Nonlinear sensory integration drives configural olfactory representations

Abstract

Natural environments are composed of complex stimulus mixtures that can be perceived either as combinations of known components (elemental coding) or acquire entirely new qualities (configural coding). While configural representation is traditionally viewed as a high-order emergent property of cortical processing, the underlying circuit mechanisms remain elusive. Employing C. elegans, we demonstrate that the neural foundations of configural representation can be established already at the sensory periphery. For most mixtures, single neuron responses arise through linear integration of the individual components. However, for a subset of mixtures, a small number of sensory neurons exhibit strong nonlinear integration, including NAND/XOR-like logic-gates computations. These nonlinear integrations collectively generate configural population codes. We present a novel quantitative predictor of configural representation and demonstrate that mixtures classified as configural induce emergent synergistic attraction and may lead to violations of rational choice behavior. Together, our findings identify single-neuron nonlinearities as a mechanistic link between sensory circuit dynamics and complex perceptual and decision-making outcomes.