Skip to main content
SpringerLink
Log in

From Play to Aggression: High-Frequency 50-kHz Ultrasonic Vocalizations as Play and Appeasement Signals in Rats

  • Chapter
  • First Online:
Book cover Social Behavior from Rodents to Humans

Part of the book series: Current Topics in Behavioral Neurosciences ((CTBN,volume 30))

Abstract

When rats engage in playful interactions, they emit appetitive 50-kHz ultrasonic vocalizations (USVs). We investigated the role of 50-kHz USVs in the playful behavior of both juvenile and adult rats. A cohort of juvenile rats was surgically devocalized and allowed to interact with either devocalized or intact partners as juveniles and again as adults. A substantial decrease in playful motivation was seen for pairs of devocalized rats, as well as all intact rats housed with devocalized ones. In pairs in which at least one partner could vocalize, there was no difference in the number of playful interactions as compared to controls. Further investigation revealed that, within the playful episode itself, 50-kHz USVs are more likely to appear before a playful attack is launched than after, regardless of the attacking partner’s ability to vocalize, and when one partner is pinned on its back by another, it is the rat that is on top that is more likely to emit 50-kHz USVs. These findings suggest that, for juveniles, 50-kHz USVs may have a critical function in maintaining and facilitating playful motivation, but a more limited role in signaling playful actions. In adults, however, whatever the motivational role of such calling may be, the various kinds of USVs appear to serve critical communicatory functions. For instance, when pairs of adult males that are unfamiliar with one another encounter each other in a neutral arena, they play together, but if one partner is devocalized, there is a significantly higher likelihood that the interaction will escalate to become aggressive. While the relative roles of appetitive 50-kHz and aversive 22-kHz USVs in this context remain to be determined, our overall findings for play in both juveniles and adults suggest that 50-kHz USVs likely have multiple functions, with different functions being more prevalent at some ages and contexts than others.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 149.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 199.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 199.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Aldis O (1975) Play fighting. Academic Press, New York, NY

    Google Scholar 

  • Altmann SA (1962) Social behavior of anthropoid primates: analysis of recent concepts. In: Bliss EL (ed) Roots of behavior. Harper, New York, pp 277–285

    Google Scholar 

  • Anisimov VN, Herbst JA, Abramchuk AN, Latanov AV, Hahnloser RH, Vyssotski AL (2014) Reconstruction of vocal interactions in a group of small songbirds. Nat Methods 11:1135–1137

    Article  CAS  PubMed  Google Scholar 

  • Bekoff M (1975) The communication of play intention: are play signals functional? Semiotica 15:231–239

    Article  Google Scholar 

  • Berridge KC, Robinson TE (2003) Parsing reward. Trends Neurosci 26:507–513

    Article  CAS  PubMed  Google Scholar 

  • Blanchard RJ, Blanchard DC (1994) Environmental targets and sensorimotor systems in aggression and defense. In: Cooper SJ, Hendrie CA (eds) Ethology and psychopharmacology. Wiley, New York, NY, pp 133–157

    Google Scholar 

  • Brudzynski SM (2013) Ethotransmission: communication of emotional states through ultrasonic vocalization in rats. Curr Opin Neurobiol 23:310–317

    Article  CAS  PubMed  Google Scholar 

  • Burgdorf J, Knutson B, Panksepp J (2000) Anticipation of rewarding brain stimulation evokes ultrasonic vocalizations in rats. Behav Neurosci 97:320–327

    Article  Google Scholar 

  • Burgdorf J, Knutson B, Panksepp J, Ikemoto S (2001) Nucleus accumbens amphetamine microinjections unconditionally elicit 50-kHz ultrasonic vocalizations in rats. Behav Neurosci 115:940–944

    Article  CAS  PubMed  Google Scholar 

  • Burgdorf J, Wood PL, Kroes RA, Moskal JR, Panksepp J (2007) Neurobiology of 50-kHz ultrasonic vocalizations in rats: electrode mapping, lesion, and pharmacology studies. Behav Brain Res 182:274–283

