Abstract
Although mice locate resources using turbulent airborne odor plumes, the stochasticity and intermittency of fluctuating plumes create challenges for interpreting odor cues in natural environments. Population activity within the olfactory bulb (OB) is thought to process this complex spatial and temporal information, but how plume dynamics impact odor representation in this early stage of the mouse olfactory system is unknown. Limitations in odor detection technology have made it difficult to measure plume fluctuations while simultaneously recording from the mouse's brain. Thus, previous studies have measured OB activity following controlled odor pulses of varying profiles or frequencies, but this approach only captures a subset of features found within olfactory plumes. Adequately sampling this feature space is difficult given a lack of knowledge regarding which features the brain extracts during exposure to natural olfactory scenes. Here we measured OB responses to naturally fluctuating odor plumes using a miniature, adapted odor sensor combined with wide-field GCaMP6f signaling from the dendrites of mitral and tufted (MT) cells imaged in olfactory glomeruli of head-fixed mice. We precisely tracked plume dynamics and imaged glomerular responses to this fluctuating input, while varying flow conditions across a range of ethologically-relevant values. We found that a consistent portion of MT activity in glomeruli follows odor concentration dynamics, and the strongest responding glomeruli are the best at following fluctuations within odor plumes. Further, the reliability and average response magnitude of glomerular populations of MT cells are affected by the flow condition in which the animal samples the plume, with the fidelity of plume following by MT cells increasing in conditions of higher flow velocity where odor dynamics result in intermittent whiffs of stronger concentration. Thus, the flow environment in which an animal encounters an odor has a large-scale impact on the temporal representation of an odor plume in the OB. Additionally, across flow conditions odor dynamics are a major driver of activity in many glomerular networks. Taken together, these data demonstrate that plume dynamics structure olfactory representations in the first stage of odor processing in the mouse olfactory system.
Highlights
Mice are adept at localizing odor sources (Gire et al, 2016; Baker et al, 2018; Liu et al, 2019; Gumaste et al, 2020), but the spatiotemporal information in olfactory environments that aids this search behavior is largely unknown
We studied the response of mitral and tufted (MT) cells in the olfactory bulb (OB) to odor concentration dynamics in awake mice as they processed natural olfactory scenes, i.e., odor plumes
Imaging was conducted in Thy1-GCaMP6f-GP5.11 mice which have fast kinetics and expression in mitral and tufted (MT) cells within the olfactory bulb (OB) (Dana et al, 2014) (Figure 2A)
Summary
Mice are adept at localizing odor sources (Gire et al, 2016; Baker et al, 2018; Liu et al, 2019; Gumaste et al, 2020), but the spatiotemporal information in olfactory environments that aids this search behavior is largely unknown. From the perspective of an olfactory searcher, these intermittent filaments create stochastic odor encounters, or whiffs, such that odor concentration dynamics fluctuate rapidly from moment to moment. Features of these complex plume dynamics contain information regarding odor source location (Murlis et al, 2000; Celani et al, 2014). An animal dependent on this search strategy would operate at a timescale far slower than that observed in mice engaged in olfactory-guided search (Gumaste et al, 2020) This suggests that rodents most likely extract information from the complex spatiotemporal dynamics of olfactory environments to support their efficient odor-guided search behavior
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