Abstract
Peripheral sensory cells and the central neuronal circuits that monitor environmental changes to drive behaviors should be adapted to match the behaviorally relevant kinetics of incoming stimuli, be it the detection of sound frequencies, the speed of moving objects or local temperature changes. Detection of odorants begins with the activation of olfactory receptor neurons in the nasal cavity following inhalation of air and airborne odorants carried therein. Thus, olfactory receptor neurons are stimulated in a rhythmic and repeated fashion that is determined by the breathing or sniffing frequency that can be controlled and altered by the animal. This raises the question of how the response kinetics of olfactory receptor neurons are matched to the imposed stimulation frequency and if, vice versa, the kinetics of olfactory receptor neuron responses determine the sniffing frequency. We addressed this question by using a mouse model that lacks the K+-dependent Na+/Ca2+ exchanger 4 (NCKX4), which results in markedly slowed response termination of olfactory receptor neuron responses and hence changes the temporal response kinetics of these neurons. We monitored sniffing behaviors of freely moving wildtype and NCKX4 knockout mice while they performed olfactory Go/NoGo discrimination tasks. Knockout mice performed with similar or, surprisingly, better accuracy compared to wildtype mice, but chose, depending on the task, different odorant sampling durations depending on the behavioral demands of the odorant identification task. Similarly, depending on the demands of the behavioral task, knockout mice displayed a lower basal breathing frequency prior to odorant sampling, a possible mechanism to increase the dynamic range for changes in sniffing frequency during odorant sampling. Overall, changes in sniffing behavior between wildtype and NCKX4 knockout mice were subtle, suggesting that, at least for the particular odorant-driven task we used, slowed response termination of the odorant-induced receptor neuron response either has a limited detrimental effect on odorant-driven behavior or mice are able to compensate via an as yet unknown mechanism.
Highlights
Breathing patterns of mice are complex and mice can dynamically and quickly change their breathing rates
Active olfactory exploration is often accompanied by an increase in breathing frequency (“sniffing”), the latter having been implicated in such diverse functions as directing odorant flow to different parts of the olfactory epithelium, increasing odorant flux to the olfactory epithelium, promoting discrimination ability, discovery of new odorants, adaptive filtering of olfactory information, encoding of olfactory information in the olfactory bulb and coordination of the olfactory system with other brain areas [2,3,4,9,10,11,12,13,14,15]
The change in breathing frequency from typically 2–5 Hz at rest to 5–10 Hz during a sniff bout in rats and mice can be triggered by the presentation of a novel odorant or in anticipation of an olfactory task with the increase in breathing frequency preceding the odorant presentation by approximately one sniff cycle [2,4,16,17]
Summary
Breathing patterns of mice are complex and mice can dynamically and quickly change their breathing rates. Besides changing the respiratory rate, this changes the frequency and duration with which olfactory receptor neurons (ORNs) are exposed to odorants carried by the inhaled air. The change in breathing frequency from typically 2–5 Hz at rest to 5–10 Hz during a sniff bout in rats and mice can be triggered by the presentation of a novel odorant or in anticipation of an olfactory task with the increase in breathing frequency preceding the odorant presentation by approximately one sniff cycle [2,4,16,17]. An increase in breathing frequency is mainly achieved by shortening the exhalation phase of the sniff cycle, with the inhalation duration staying relatively constant [10]. An increase in breathing frequency is mainly achieved by shortening the exhalation phase of the sniff cycle, with the inhalation duration staying relatively constant [10]. 1–2 sniffs, or around 250 ms of odorant exposure, are sufficient to reliably distinguish odorants as shown by behavioral experiments in mice and rats [2,18,19,20]
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