    Article  PubMed  Google Scholar 

  • Burgdorf J, Kroes RA, Moskal JR, Pfaus JG, Brudzynski SM, Panksepp J (2008) Ultrasonic vocalizations of rats (Rattus norvegicus) during mating, play, and aggression: behavioral concomitants, relationship to reward, and self-administration of playback. J Comp Psychol 122:357–367

    Article  PubMed  Google Scholar 

  • Fagen R (1981) Animal play behavior. Oxford University Press, New York

    Google Scholar 

  • Graham KL (2011) Coevolutionary relationship between striatum size and social play in nonhuman primates. Am J Primat 73:314–322

    Article  Google Scholar 

  • Himmler BT, Pellis VC, Pellis SM (2013) Peering into the dynamics of social interactions: measuring play fighting in rats. J Vis Exp 71:e4288

    Google Scholar 

  • Himmler BT, Kisko TM, Euston DR, Kolb B, Pellis SM (2014) Are 50-kHz calls used as play signals in the playful interactions of rats? I. Evidence from the timing and context of their use. Behav Process 106:60–66

    Article  CAS  Google Scholar 

  • Hole GJ, Einon DF (1984) Play in rodents. In: Smith PK (ed) Play in animals and children. Blackwell, Oxford, pp 95–117

    Google Scholar 

  • Kipper S, Todt D (2002) The use of vocal signals in the social play of Barbary macaques. Primates 43:3–17

    Article  PubMed  Google Scholar 

  • Kisko TM, Euston DR, Pellis SM (2015a) Are 50-kHz calls used as play signals in the playful interactions of rats? III. The effects of devocalization on play with unfamiliar partners as juveniles and as adults. Behav Process 113:113–121

    Article  Google Scholar 

  • Kisko TM, Himmler BT, Himmler SM, Euston DR, Pellis SM (2015b) Are 50-kHz calls used as play signals in the playful interactions of rats? II. Evidence from the effects of devocalization. Behav Process 111:25–33

    Article  Google Scholar 

  • Knutson B, Burgdorf J, Panksepp J (1998) Anticipation of play elicits high-frequency ultrasonic vocalizations in young rats. J Comp Psychol 112:65–73

    Article  CAS  PubMed  Google Scholar 

  • Lehman MN, Adams DB (1976) A statistical and motivational analysis of the social behaviors of the male laboratory rat. Behaviour, LXI:3–4

    Google Scholar 

  • Lore R, Flannelly K, Farina P (1976) Ultrasounds produced by rats accompany decreases in intraspecific fighting. Aggress Behav 2:175–181

    Article  Google Scholar 

  • Lukas M, Wöhr M (2015) Endogenous vasopressin, innate anxiety, and the emission of pro-social 50-kHz ultrasonic vocalizations during social play behavior in juvenile rats. Psychoneuroendocrinology 56:35–44

    Article  CAS  PubMed  Google Scholar 

  • Moore SJ, Turnpenny P, Quinn A, Glover S, Lloyd DJ, Montgomery T, Dean JCS (2000) A clinical study of 57 children with fetal anticonvulsant syndromes. J Med Genet 37:489–497

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Neunuebel JP, Taylor AL, Arthur BJ, Egnor SR (2015) Female mice ultrasonically interact with males during courtship displays. eLife 4:e06203

    Google Scholar 

  • Palagi E (2011) Playing at every age: modalities and potential functions in non-human primates. In: Pellegrini AD (ed) Oxford handbook of the development of play. Oxford University Press, Oxford, pp 70–82

    Google Scholar 

  • Palagi E, Burghardt GM, Smuts B, Cordoni G, Dall’Olio S, Fouts HN, Řeháková-Petrů M, Siviy SM, Pellis SM (2015). Rough-and-tumble play as a window on animal communication. Biol Rev, in press

    Google Scholar 

  • Panksepp J (1981) The ontogeny of play in rats. Dev Psychobiol 14:327–332

    Article  CAS  PubMed  Google Scholar 

  • Panksepp J, Burgdorf J (2000) 50-kHz chirping (laughter?) in response to conditioned and unconditioned tickle-induced reward in rats: effects of social housing and genetic variables. Behav Brain Res 115:25–38

