The olfactory bulb receives rich glutamatergic projections from the piriform cortex. However, the dynamics and importance of these feedback signals remain unknown. Here, we use multiphoton calcium imaging to monitor cortical feedback in the olfactory bulb of awake mice and further probe its impact on the bulb output. Responses of feedback boutons were sparse, odor specific, and often outlasted stimuli by several seconds. Odor presentation either enhanced or suppressed the activity of boutons. However, any given bouton responded with stereotypic polarity across multiple odors, preferring either enhancement or suppression. Feedback representations were locally diverse and differed in dynamics across bulb layers. Inactivation of piriform cortex increased odor responsiveness and pairwise similarity of mitral cells but had little impact on tufted cells. We propose that cortical feedback differentially impacts these two output channels of the bulb by specifically decorrelating mitral cell responses to enable odor separation.

The elementary stimulus features encoded by the olfactory system remain poorly understood. We examined the relationship between 1,666 physical-chemical descriptors of odors and the activity of olfactory bulb inputs and outputs in awake mice. Glomerular and mitral/tufted cell (MTC) responses were sparse and locally heterogeneous, with only weak dependence of their positions on physical-chemical properties. Odor features represented by ensembles of MTCs were overlapping but distinct from those represented in glomeruli, consistent with extensive interplay between feedforward and feedback inputs to the bulb. This reformatting was well-described as a rotation in odor space. The physical-chemical descriptors accounted for a small fraction in response variance, and the similarity of odors in physical-chemical space was a poor predictor of similarity in neuronal representations. Our results suggest that commonly used physical-chemical properties are not systematically represented in bulbar activity and encourage further search for better descriptors of odor space.

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Sensory systems rely on statistical regularities in the experienced inputs to either group disparate stimuli, or parse them into separate categories. While considerable progress has been made in understanding invariant object recognition in the visual system, how this is implemented by olfactory neural circuits remains an open question. The current leading model states that odor identity is primarily computed in the piriform cortex, drawing from mitral cell (MC) input. Surprisingly, the role of tufted cells (TC), the other principal cell-type of the olfactory bulb (OB) in decoding odor identity, and their dependence on cortical feedback, has been overlooked. Tufted cells preferentially project to the anterior olfactory nucleus (AON) and olfactory striatum, while mitral cells strongly innervate the piriform cortex (PC). Here we show that classifiers based on the population activity of tufted cells successfully decode both odor identity and intensity across a large concentration range. In these computations, tufted cells substantially outperform mitral cells, and are largely unaffected by silencing of cortical feedback. Further, cortical feedback from AON controls preferentially the gain of tufted cell odor representations, while PC feedback specifically restructures mitral cell responses, matching biases in feedforward connectivity. Leveraging cell-type specific analyses, we identify a non-canonical feedforward pathway for odor recognition and discrimination mediated by the tufted cells, and propose that OB target areas, other than the piriform cortex, such as AON and olfactory striatum, are well-positioned to compute odor identity.

The elementary stimulus features encoded by the olfactory system remain poorly understood. We All rights reserved. No reuse allowed without permission.was not peer-reviewed) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity.