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Affective communication in rodents: ultrasonic vocalizations as a tool for research on emotion and motivation

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Abstract

Mice and rats emit and perceive calls in the ultrasonic range, i.e., above the human hearing threshold of about 20 kHz: so-called ultrasonic vocalizations (USV). Juvenile and adult rats emit 22-kHz USV in aversive situations, such as predator exposure and fighting or during drug withdrawal, whereas 50-kHz USV occur in appetitive situations, such as rough-and-tumble play and mating or in response to drugs of abuse, e.g., amphetamine. Aversive 22-kHz USV and appetitive 50-kHz USV serve distinct communicative functions. Whereas 22-kHz USV induce freezing behavior in the receiver, 50-kHz USV lead to social approach behavior. These opposite behavioral responses are paralleled by distinct patterns of brain activation. Freezing behavior in response to 22-kHz USV is paralleled by increased neuronal activity in brain areas regulating fear and anxiety, such as the amygdala and periaqueductal gray, whereas social approach behavior elicited by 50-kHz USV is accompanied by reduced activity levels in the amygdala but enhanced activity in the nucleus accumbens, a brain area implicated in reward processing. These opposing behavioral responses, together with distinct patterns of brain activation, particularly the bidirectional tonic activation or deactivation of the amygdala elicited by 22-kHz and 50-kHz USV, respectively, concur with a wealth of behavioral and neuroimaging studies in humans involving emotionally salient stimuli, such as fearful and happy facial expressions. Affective ultrasonic communication therefore offers a translational tool for studying the neurobiology underlying socio-affective communication. This is particularly relevant for rodent models of neurodevelopmental disorders characterized by social and communication deficits, such as autism and schizophrenia.

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Acknowledgements

The authors thank Nicole Yee for the photographs shown in Fig. 4a–c.

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  1. Behavioral Neuroscience, Experimental and Physiological Psychology, Philipps University of Marburg, Gutenbergstrasse 18, 35032, Marburg, Germany

    Markus Wöhr & Rainer K. W. Schwarting

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  1. Markus Wöhr
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Correspondence to Markus Wöhr.

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M.W. is supported by the Deutsche Forschungsgemeinschaft (DFG WO 1732/1-1).

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Wöhr, M., Schwarting, R.K.W. Affective communication in rodents: ultrasonic vocalizations as a tool for research on emotion and motivation. Cell Tissue Res 354, 81–97 (2013). https://doi.org/10.1007/s00441-013-1607-9

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  • Issue Date:

  • DOI: https://doi.org/10.1007/s00441-013-1607-9

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