Acoustic Communication in Rats: Effects of Social Experiences on Ultrasonic Vocalizations as Socio-affective Signals

  • Markus Wöhr
  • K. Alexander Engelhardt
  • Dominik Seffer
  • A. Özge Sungur
  • Rainer K. W. Schwarting
Chapter
Part of the Current Topics in Behavioral Neurosciences book series (CTBN, volume 30)

Abstract

Ultrasonic vocalizations (USV) serve important communicative functions as socio-affective signals in rats. In aversive situations, such as inter-male aggression and predator exposure, 22-kHz USV are emitted. They likely function as appeasement signals during fighting and/or as alarm calls to warn conspecifics. In appetitive situations, 50-kHz USV are uttered, most notably during social interactions, such as rough-and-tumble play and mating. It is believed that they fulfill an affiliative function as social contact calls. Social experiences or their lack, such as social isolation, can have profound impact on the emission of 22- and 50-kHz USV by the sender in later life, albeit direction and strength of observed effects vary, with time point of occurrence and duration being critical determinants. Little, however, is known about how social experiences affect the behavioral responses evoked by 22- and 50-kHz USV in the recipient. By means of our 50-kHz USV radial maze playback paradigm, we recently showed that the behavioral response elicited in the recipient is affected by post-weaning social isolation. Rats exposed to four weeks of isolation during the rough-and-tumble play period did not display social approach behavior toward 50-kHz USV but some signs of social avoidance. We further found that physical environmental enrichment providing minimal opportunities for social interactions has similar detrimental effects. Together, this indicates that social experiences can affect socio-affective communication in rodents, both at the level of sender and recipient. Deficits seen following post-weaning social isolation or physical environmental enrichment might be useful to model aspects of neurodevelopmental disorders characterized by social and communication deficits, such as autism and schizophrenia.

Keywords

Ultrasonic communication Social behavior Social isolation Animal model Autism Schizophrenia Intense world syndrome 

Notes

Acknowledgments

The authors wish to thank J.C. Brenes for the pictures depicted in Fig. 3. M.W. is supported by the Deutsche Forschungsgemeinschaft (DFG WO 1732/4-1).

