Disorder and the neural representation of complex odors: smelling in the real world

TL;DR

This paper proposes a new theory explaining how the olfactory system's architecture, characterized by disorder and diffuse receptor binding, enables animals to efficiently process complex odors and learn associations in real-world environments.

Contribution

It introduces a novel interpretation of olfactory circuit architecture, emphasizing the role of disorder and disordered projections in odor processing and learning.

Findings

Receptor diffuse binding compresses odor space while preserving similarity.

Lateral interactions densify and decorrelate responses, improving robustness.

Empirical data from Drosophila supports the theory.

Abstract

Animals smelling in the real world use a small number of receptors to sense a vast number of natural molecular mixtures, and proceed to learn arbitrary associations between odors and valences. Here, we propose a new interpretation of how the architecture of olfactory circuits is adapted to meet these immense complementary challenges. First, the diffuse binding of receptors to many molecules compresses a vast odor space into a tiny receptor space, while preserving similarity. Next, lateral interactions "densify" and decorrelate the response, enhancing robustness to noise. Finally, disordered projections from the periphery to the central brain reconfigure the densely packed information into a format suitable for flexible learning of associations and valences. We test our theory empirically using data from Drosophila. Our theory suggests that the neural processing of olfactory information differs from the other senses in its fundamental use of disorder.