Temporal organization of odor responses in the human olfactory bulb

When sampling odors, humans typically take a single long sniff. This differs from other mammals, who typically sample odors through rapid repetitive sniffing bouts. Decades of work has established that rapid sniffing rhythms underlie the organizational principles of odor coding in the brain, with sniff speed clocking the temporal resolution of odor responses in the olfactory bulb. In the absence of rapid sniffing, how are odor responses organized in the human olfactory system? The divergence of human sniffing behavior from other mammals could have profound implications for the underlying neural mechanisms of odor coding, yet this question remains unexplored. Since most mammals sniff at rates centered around the theta frequency (2–12Hz), we hypothesized that the human olfactory bulb might exploit a theta-range neural oscillation to set the pace of odor coding in the system. If true, a single long human sniff should produce a phase-aligned theta oscillation in the olfactory bulb, responsive to behavioral changes in sniffing and related to higher-frequency bulb oscillations that support odor processing. Whether theta oscillations exist in the human olfactory bulb is unknown. Here, we collected high-precision neural recordings from the human olfactory bulb in healthy volunteers, allowing for quantification of neuronal oscillations at the single-trial level. We show that initiation of a sniff elicits and temporarily aligns theta oscillations in the human olfactory bulb. We further found that sniff-induced theta oscillations organize the timing and amplitude of responses to odor, suggesting that despite the lack of rapid sniffing bouts in humans, the system has preserved a similarly-timed unit of olfactory processing.