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Structure of Perceptual Odor Coding in the Human Brain: Neural Basis, Dimensionality, and Subjectivity

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Our sense of smell, or olfaction, is one of our most evolutionarily ancient senses. In vertebrates, olfaction plays a crucial role in many functions, such as detecting and evaluating food, avoiding predators, regulating appetite, spatial navigation, and selecting mating partners. In addition, the olfactory system is highly dynamic and exhibits experience-dependent plasticity, reflecting a high degree of subjectivity across individuals. However, despite its crucial functions and intriguing properties, we do not clearly understand the neural basis of olfactory perception. Previous research has shown that odorous molecules activate patterns of neural activity distributed throughout the olfactory cortices, but how these patterns correspond to our subjective perception of odors remains to be elucidated.Here we address this gap by conducting a precision imaging study of olfactory perception. We collected neuroimaging data from three individuals as they smelled 160 odors over 18 hours per subject. We examined odor coding in several olfactory brain areas, namely, the frontal piriform cortex (PirF), temporal piriform cortex (PirT), amygdala (AMY), and orbitofrontal cortex (OFC). We observed that OFC plays a crucial role in representing the precise fine-grained identity of odors, while the piriform cortex (PirC) and amygdala capture coarse and general odor features. Additionally, we could predict how the brain would respond to novel odors by using perceptual encoding models. We found that the perceptual spaces encoded by the brain increase in dimensionality from the piriform cortex (PirC) to OFC. Further, while lower-order dimensions are consistent across individuals, higher-order dimensions are unique to each individual. These findings offer valuable new insights into the cortical mechanisms that encode odors and suggest that the subjective perception of odors is rooted in the OFC.

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