Abstract
Adult mice emit many ultrasonic vocalizations (USVs) during social interaction tasks, but only a few studies have yet reported USVs in stressed adult mice. Our aim was to study which experimental conditions favor USV emission during behaviors associated with different emotional states. As USVs likely mediate social communication, we hypothesized that temporary social isolation followed by exposure to a novel social congener would promote USV emission. USVs were recorded in three different behavioral paradigms: restraint, free moving in a new environment, and during a social interaction task. We compared USV emission, with or without the presence of a social congener, in animals socially isolated during different periods (0, 6 or 21 days). Social isolation decreased the number of USVs during free moving, whereas it increased during restraint. During the social interaction task, animals produced high-frequency USVs (median: 72.6 kHz, 25–75% range: 67.6–78.2 kHz), especially when the social partner was active and social motivation was high. During restraint, presence of a social congener increased the call rate of low-frequency USVs (median: 52.4 kHz, 25–75% range: 44.8–56.5 kHz). USV frequency followed two unimodal distributions that distinguished low-frequency USVs (≤ 60 kHz) mainly emitted during free-moving (90.9% of total USVs) and restraint (93.1%) conditions, from high-frequency USVs (> 60 kHz) mainly emitted during the social interaction task (85.1% of total USVs). The present study confirms that USV call rate and frequency depend on behavioral states, and provides evidence that the presence of a congener promotes ultrasonic vocalizations in restrained adult mice.
Article Highlights
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Social isolation increased restraint-induced USVs, but decreased USVs induced by free-exploration of a novel environment.
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Social contact increased call rates of high-frequency USVs (> 60 kHz), especially when social partner was active and social motivation was high.
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Restraint induced low-frequency USVs (≤ 60 kHz) in mice, especially when a social congener was in the vicinity.
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References
Bartal I, Decety J, Mason P (2011) Empathy and pro-social behavior in rats. Science 334:1427–1430. https://doi.org/10.1126/science.1210789
Blanchard RJ, Flannelly KJ, Blanchard DC (1986) norvegicus. J Comp Psychol 100:101–107
Blanchard RJ, Blanchard DC, Agullana R, Weiss SM (1991) Twenty-two kHz alarm cries to presentation of a predator, by laboratory rats living in visible burrow systems. Physiol Behav 50:967–972
Borta A, Wöhr M, Schwarting RKW (2006) Rat ultrasonic vocalization in aversively motivated situations and the role of individual differences in anxiety-related behavior. Behav Brain Res 166:271–280. https://doi.org/10.1016/j.bbr.2005.08.009
Brudzynski SM (2013) Ethotransmission: communication of emotional states through ultrasonic vocalization in rats. Curr Opin Neurobiol 23:310–317. https://doi.org/10.1016/j.conb.2013.01.014
Brudzynski SM, Ociepa D (1992) Ultrasonic vocalization of laboratory rats in response to handling and touch. Physiol Behav 52:655–660
Chabout J, Serreau P, Ey E et al (2012) Adult male mice emit context-specific ultrasonic vocalizations that are modulated by prior isolation or group rearing environment. PLoS ONE ONE 7:e29401. https://doi.org/10.1371/journal.pone.0029401
Chabout J, Cressant A, Hu X et al (2013) Making choice between competing rewards in uncertain vs. safe social environment: role of neuronal nicotinic receptors of acetylcholine. Front Hum Neurosci 7:468. https://doi.org/10.3389/fnhum.2013.00468
Chabout J, Sarkar A, Dunson DB, Jarvis ED (2015) Male mice song syntax depends on social contexts and influences female preferences. Front Behav Neurosci. https://doi.org/10.3389/fnbeh.2015.00076
Chauveau F, Lange MD, Jungling K et al (2012) Prevention of stress-impaired fear extinction through neuropeptide s action in the lateral amygdala. Neuropsychopharmacology 37:1588–1599. https://doi.org/10.1038/npp.2012.3
Cuomo V, Cagiano R, De Salvia MA et al (1988) Ultrasonic vocalization in response to unavoidable aversive stimuli in rats: effects of benzodiazepines. Life Sci 43:485–491
Ey E, Torquet N, Le Sourd A-M et al (2013) The autism ProSAP1/Shank2 mouse model displays quantitative and structural abnormalities in ultrasonic vocalisations. Behav Brain Res 256:677–689. https://doi.org/10.1016/j.bbr.2013.08.031
Faure A, Pittaras E, Nosjean A et al (2017) Social behaviors and acoustic vocalizations in different strains of mice. Behav Brain Res 320:383–390. https://doi.org/10.1016/j.bbr.2016.11.003
Grimsley JMS, Monaghan JJM, Wenstrup JJ (2011) Development of social vocalizations in mice. PLoS ONE ONE 6:e17460. https://doi.org/10.1371/journal.pone.0017460
Grimsley JMS, Sheth S, Vallabh N et al (2016) Contextual modulation of vocal behavior in mouse: newly identified 12 kHz “Mid-Frequency” vocalization emitted during restraint. Front Behav Neurosci 10:38. https://doi.org/10.3389/fnbeh.2016.00038
Hegoburu C, Sevelinges Y, Thevenet M et al (2009) Differential dynamics of amino acid release in the amygdala and olfactory cortex during odor fear acquisition as revealed with simultaneous high temporal resolution microdialysis. Learn Mem 16:687–697
