Ultrasonic signals associated with different types of social behavior of mice

Abstract

Communication plays an integral role in human social dynamics and is impaired in several neurodevelopmental disorders. Mice are used to study the neurobiology of social behavior; however, the extent to which mouse vocalizations influence social dynamics has remained elusive because it is difficult to identify the vocalizing animal among mice involved in a group interaction. By tracking the ultrasonic vocal behavior of individual mice and using an algorithm developed to group phonically similar signals, we showed that distinct patterns of vocalization emerge as male mice perform specific social actions. Mice dominating other mice were more likely to emit different vocal signals than mice avoiding social interactions. Furthermore, we showed that the patterns of vocal expression influence the behavior of the socially engaged partner but do not influence the behavior of other animals in the cage. These findings clarify the function of mouse communication by revealing a communicative ultrasonic signaling repertoire.

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Fig. 1: Dynamic behavioral repertoires.
Fig. 2: Localization of vocal signals during social behavior.
Fig. 3: Categories of vocal signals.
Fig. 4: Quantification of vocal repertoires.
Fig. 5: Examples of vocal emission during distinct behaviors.
Fig. 6: Behaviorally dependent vocal emission.
Fig. 7: Decoding behavior on the basis of vocal emission.
Fig. 8: Vocalizing alters the behavior of an engaged social partner.

Data availability

The data that support the findings of this study are available from the corresponding author upon reasonable request.

Code availability

All code that supports the findings of this study is available from the corresponding author upon reasonable request.

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Acknowledgements

We thank R. Neunuebel, A. Griffin, M. Duncan, M. Smear, R. Egnor, J. Knierim and R. Clein for helpful comments on the manuscript and the staffs of the Life Science Research Facility and the University of Delaware Information Technologies for assistance. We thank R. Egnor and G. Berman for providing software for normalizing vocal signals, D. Kelly for insightful discussions and J. Farmer and J. Quesenberry for help building lab equipment. This work was funded by the National Institutes of Health (2P20GM103653), the University of Delaware Research Foundation and Delaware’s General University Research Program.

Author information

J.P.N. designed the study. D.T.S. and M.R.W. collected and processed the data. D.T.S. and J.P.N. analyzed the data. D.T.S. and J.P.N. wrote the manuscript. M.R.W. provided feedback on the manuscript.

Correspondence to Joshua P. Neunuebel.

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The authors declare no competing interests.

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Peer review information Nature Neuroscience thanks Robert Liu and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

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Supplementary information

41593_2020_584_MOESM3_ESM.mp4

The video shows a representative example of a male mouse walking. Behaviors were extracted using JAABA. Because increasing the contrast between the white bedding and the black fur of the mouse improves our automated tracking system (Motr), the video recording was intentionally oversaturated. Each recorded male was observed walking (n = 22).

41593_2020_584_MOESM4_ESM.mp4

The video shows a representative example of two male mice circling each other. Mutual circles were observed between males in each recording (males: n = 22; recordings: n = 11).

41593_2020_584_MOESM5_ESM.mp4

The video shows a representative example of two male mice fighting. Fights were observed between males in each recording (males: n = 22; recordings: n = 11).

41593_2020_584_MOESM6_ESM.mp4

The video shows a representative example of a male mouse chasing a female. Each recorded male was observed chasing females (males: n = 22; recordings: n = 11).

41593_2020_584_MOESM7_ESM.mp4

The video shows a representative example of a male mouse running away from the other male. Fleeing was observed for each male recorded (males: n = 22; recordings: n = 11).

41593_2020_584_MOESM8_ESM.mp4

The video shows a representative example of a mouse chasing the other male. Each recorded male was observed chasing the other male (males: n = 22; recordings: n = 11).

41593_2020_584_MOESM9_ESM.mp4

The proportion of each vocal signal type within each behavior was calculated for each mouse. These values were then collapsed across mice. Average ± s.e.m.; n = 3,586 biologically independent samples analyzed.

Supplementary Information

Supplementary Figs. 1–25.

Reporting Summary

Supplementary Video 1

The video shows a representative example of a male mouse walking. Behaviors were extracted using JAABA. Because increasing the contrast between the white bedding and the black fur of the mouse improves our automated tracking system (Motr), the video recording was intentionally oversaturated. Each recorded male was observed walking (n = 22).

Supplementary Video 2

The video shows a representative example of two male mice circling each other. Mutual circles were observed between males in each recording (males: n = 22; recordings: n = 11).

Supplementary Video 3

The video shows a representative example of two male mice fighting. Fights were observed between males in each recording (males: n = 22; recordings: n = 11).

Supplementary Video 4

The video shows a representative example of a male mouse chasing a female. Each recorded male was observed chasing females (males: n = 22; recordings: n = 11).

Supplementary Video 5

The video shows a representative example of a male mouse running away from the other male. Fleeing was observed for each male recorded (males: n = 22; recordings: n = 11).

Supplementary Video 6

The video shows a representative example of a mouse chasing the other male. Each recorded male was observed chasing the other male (males: n = 22; recordings: n = 11).

Supplementary Video 7

The proportion of each vocal signal type within each behavior was calculated for each mouse. These values were then collapsed across mice. Average ± s.e.m.; n = 3,586 biologically independent samples analyzed.

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Sangiamo, D.T., Warren, M.R. & Neunuebel, J.P. Ultrasonic signals associated with different types of social behavior of mice. Nat Neurosci 23, 411–422 (2020). https://doi.org/10.1038/s41593-020-0584-z

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