Coordination of sniffing and whisking depends on the mode of interaction with the environment

Abstract

Smell and touch convey most of the information that nocturnal rodents collect in their natural environments, each via its own complex network of muscles, receptors and neurons. Being active senses, a critical factor determining the integration of their sensations relates to the degree of their coordination. While it has been known for nearly 50 years that sniffing and whisking can be coordinated, the dynamics of such coordination and its dependency on behavioral and environmental conditions are not yet understood. Here we introduce a novel non-invasive method to track sniffing along with whisking and locomotion using high-resolution video recordings of mice, during free exploration of an open arena. Active sensing parameters in each modality showed significant dependency on exploratory modes (“Outbound”, “Exploration” and “Inbound”) and locomotion speed. Surprisingly, the correlation between sniffing and whisking was often as high as the bilateral inter-whisker correlation. Both inter-whisker and inter-modal coordination switched between distinct high-correlation and low-correlation states. The fraction of time with high-correlation states was higher in the Outbound and Exploration modes compared with the Inbound mode. Overall, these data indicate that sniffing–whisking coordination is a complex dynamic process, likely to be controlled by multiple-level inter-modal coordinated loops of motor-sensory networks.

Keywords:

• active sensing
• sniffing and whisking behavior
• bi-modal sensation
• motor-sensory coordination
• non-invasive tracking
• freely moving mice

Acknowledgements

We thank Inbar Saraf-Sinik for her help in validating the nose tracking technique and Aharon Weissbrod for the help in establishing the nasal air pressure apparatus. This research was supported by the Israel Science Foundation [grant no. 1127/14]; the Minerva Foundation funded by the Federal German Ministry for Education and Research, the United States-Israel Binational Science Foundation (BSF) [grant 201143] and the NSF-BSF Brain Research EAGER program [grant number 2014906]. Ehud Ahissar incumbent of the Helen Diller Family Professorial Chair of Neurobiology. Ehud Fonio incumbent of the Tom Beck Research Fellow Chair in Physics of Complex Systems.

Disclosure statement

No potential conflict of interest was reported by the authors.

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Additional information

Funding

This research was supported by the Israel Science Foundation [grant number 1127/14]; the Minerva Foundation funded by the Federal German Ministry for Education and Research, the United States-Israel Binational Science Foundation (BSF) [grant number 201143]; the NSF-BSF Brain Research EAGER program [grant number 2014906].