    Article  CAS  PubMed  Google Scholar 

  • Pellis SM (1988) Agonistic versus amicable targets of attack and defense: consequences for the origin, function and descriptive classification of play-fighting. Aggress Behav 14:85–104

    Article  Google Scholar 

  • Pellis SM, McKenna MM (1995) What do rats find rewarding in play fighting? An analysis using drug-induced non-playful partners. Behav Brain Res 68:65–73

    Article  CAS  PubMed  Google Scholar 

  • Pellis SM, Pellis VC (1983) Locomotor-rotational movements in the ontogeny and play of the laboratory rat (Rattus norvegicus). Dev Psychobiol 16:269–286

    Article  CAS  PubMed  Google Scholar 

  • Pellis SM, Pellis VC (1987) Play-fighting differs from serious fighting in both target of attack and tactics of fighting in the laboratory rat (Rattus norvegicus). Aggress Behav 13:227–242

    Article  Google Scholar 

  • Pellis SM, Pellis VC (1988) Play-fighting in the Syrian golden hamster (Mesocricetus auratus waterhouse), and its relationship to serious fighting during post-weaning development. Dev Psychobiol 21:323–337

    Article  CAS  PubMed  Google Scholar 

  • Pellis SM, Pellis VC (1990) Differential rates of attack, defense and counterattack during the developmental decrease in play fighting by male and female rats. Dev Psychobiol 23:215–231

    Article  CAS  PubMed  Google Scholar 

  • Pellis SM, Pellis VC (1998) The play fighting of rats in comparative perspective: a schema for neurobehavioral analyses. Neurosci Biobehav Rev 23:87–101

    Article  CAS  PubMed  Google Scholar 

  • Pellis SM, Pellis VC (2009) The playful brain: venturing to the limits of neuroscience. Oneworld Press, Oxford

    Google Scholar 

  • Pellis SM, Pellis VC, Himmler BT (2014) How play makes for a more adaptable brain: a comparative and neural perspective. Am J Play 7:73–98

    Google Scholar 

  • Pellis SM, Pellis VC, Foroud A (2005) Play fighting: aggression, affiliation and the development of nuanced social skills. In: Tremblay R, Hartup WW, Archer J (eds) Developmental origins of aggression. Guilford Press, New York, NY, pp 47–62

    Google Scholar 

  • Pellis SM, Pellis VC, Reinhart CJ (2010) The evolution of social play. In: Worthman C, Plotsky P, Schechter D, Cummings C (eds) Formative experiences: the interaction of caregiving, culture, and developmental psychobiology. Cambridge University Press, Cambridge, pp 404–431

    Chapter  Google Scholar 

  • Pellis SM, Field EF, Smith LK, Pellis VC (1997) Multiple differences in the play fighting of male and female rats. Implications for the causes and functions of play. Neurosci Biobehav Rev 21:105–120

    Article  CAS  PubMed  Google Scholar 

  • Raza S, Himmler BT, Himmler SM, Harker A, Kolb B, Pellis SM, Gibb R (2015) Effects of prenatal exposure to valproic acid on the development of juvenile-typical social play in rats. Behav Pharmacol 26:707–719

    Article  CAS  PubMed  Google Scholar 

  • Sadananda M, Wöhr M, Schwarting RKW (2008) Playback of 22-kHz and 50-kHz ultrasonic vocalizations induces differential c-fos expression in rat brain. Neurosci Lett 435:17–23

    Article  CAS  PubMed  Google Scholar 

  • Sales GD (1972a) Ultrasound and mating behaviour in rodents with some observations on other behavioural situations. J Zool 168:149–164

    Google Scholar 

  • Sales GD (1972b) Ultrasound and aggressive behaviour in rats and other small mammals. Anim Behav 20:88–100

    Article  CAS  PubMed  Google Scholar 

  • Schneider T, Przewłocki R (2005) Behavioral alterations in rats prenatally exposed to valproic acid: animal model of autism. Neuropsychopharmacology 30:80–89

