Rodent ultrasonic vocal interaction resolved with millimeter precision using hybrid beamforming

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Abstract

Ultrasonic vocalizations (USVs) fulfill an important role in communication and navigation in many species. Because of their social and affective significance, rodent USVs are increasingly used as a behavioral measure in neurodevelopmental and neurolinguistic research. Reliably attributing USVs to their emitter during close interactions has emerged as a difficult, key challenge. If addressed, all subsequent analyses gain substantial confidence. We present a hybrid ultrasonic tracking system, HyVL, that synergistically integrates a high-resolution acoustic camera with high-quality ultrasonic microphones. HyVL is the first to achieve millimeter precision (~3.4-4.8mm, 91% assigned) in localizing USVs, ~3x better than other systems, approaching the physical limits (mouse snout ~ 10mm). We analyze mouse courtship interactions and demonstrate that males and females vocalize in starkly different relative spatial positions, and that the fraction of female vocalizations has likely been overestimated previously due to imprecise localization. Further, we find that when two male mice interact with one female, one of the males takes a dominant role in the interaction both in terms of the vocalization rate and the location relative to the female. HyVL substantially improves the precision with which social communication between rodents can be studied. It is also affordable, open-source, easy to set up, can be integrated with existing setups, and reduces the required number of experiments and animals.

Data availability

All code necessary to implement the HyVL system has been deposited at https://github.com/benglitz/HyVL and https://doi.org/10.34973/7kgc-ta72.All data has been made available at https://doi.org/10.34973/7kgc-ta72.

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Max L Sterling

Donders Institute for Brain, Cognition and Behaviour, Radboud University Nijmegen, Nijmegen, Netherlands

Competing interests
The authors declare that no competing interests exist.
Ruben Teunisse

Donders Institute for Brain, Cognition and Behaviour, Radboud University Nijmegen, Nijmegen, Netherlands

Competing interests
The authors declare that no competing interests exist.
Bernhard Englitz

Donders Institute for Brain, Cognition and Behaviour, Radboud University Nijmegen, Nijmegen, Netherlands

For correspondence
englitz@science.ru.nl

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0001-9106-0356

Funding

DCN Internal Grant, Noldus IT

Bernhard Englitz

NWO VIDI grant (016.VIDI.189.052)

Bernhard Englitz

Technology Hotel Grant, ZonMW (40-43500-98-4141)

Bernhard Englitz

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Ethics

Animal experimentation: All of the animals and experimental procedures were conducted according to the guidelines of the Animal Welfare Body of the Central Animal Facility at the Radboud University. The protocol was approved by the Dutch National Committee CCD (Permit Number: 2017-0041).

Copyright

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.