Respiration-Locking of Olfactory Receptor and Projection Neurons in the Mouse Olfactory Bulb and Its Modulation by Brain State

Abstract

For sensory systems of the brain, the dynamics of an animal’s own sampling behaviour has a direct consequence on ensuing computations. This is particularly the case for mammalian olfaction, where a rhythmic flow of air over the nasal epithelium entrains activity in olfactory system neurons in a phenomenon known as sniff-locking. Parameters of sniffing can, however, change drastically with brain states. Coupled to the fact that different observation methods have different kinetics, consensus on the sniff-locking properties of neurons is lacking. To address this, we investigated the sniff-related activity of olfactory sensory neurons (OSNs), as well as the principal neurons of the olfactory bulb (OB), using 2-photon calcium imaging and intracellular whole-cell patch-clamp recordings in vivo, both in anaesthetised and awake mice. Our results indicate that OSNs and OB output neurons lock robustly to the sniff rhythm, but with a slight temporal shift between behavioural states. We also observed a slight delay between methods. Further, the divergent sniff-locking by TCs and MCs in the absence of odour can be used to determine the cell type reliably using a simple linear classifier. Using this classification on datasets where morphological identification is unavailable, we find that MCs use a wider range of temporal shifts to encode odours than previously thought, while TCs have a constrained timing of activation due to an early-onset hyperpolarisation. We conclude that the sniff rhythm serves as a fundamental rhythm but its impact on odour encoding depends on cell type, and this difference is accentuated in awake mice.