding period, that was focussed on anisotropic inhibition across phylae and in partly delayed due to the pandemic, we now plan to also identify the anatomical correlates of recurrent inhibition and isotropic lateral inhibition in the fly, to ultimately assign the mentioned specific inhibitory interactions to defined interneuron types. Next, we will test these assignments and their functional impact in experiments that involve targeted silencing of the respective interneuron subtypes during innate and learned odor-guided behavior. In parallel we plan to integrate the results of these and previous investigations into lineage-specific network models that are based on realistic neuroanatomical parameters derived from recent ultrastructural data and functional data from our own and others work. Ultimately, we aim to use these models to develop a new generic network model of the convergent olfactory system, in tight collaboration with other members of the priority program with computational and circuits expertise.