Abstract
For many organisms, searching for relevant targets such as food or mates entails active, strategic sampling of the environment. Finding odorous targets may be the most ancient search problem that motile organisms evolved to solve. While chemosensory navigation has been well characterized in microorganisms and invertebrates, spatial olfaction in vertebrates is poorly understood. We have established an olfactory search assay in which freely moving mice navigate noisy concentration gradients of airborne odor. Mice solve this task using concentration gradient cues and do not require stereo olfaction for performance. During task performance, respiration and nose movement are synchronized with tens of milliseconds precision. This synchrony is present during trials and largely absent during inter-trial intervals, suggesting that sniff-synchronized nose movement is a strategic behavioral state rather than simply a constant accompaniment to fast breathing. To reveal the spatiotemporal structure of these active sensing movements, we used machine learning methods to parse motion trajectories into elementary movement motifs. Motifs fall into two clusters, which correspond to investigation and approach states. Investigation motifs lock precisely to sniffing, such that the individual motifs preferentially occur at specific phases of the sniff cycle. The allocentric structure of investigation and approach indicates an advantage to sampling both sides of the sharpest part of the odor gradient, consistent with a serial-sniff strategy for gradient sensing. This work clarifies sensorimotor strategies for mouse olfactory search and guides ongoing work into the underlying neural mechanisms.
Highlights
Sensory observations are often made in concert with movements (Ahissar &Assa, 2016; Gibson, 1966)
Our findings reveal the microstructure of olfactory search behavior in mice, identifying sensory computations and movement strategies that are shared across a broad range of species
To test olfactory search over a range of difficulties, we presented four odor patterns, defined by the ratio of odor concentration released from the two sides (100:0, 80:20, 60:40, 0:0)
Summary
2016; Gibson, 1966). During active search behavior, animals make sampling movements in order to extract relevant sensory information from the environment (Gibson, 1962; Schroeder et al, 2010). Behavioral modeling in mice further supports that inter-naris concentration comparison plays a more important role in search near the source (Liu et al, 2020) Both serial sniffing and stereo cues can guide olfactory search behavior. To better understand the sensory computations and sampling strategies for olfactory search, we designed a two-choice behavioral assay where mice use olfactory cues to locate an odor source while we monitor sniffing and movements of the head, nose, and body. Given the fundamental importance of sniffing to olfactory function, we hypothesized that mice would selectively sample the environment such that nose movement would be tightly coupled to respiration Consistent with this hypothesis, we found that mice synchronize rhythmic three-dimensional head movements with the sniff cycle during search. Our findings reveal the microstructure of olfactory search behavior in mice, identifying sensory computations and movement strategies that are shared across a broad range of species
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