Primary sensory neurons form the interface between world and brain. Their function is well-understood during passive stimulation but, under natural behaving conditions, sense organs are under active, motor control. In an attempt to predict primary neuron firing under natural conditions of sensorimotor integration, we recorded from primary mechanosensory neurons of awake, head-fixed mice as they explored a pole with their whiskers, and simultaneously measured both whisker motion and forces with high-speed videography. Using Generalised Linear Models, we found that primary neuron responses were poorly predicted by whisker angle, but well-predicted by rotational forces acting on the whisker: both during touch and free-air whisker motion. These results are in apparent contrast to previous studies of passive stimulation, but could be reconciled by differences in the kinematics-force relationship between active and passive conditions. Thus, simple statistical models can predict rich neural activity elicited by natural, exploratory behaviour involving active movement of sense organs.DOI: http://dx.doi.org/10.7554/eLife.10696.001

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...

Communication in the nervous system occurs by spikes: the timing precision with which spikes are fired is a fundamental limit on neural information processing. In sensory systems, spike-timing precision is constrained by first-order neurons. We found that spike-timing precision of trigeminal primary afferents in rats and mice is limited both by stimulus speed and by electrophysiological sampling rate. High-speed video of behaving mice revealed whisker velocities of at least 17,000°/s, so we delivered an ultrafast "ping" (Ͼ50,000°/s) to single whiskers and sampled primary afferent activity at 500 kHz. Median spike jitter was 17.4 s; 29% of neurons had spike jitter Ͻ 10 s. These results indicate that the input stage of the trigeminal pathway has extraordinary spike-timing precision and very high potential information capacity. This timing precision ranks among the highest in biology.