Holy TE, Guo Z (2005) Ultrasonic songs of male mice. PLoS Biol 3:e386. https://doi.org/10.1371/journal.pbio.0030386
Kaltwasser MT (1991) Acoustic startle induced ultrasonic vocalization in the rat: a novel animal model of anxiety? Behav Brain Res 43:133–137
Kurejova M, Nattenmüller U, Hildebrandt U et al (2010) An improved behavioural assay demonstrates that ultrasound vocalizations constitute a reliable indicator of chronic cancer pain and neuropathic pain. Mol Pain 6:18. https://doi.org/10.1186/1744-8069-6-18
Laloux C, Mairesse J, Van Camp G et al (2012) Anxiety-like behaviour and associated neurochemical and endocrinological alterations in male pups exposed to prenatal stress. Psychoneuroendocrinology 37:1646–1658. https://doi.org/10.1016/j.psyneuen.2012.02.010
Litvin Y, Blanchard DC, Blanchard RJ (2007) Rat 22 kHz ultrasonic vocalizations as alarm cries. Behav Brain Res 182:166–172. https://doi.org/10.1016/j.bbr.2006.11.038
Lumley LA, Sipos ML, Charles RC et al (1999) Social stress effects on territorial marking and ultrasonic vocalizations in mice. Physiol Behav 67:769–775
Mun H-S, Lipina TV, Roder JC (2015) Ultrasonic vocalizations in mice during exploratory behavior are context-dependent. Front Behav Neurosci 9:316. https://doi.org/10.3389/fnbeh.2015.00316
Naito H, Nakamura A, Inoue M, Suzuki Y (2003) Effect of anxiolytic drugs on air-puff-elicited ultrasonic vocalization in adult rats. Exp Anim 52:409–414
Nosjean A, Cressant A, de Chaumont F et al (2015) Acute stress in adulthood impoverishes social choices and triggers aggressiveness in preclinical models. Front Behav Neurosci. https://doi.org/10.3389/fnbeh.2014.00447
Panksepp JB, Lahvis GP (2007) Social reward among juvenile mice. Genes Brain Behav 6:661–671. https://doi.org/10.1111/j.1601-183X.2006.00295.x
Portfors CV, Perkel DJ (2014) The role of ultrasonic vocalizations in mouse communication. Curr Opin Neurobiol 28:115–120. https://doi.org/10.1016/j.conb.2014.07.002
Saito Y, Yuki S, Seki Y et al (2016) Cognitive bias in rats evoked by ultrasonic vocalizations suggests emotional contagion. Behav Processes. https://doi.org/10.1016/j.beproc.2016.08.005
Sánchez C (2003) Stress-induced vocalisation in adult animals. A valid model of anxiety? Eur J Pharmacol 463:133–143
Scattoni ML, Crawley J, Ricceri L (2009) Ultrasonic vocalizations: a tool for behavioural phenotyping of mouse models of neurodevelopmental disorders. Neurosci Biobehav Rev 33:508–515. https://doi.org/10.1016/j.neubiorev.2008.08.003
Scattoni ML, Ricceri L, Crawley JN (2011) Unusual repertoire of vocalizations in adult BTBR T+tf/J mice during three types of social encounters. Genes Brain Behav 10:44–56. https://doi.org/10.1111/j.1601-183X.2010.00623.x
Seffer D, Schwarting RKW, Wöhr M (2014) Pro-social ultrasonic communication in rats: insights from playback studies. J Neurosci Methods 234:73–81. https://doi.org/10.1016/j.jneumeth.2014.01.023
Simola N (2015) Rat ultrasonic vocalizations and behavioral neuropharmacology: from the screening of drugs to the study of disease. Curr Neuropharmacol 13:164–179
Simola N, Granon S (2018) Ultrasonic vocalizations as a tool in studying emotional states in rodent models of social behavior and brain disease. Neuropharmacology. https://doi.org/10.1016/j.neuropharm.2018.11.008
Tonoue T, Ashida Y, Makino H, Hata H (1986) Inhibition of shock-elicited ultrasonic vocalization by opioid peptides in the rat: a psychotropic effect. Psychoneuroendocrinology 11:177–184
Vivian JA, Miczek KA (1993a) Diazepam and gepirone selectively attenuate either 20–32 or 32–64 kHz ultrasonic vocalizations during aggressive encounters. Psychopharmacology 112:66–73
Vivian JA, Miczek KA (1993b) Morphine attenuates ultrasonic vocalization during agonistic encounters in adult male rats. Psychopharmacology 111:367–375
Acknowledgements
We thank Ophélie Joly and Lorie Carassini for participating in the animal experiment during internships in the laboratory. This work benefited from the animal platform facility at Neuro-PSI (Orsay, France). The manuscript was corrected by a native English proofreader (Brandon Loveall; contact@improvence.net).
Funding
This research was supported by the Service de Santé des Armées, by the CNRS, Université Paris Sud, and by a grant to FC (PEA 13co709) from the Direction Générale de l’Armement (DGA, France).
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The authors declare that there is no conflict of interest. This research received no specific grant from any funding agency in the commercial sector.
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All applicable international and/or institutional guidelines for the care and use of animals were followed. Experiments were conducted in accordance with the recommendations for animal experiments issued by the European Community Council guidelines (directive 2010/63/EU). The protocol was approved beforehand by an independent ethical board (reference 2015-04).
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Lefebvre, E., Granon, S. & Chauveau, F. Social context increases ultrasonic vocalizations during restraint in adult mice. Anim Cogn 23, 351–359 (2020). https://doi.org/10.1007/s10071-019-01338-2
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DOI: https://doi.org/10.1007/s10071-019-01338-2