Abstract

Understanding how the brain transforms peripheral sensory inputs into higher-level representations, and how these contribute to perceptual and behavioral performance, is a central question in sensory neuroscience. However, in human olfaction, the temporal evolution of neural odor codes and their functional significance remain poorly characterized, especially at early stages. To address which odor features define early neural responses and how these relate to olfactory function, we recorded EEG from male and female participants as they inhaled a diverse panel of odors. The same cohort also completed standardized tests of odor detection, discrimination, and identification, along with questionnaires. Time- and frequency-resolved decoding and representational similarity analysis revealed that early theta activity (starting at 80 ms, peaking at 370 ms) encodes low-level physicochemical properties of odor molecules. Critically, the fidelity of this early-theta coding to odor physicochemical properties selectively correlated with participants’ trait-level odor discrimination ability, but not with other olfactory measures. In contrast, delta-band representations of pleasantness emerged later (from 720 ms), linked only to trait-level odor affective reactivity, as measured by questionnaires. These results suggest that earlier theta-band representations reflect a distinct functional role from the later-emerging delta-band activity and are associated with olfactory performance. Extending these findings, separate EEG recordings during a task involving odor discrimination showed that early-theta decoding accuracy was significantly higher on correct than incorrect trials, indicating that theta-band coding accounts for trial-by-trial performance fluctuations. Collectively, our study demonstrates that early theta-band representations of low-level odor features—prior to perceptual representations—are already functionally relevant to odor-guided behavior.

Significance statement The olfactory system rapidly transforms the physicochemical characteristics of odor molecules into perceptually and behaviorally relevant signals. However, the nature of neural representations at each processing stage—and whether these representations influence olfactory performance—remains poorly understood. Using electroencephalography during odor stimulation, we show that individuals with superior odor discrimination ability more precisely encode physicochemical odor features within first 300 milliseconds. Neural coding in the same time window also predicts trial-by-trial performance in a task involving odor discrimination. In contrast, later brain activity reflects perceived pleasantness and does not relate to olfactory ability. These findings suggest that early-stage neural representation of low-level odor features plays a unique role in shaping odor-guided behavior in humans, distinct from representations associated with pleasantness.