    Article  CAS  PubMed  Google Scholar 

  • Seffer D, Rippberger H, Schwarting RKW, Wöhr M (2015) Pro-social 50-kHz ultrasonic communication in rats: post-weaning but not post-adolescent social isolation leads to social impairments—phenotypic rescue by re-socialization. Front Behav Neurosci 9:102

    Article  PubMed  PubMed Central  Google Scholar 

  • Sewell GD (1967) Ultrasound in adult rodents. Nature 215:512

    Article  CAS  PubMed  Google Scholar 

  • Siviy SM, Panksepp J (1987) Sensory modulation of juvenile play in rats. Dev Psychobiol 20:39–55

    Article  CAS  PubMed  Google Scholar 

  • Siviy SM, Panksepp J (2011) In search of the neurobiological substrates for social playfulness in mammalian brains. Neurosci Biobehav Rev 35:1821–1830

    Article  PubMed  Google Scholar 

  • Siviy SM, Harrison KA, McGregor LS (2006) Fear, risk assessment, and playfulness in the juvenile rat. Behav Neurosci 120:49–59

    Article  PubMed  Google Scholar 

  • Suomi SJ (2005) Genetic and environmental factors influencing the expression of impulsive aggression and serotonergic functioning in rhesus monkeys. In: Tremblay RE, Hartup WW, Archer J (eds) Developmental origins of aggression. Guilford Press, New York, pp 63–82

    Google Scholar 

  • Takahashi LK, Thomas DA, Barfield RJ (1983) Analysis of ultrasonic vocalizations emitted by residents during aggressive encounters among rats (Rattus norvegicus). J Comp Psychol 97:207–212

    Article  CAS  PubMed  Google Scholar 

  • Takeuchi H, Kawashima S (1986) Ultrasonic vocalizations and aggressive behavior in male rats. Physiol Behav 38:545–550

    Article  CAS  PubMed  Google Scholar 

  • Thomas DA, Takahashi LK, Barfield RJ (1983) Analysis of ultrasonic vocalizations emitted by intruders during aggressive encounters among rats (rattus norvegicus). J Comp Psychol 97:201–206

    Article  CAS  PubMed  Google Scholar 

  • Tornatzky W, Miczek KA (1994) Behavioural and autonomic responses to intermittent social stress: differential protection by clonidine and metoprolol. Psychopharmacol 116:346–356

    Article  CAS  Google Scholar 

  • Tornatzky W, Miczek KA (1995) Alcohol, anxiolytics and social stress in rats. Psychopharmacol 121:135–144

    Article  CAS  Google Scholar 

  • Trezza V, Baarendse PJ, Vanderschuren LJ (2010) The pleasures of play: pharmacological insights into social reward mechanisms. Trends Pharmacol Sci 31:463–469

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vanderschuren LJ, Trezza V (2014) What the laboratory rat has taught us about social play behavior: role in behavioral development and neural mechanisms. Curr Top Behav Neurosci 16:189–212

    Article  PubMed  Google Scholar 

  • van Hooff J (1967) The facial displays of the catarrhine monkeys and apes. In: Morris D (ed) Primate Ethology. Weidenfeld & Nicolson, London, pp 9–88

    Google Scholar 

  • van Oortmerssen GA (1971) Biological significance, genetics, and evolutionary origin of variability in behavior within and between inbred strains of mice (Mus musculus). Behav 38:1–91

    Article  Google Scholar 

  • Vivian JA, Miczek KA (1993) Diazepam and gepirone selectively attenuate either 20–32 or 32–64 kHz ultrasonic vocalizations during aggressive encounters. Psychopharmacol (Berl.) 112:66–73

    Article  CAS  Google Scholar 

  • Webber ES, Harmon KM, Beckwith TJ, Peña S, Burgdorf J, Panksepp J, Cromwell HC (2012) Selective breeding for 50 kHz ultrasonic vocalization emission produces alterations in the ontogeny and regulation of rough-and-tumble play. Behav Brain Res 229:138–144

