Behavioral Relevance of Early Neural Coding of Low-Level Odor Features in Humans.

Understanding how the brain transforms peripheral sensory inputs into higher-level representations, and how these contribute to perception 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 diverse odors. Participants 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 encodes low-level physicochemical properties of odor molecules, with encoding peaking at 370 ms. 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 (peaking at 980 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.