Fast odour dynamics are encoded in the olfactory system and guide behaviour

Abstract

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...

Biological Roles of Lipocalins in Chemical Communication, Reproduction, and Regulation of Microbiota

“…The signals detected by VNO are then processed in the AOB which maintain stereotypic sensory representations for broad types of stimuli, providing a substrate for relevant behaviours ( Bansal et al, 2021 ). The responses of VNO and MOE are fast because odours are transported in turbulent plumes from the sites of origin and for example mice are able to detect these dynamically changing odours with a frequency of up to 40Hz ( Ackels et al, 2021 ). The main message from this study is that volatiles, released from MUPs in the urine marks, must directly interact with chemosensory receptors and not via nasal volatile-binding proteins that would slow down this interaction.…”

Principles of odor coding in vertebrates and artificial chemosensory systems

“…9) it appears to be coded in the first spike latencies (468), and those latencies obviously depend on the dynamics of odor-induced ORN activities. In a very recent paper, Ackels and colleagues (473) have shown that the temporal resolution of the olfactory system of mice is even higher than generally thought. They have demonstrated that 10-ms odor pulse patterns elicit distinct responses in olfactory receptor neurons.…”

Sparse connectivity for MAP inference in linear models using sister mitral cells

“…The prior p(x) encodes the animal's background knowledge about the presence of odours in the environment. We assume that the animal makes the simplifying assumptions that molecules appear independently of each other (but see [15,16]), and that the marginal probability distribution for each molecule, p(x i ), has the same form.…”

“…We can, therefore, replace λ i in Eq (10a) with the right hand side of Eq (16), and, so long as the sister mitral cells evolve according to Eq (11), our model will implement MAP inference. Eq (14) tells us only that the weights of the sister mitral cells add up to A ij , but besides that we have complete freedom in choosing them.…”