Relational representation in the olfactory system

Abstract

The perceptual quality of odors usually is robust to variability in concentration. However, maps of neural activation across the olfactory bulb glomerular layer are not stable in this respect; rather, glomerular odor representations both broaden and intensify as odorant concentrations are increased. The relative levels of activation among glomeruli, in contrast, remain relatively stable across concentrations, suggesting that the representation of odor quality may rely on these relational activity patterns. However, the neural normalization mechanisms enabling extraction of such relational representations are unclear. Using glomerular imaging activity profiles from the rat olfactory bulb together with computational modeling, we here show that (i) global normalization preserves concentration-independent odor-quality information; (ii) perceptual similarities, as assessed behaviorally, are better predicted by normalized than by raw bulbar activity profiles; and (iii) a recurrent excitatory circuit recently described in the olfactory bulb is capable of performing such normalization. We show that global feed-forward normalization in a sensory system is behaviorally relevant, and that a center-surround neural architecture does not necessarily imply center-surround function.