References

  1. Barfield RJ, Thomas DA (1986) The role of ultrasonic vocalizations in the regulation of reproduction in rats. Ann N Y Acad Sci 474:33–43CrossRefPubMedGoogle Scholar
  2. Bassi SG, Nobre NJ, Carvalho MC, Brandao ML (2007) Substance P injected into the dorsal periaqueductal gray causes anxiogenic effects similar to long-term isolation as assessed by ultrasound vocalizations measurements. Behav Brain Res 182:301–307CrossRefPubMedGoogle Scholar
  3. 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 50:967–972CrossRefPubMedGoogle Scholar
  4. Brenes JC, Lackinger M, Höglinger GU, Schratt G, Schwarting RKW, Wöhr M (2015) Differential effects of social and physical environmental enrichment on brain plasticity, cognition, and ultrasonic communication in rats. J Comp Neurol (in press)Google Scholar
  5. Brudzynski SM (2013) Ethotransmission: communication of emotional states through ultrasonic vocalization in rats. Curr Opin Neurobiol 23:310–317CrossRefPubMedGoogle Scholar
  6. Brudzynski SM, Ociepa D (1992) Ultrasonic vocalization of laboratory rats in response to handling and touch. Physiol Behav 52:655–660CrossRefPubMedGoogle Scholar
  7. Brudzynski SM, Pniak A (2002) Social contacts and production of 50-kHz short ultrasonic calls in adult rats. J Comp Psychol 116:73–82CrossRefPubMedGoogle Scholar
  8. Burgdorf J, Panksepp J (2001) Tickling induces reward in adolescent rats. Physiol Behav 72:167–173CrossRefPubMedGoogle Scholar
  9. 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 122:357–367CrossRefPubMedGoogle Scholar
  10. Cloutier S, Baker C, Wahl K, Panksepp J, Newberry RC (2013) Playful handling as social enrichment for individually- and group-housed laboratory rats. Appl Anim Behav Sci 143:85–95CrossRefGoogle Scholar
  11. Favre MR, La Mendola D, Meystre J, Christodoulou D, Cochrane MJ, Markram H, Markram K (2015) Predictable enriched environment prevents development of hyper-emotionality in the VPA rat model of autism. Front Neurosci 9:127CrossRefPubMedPubMedCentralGoogle Scholar
  12. Fone K, Porkess V (2008) Behavioral and neurochemical effects of post-weaning social isolation in rodents—Relevance to developmental neuropsychiatric disorders. Neurosci Biobehav Rev 32:1087–1102CrossRefPubMedGoogle Scholar
  13. Gruendel AD, Arnold WJ (1974) Influence of preadolescent experiential factors on the development of sexual behavior in albino rats. J Comp Physiol Psych 1:172–178CrossRefGoogle Scholar
  14. Hamed A, Jaroszewski T, Maciejak P, Szyndler J, Lehner M, Kamecka I, Olczak M, Kuzinska U, Taracha E, Płaźnik A (2009) The effects of buspirone and diazepam on aversive context- and social isolation-induced ultrasonic vocalization. Physiol Behav 98:474–480CrossRefPubMedGoogle Scholar
  15. Hamed A, Szyndler J, Taracha E, Turzyńska D, Sobolewska A, Lehner M, Krząścik P, Daszczuk P (2015) κ-opioid receptor as a key mediator in the regulation of appetitive 50-kHz ultrasonic vocalizations. Psychopharmacology 232:1941–1955CrossRefPubMedGoogle Scholar
  16. Hunter AS (2015) Impaired extinction of fear conditioning after REM deprivation is magnified by rearing in an enriched environment. Neurobiol Learn Mem 122:11–18CrossRefPubMedGoogle Scholar
  17. Inagaki H, Mori Y (2013) The critical point at which post-weaning individual housing conditions affect the emission of 22-kHz calls in male rats. J Vet Med Sci 75:527–529CrossRefPubMedGoogle Scholar
  18. Inagaki H, Kuwahara M, Kikusui T, Tsubone H (2005) The influence of social environmental condition on the production of stress-induced 22 kHz calls in adult male Wistar rats. Physiol Behav 84:17–22CrossRefPubMedGoogle Scholar
  19. Inagaki H, Kuwahara M, Tsubone H, Mori Y (2013) The effect of post-weaning individual housing on 50-kHz calls emitted from male rats to sexually receptive female rats. Physiol Behav 110–1:30–33CrossRefGoogle Scholar
  20. Kim EJ, Kim ES, Covey E, Kim JJ (2010) Social transmission of fear in rats: the role of 22-kHz ultrasonic distress vocalizations. PLoS ONE 5:e15077CrossRefPubMedPubMedCentralGoogle Scholar
  21. Kisko TM, Himmler BT, Himmler SM, Euston DR, Pellis SM (2015) Are 50-kHz calls used as play signals in the playful interactions of rats? II. Evidence from the effects of devocalization. Behav Process 111:25–33CrossRefGoogle Scholar
  22. Kisko TM, Wöhr M, Pellis VC, Pellis SM (this issue) Play or aggression: high-frequency 50-kHz ultrasonic vocalizations as play or appeasement signals in rats. Curr Top Behav NeurosciGoogle Scholar
  23. Knutson B, Burgdorf J, Panksepp J (1998) Anticipation of play elicits high-frequency ultrasonic vocalizations in young rats. J Comp Psychol 112:65–73CrossRefPubMedGoogle Scholar
  24. Lapiz MD, Fulford A, Muchimapura S, Mason R, Parker T, Marsden CA (2003) Influence of postweaning social isolation in the rat on brain development, conditioned behavior, and neurotransmission. Neurosci Behav Physiol 33:13–29CrossRefPubMedGoogle Scholar
  25. Łopuch S, Popik P (2011) Cooperative behavior of laboratory rats (Rattus norvegicus) in an instrumental task. J Comp Psychol 125:250–253CrossRefPubMedGoogle Scholar
  26. Lore R, Flannelly K, Farina P (1976) Ultrasounds produced by rats accompany decreases in intraspecific fighting. Aggress Behav 2:175–181CrossRefGoogle Scholar
