The role of sniffing in shaping the primary receptor code for odors

The basic strategy by which the olfactory system encodes odor information arises from the molecular biology and anatomical projections of olfactory receptor neurons (ORNs). Each ORN expresses a single receptor protein that determines the neuron's sensitivity to particular odorants. All ORNs expressing the same receptor converge onto the same glomerulus in the olfactory bulb (OB), creating a map of receptor and odorant identity on the surface of the OB. However, a critical feature of the olfactory system is that odorant access to ORNs is controlled by the rhythmic inspiration and expiration of air through the nose (‘sniffing’), a process heavily modulated by behavioral state. To address how sniffing shapes primary receptor codes for odors, we have imaged ORN input to the OB in awake rats performing odor discrimination tasks and compared how odors are represented during different sniffing behaviors. We have found that sniffing dramatically alters both temporal and spatial patterns of ORN input to the OB. At low (resting) sniff frequencies, ORNs respond with short bursts of activity following each inhalation and encode information about all odorants present. In contrast, at higher frequencies typical of active investigation, ORNs do not burst after each sniff, show strong and rapid adaptation to continued odor presentation, and primarily encode information about changes in the olfactory environment. Thus, the ‘mode’ of odor coding can be rapidly switched simply by changing sniff frequency. These data show that significant transformations of sensory codes can be controlled by sampling behavior alone. The data also have important implications for how information is processed synaptically in the OB and beyond.