Effect of Interglomerular Inhibitory Networks on Olfactory Bulb Odor Representations

Lateral inhibition is a fundamental feature of circuits that process sensory information. In the mammalian olfactory system, inhibitory interneurons called short axon cells (SACs) comprise the first network mediating lateral inhibition between glomeruli, the functional units of early olfactory coding and processing. The connectivity of this network and its impact on odor representations is not well understood. To explore this question, we constructed a computational model of the interglomerular inhibitory network using detailed characterizations of SAC morphologies taken from mouse olfactory bulb (OB). We then examined how this network transformed glomerular patterns of odorant-evoked sensory input (taken from previously-published datasets) as a function of the selectivity of interglomerular inhibition. We examined three connectivity schemes: selective (each glomerulus connects to few others with heterogeneous strength), nonselective (glomeruli connect to most others with heterogenous strength), or global (glomeruli connect to all others with equal strength). We found that both selective and nonselective interglomerular networks could mediate heterogeneous patterns of inhibition across glomeruli when driven by realistic sensory input patterns, but that global inhibitory networks were unable to produce input-output transformations that matched experimental data and were poor mediators of intensity-dependent gain control. We further found that networks whose interglomerular connectivities were tuned by sensory input profile decorrelated odor representations more effectively. These results suggest that, despite their multiglomerular innervation patterns, SACs are capable of mediating odorant-specific patterns of inhibition between glomeruli that could, theoretically, be tuned by experience or evolution to optimize discrimination of particular odorants.