Odours are transported in turbulent plumes resulting in rapid concentration fluctuations 1,2 that contain rich information about the olfactory scenery, such as odour source composition and location 2-4 . Yet whether the mammalian olfactory system has access to the underlying temporal structure to extract information about the environment remains unknown. Here, we show that 10 ms odour pulse patterns result in distinct responses in olfactory receptor neurons. In operant conditioning experiments mice discriminated temporal correlations of rapidly fluctuating odours at frequencies of up to 40 Hz. In imaging and electrophysiological recordings, such correlation information could be readily extracted from the activity of mitral and tufted cells, the output of the olfactory bulb. Furthermore, we show that temporal correlation of odour concentrations 5 reliably predicts whether odorants emerge from the same or different sources in naturalistic environments with complex airflow. Training mice on such tasks and probing with synthetic correlated stimuli at different frequencies suggests that mice can indeed use the temporal structure of odours to extract information about space. Our work thus demonstrates that the mammalian olfactory system has access to unexpectedly fast temporal features in odour stimuli. This in turn endows animals with the capacity to overcome key behavioural challenges such as odour source separation 5 , figure-ground segregation 6 and odour localisation 7 , by extracting information about space from temporal odour dynamics. Main textThe turbulent nature of air 1,2,4,8 as well as water 9,10 flow results in complex temporal fluctuations of odour concentrations that depend on the distance and direction of odour sources [1][2][3][4]8,10 . Insects are thought to use the temporal structure of odour plumes to infer e.g. odour source location 4,7,[11][12][13] or composition [13][14][15] . Mammalian olfaction on the other hand has generally been considered a slow sense. Individual sniffs are thought to be the unit of information 16 , implying that fast odour concentration changes (at sub-sniff resolution) should be inaccessible to the mammalian olfactory system. However, the neural circuitry of e.g. the mouse olfactory bulb (OB) is in principle capable of millisecond-precise action potential firing 17,18 , and is endowed with rich computational resources that could be employed to extract fine temporal information from dynamic inputs 19 . Here, we show that the mouse olfactory system has access to fast, sub-sniff temporal patterns in the odour scenery and that mice can use this information to detect high-frequency odour correlations enabling source separation. Fast odour dynamics encoded in OB inputsNormal airflow is characterized by complex, often turbulent, flow patterns and imposes a rich temporal structure on odour concentration profiles with significant power in frequencies well above typical sniff rates (Fig. 1a). To assess whether the mouse olfactory system has access to this frequency regime, we design...
The sense of smell is an essential modality for many species, in particular nocturnal and crepuscular mammals, to gather information about their environment. Olfactory cues provide information over a large range of distances, allowing behaviours ranging from simple detection and recognition of objects, to tracking trails and navigating using odour plumes from afar. In this review, we discuss the features of the natural olfactory environment and provide a brief overview of how odour information can be sampled and might be represented and processed by the mammalian olfactory system. Finally, we discuss recent behavioural approaches that address how mammals extract spatial information from the environment in three different contexts: odour trail tracking, odour plume tracking and, more general, olfactory-guided navigation. Recent technological developments have seen the spatiotemporal aspect of mammalian olfaction gain significant attention, and we discuss both the promising aspects of rapidly developing paradigms and stimulus control technologies as well as their limitations. We conclude that, while still in its beginnings, research on the odour environment offers an entry point into understanding the mechanisms how mammals extract information about space.
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