    Article  CAS  PubMed  Google Scholar 

  • Willey AR, Spear LP (2012) Development of anticipatory 50 kHz USV production to a social stimuli in adolescent and adult male Sprague-Dawley rats. Behav Brain Res 226:613–618

    Article  PubMed  Google Scholar 

  • Willuhn I, Tose A, Wanat MJ, Hart AS, Hollon NG, Phillips PE, Schwarting RKW, Wöhr M (2014) Phasic dopamine release in the nucleus accumbens in response to pro-social 50 kHz ultrasonic vocalizations in rats. J Neurosci 34:10616–10623

    Article  PubMed  PubMed Central  Google Scholar 

  • Wilson SC (1973) The development of social behaviour in the vole (Microtus agrestis). Zool J Linn Soc 52:45–62

    Article  Google Scholar 

  • Wöhr M, Schwarting RKW (2007) Ultrasonic communication in rats: can playback of 50-kHz calls induce approach behavior? PLoS ONE 2:e1365

    Article  PubMed  PubMed Central  Google Scholar 

  • Wöhr M, Schwarting RKW (2008) Maternal care, isolation-induced infant ultrasonic calling, and their relations to adult anxiety-related behavior in the rat. Behav Neurosci 122:310

    Article  PubMed  Google Scholar 

  • Wöhr M, Schwarting RKW (2013) Affective communication in rodents: ultrasonic vocalizations as a tool for research on emotion and motivation. Cell Tissue Res 354:81–97

    Article  PubMed  Google Scholar 

  • Wöhr M, Engelhardt AK, Seffer D, Sungur AÖ, Schwarting RKW (2015) Acoustic communication in rats: effects of social experiences on ultrasonic vocalizations as socio-affective signals. Curr Topics Behav Neurosci, in press

    Google Scholar 

  • Wright JM, Gourdon JM, Clarke PB (2010) Identification of multiple call categories within the rich repertoire of adult rat 50-kHz ultrasonic vocalizations: effects of amphetamine and social context. Psychopharmacol 211:1–13

    Article  CAS  Google Scholar 

  • Yanagi A, Berman CM (2014) Body signals during social play in free-ranging Rhesus macaques (Macaca mulatta): a systematic analysis. Am J Primatol 76:168–179

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

M.W. is supported by the Deutsche Forschungsgemeinschaft (DFG WO 1732/4-1). S.M.P. is supported by the National Sciences and Engineering Research Council of Canada (NSERC—4058).

Author information

Authors and Affiliations

  1. Behavioral Neuroscience, Experimental and Biological Psychology, Philipps-University of Marburg, Gutenbergstr. 18, D-35032, Marburg, Germany

    Theresa M. Kisko & Markus Wöhr

  2. Canadian Centre for Behavioural Neuroscience, Department of Neuroscience, University of Lethbridge, Lethbridge, AB, T1K 3M4, Canada

    Vivien C. Pellis & Sergio M. Pellis

Authors
  1. Theresa M. Kisko
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Markus Wöhr
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Vivien C. Pellis
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Sergio M. Pellis
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Theresa M. Kisko .

Editor information

Editors and Affiliations

  1. Behavioral Neuroscience, Experim. and Physiological Psychology Philipps-University of Marburg, Marburg, Germany

    Markus Wöhr

  2. Dep of Psychiatry and Psychotherapy, Philipps-University of Marburg, Marburg, Germany

    Sören Krach

Rights and permissions

Reprints and permissions

Copyright information

© 2015 Springer International Publishing Switzerland

About this chapter

Cite this chapter

Kisko, T.M., Wöhr, M., Pellis, V.C., Pellis, S.M. (2015). From Play to Aggression: High-Frequency 50-kHz Ultrasonic Vocalizations as Play and Appeasement Signals in Rats. In: Wöhr, M., Krach, S. (eds) Social Behavior from Rodents to Humans. Current Topics in Behavioral Neurosciences, vol 30. Springer, Cham. https://doi.org/10.1007/7854_2015_432

Download citation

Publish with us

Policies and ethics

Search

Navigation