  27. Markram K, Markram H (2010) The intense world theory—A unifying theory of the neurobiology of autism. Front Hum Neurosci 4:224CrossRefPubMedPubMedCentralGoogle Scholar
  28. Markram H, Rinaldi T, Markram K (2007) The intense world syndrome–an alternative hypothesis for autism. Front Neurosci 1:77–96CrossRefPubMedPubMedCentralGoogle Scholar
  29. Nunes Mamede Rosa ML, Nobre MJ, Ribeiro Oliveira A, Brandão ML (2005) Isolation-induced changes in ultrasonic vocalization, fear-potentiated startle and prepulse inhibition in rats. Neuropsychobiology 51:248–255Google Scholar
  30. 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 115:25–38CrossRefPubMedGoogle Scholar
  31. Panksepp J, Gordon N, Burgdorf J (2002) Empathy and the action-perception resonances of basic socio-emotional systems of the brain. Behav Brain Sci 25:43–44CrossRefGoogle Scholar
  32. Parsana AJ, Li N, Brown TH (2012a) Positive and negative ultrasonic social signals elicit opposing firing patterns in rat amygdala. Behav Brain Res 226:77–86CrossRefPubMedGoogle Scholar
  33. Parsana AJ, Moran EE, Brown TH (2012b) Rats learn to freeze to 22-kHz ultrasonic vocalizations through autoconditioning. Behav Brain Res 232:395–399CrossRefPubMedPubMedCentralGoogle Scholar
  34. Pohorecky LA (2008) Psychosocial stress and chronic ethanol ingestion in male rats: Effects on elevated plus maze behavior and ultrasonic vocalizations. Physiol Behav 94:432–447CrossRefPubMedGoogle Scholar
  35. 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 435:17–23CrossRefPubMedGoogle Scholar
  36. Schneider T, Turczak J, Przewłocki R (2006) Environmental enrichment reverses behavioral alterations in rats prenatally exposed to valproic acid: issues for a therapeutic approach in autism. Neuropsychopharmacology 31:36–46PubMedGoogle Scholar
  37. 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 9:102CrossRefPubMedPubMedCentralGoogle Scholar
  38. Seffer D, Schwarting RK, Wöhr M (2014) Pro-social ultrasonic communication in rats: insights from playback studies. J Neurosci Methods 234:73–81CrossRefPubMedGoogle Scholar
  39. Silverman JL, Yang M, Lord C, Crawley JN (2010) Behavioural phenotyping assays for mouse models of autism. Nat Rev Neurosci 11:490–502CrossRefPubMedPubMedCentralGoogle Scholar
  40. Siviy SM, Panksepp J (1987) Sensory modulation of juvenile play in rats. Dev Psychobiol 20:39–55CrossRefPubMedGoogle Scholar
  41. Tomazini FM, Reimer A, Albrechet-Souza L, Brandao ML (2006) Opposite effects of short- and long-duration isolation on ultrasonic vocalization, startle and prepulse inhibition in rats. J Neurosci Meth 153:114–120CrossRefGoogle Scholar
  42. Valluy J, Bicker S, Aksoy-Aksel A, Lackinger M, Sumer S, Fiore R, Wüst T, Seffer D, Metge F, Dieterich C, Wöhr M, Schwarting R, Schratt G (2015) A coding-independent function of an alternative Ube3a transcript during neuronal development. Nat Neurosci 18:666–673CrossRefPubMedGoogle Scholar
  43. Von Frijtag JC, Schot M, van den Bos R, Spruijt BM (2002) Individual housing during the play period results in changed responses to and consequences of a psychosocial stress situation in rats. Dev Psychobiol 41:58–69CrossRefGoogle Scholar
  44. Wen F, Xu L (2010) Effects of isolation after sexual experience on anxiety-like, depressive-like behaviors and affective states in male rats. Chin Sci Bull 55:4136–4142CrossRefGoogle Scholar
  45. Willadsen M, Seffer D, Schwarting RKW, Wöhr M (2014) Rodent ultrasonic communication: male prosocial 50-kHz ultrasonic vocalizations elicit social approach behavior in female rats (Rattus norvegicus). J Comp Psychol 128:56–64CrossRefPubMedGoogle Scholar
  46. Willey AR, Spear LP (2013) The effects of pre-test social deprivation on a natural reward incentive test and concomitant 50 kHz ultrasonic vocalization production in adolescent and adult male Sprague-Dawley rats. Behav Brain Res 245:107–112CrossRefPubMedPubMedCentralGoogle Scholar
  47. Willuhn I, Tose A, Wanat MJ, Hart AS, Hollon NG, Phillips PE, Schwarting RK, Wöhr M (2014) Phasic dopamine release in the nucleus accumbens in response to pro-social 50 kHz ultrasonic vocalizations in rats. J Neurosci 34:10616–10623CrossRefPubMedPubMedCentralGoogle Scholar
  48. Wöhr M, Scattoni ML (2013) Behavioural methods used in rodent models of autism spectrum disorders: current standards and new developments. Behav Brain Res 251:5–17CrossRefPubMedGoogle Scholar
  49. Wöhr M, Schwarting RKW (2007) Ultrasonic communication in rats: can playback of 50-kHz calls induce approach behavior? PLoS ONE 2:e1365CrossRefPubMedPubMedCentralGoogle Scholar
  50. Wöhr M, Schwarting RKW (2008a) Maternal care, isolation-induced infant ultrasonic calling, and their relations to adult anxiety-related behavior in the rat. Behav Neurosci 122:310–330CrossRefPubMedGoogle Scholar
  51. Wöhr M, Schwarting RKW (2008b) Ultrasonic calling during fear conditioning in the rat: no evidence for an audience effect. Anim Behav 76:749–760CrossRefGoogle Scholar
  52. Wöhr M, Schwarting RKW (2009) Ultrasonic communication in rats: effects of morphine and naloxone on vocal and behavioral responses to playback of 50-kHz vocalizations. Pharmacol Biochem Behav 94:285–295CrossRefPubMedGoogle Scholar
  53. Wöhr M, Schwarting RKW (2012) Testing social acoustic memory in rats: effects of stimulus configuration and long-term memory on the induction of social approach behavior by appetitive 50-kHz ultrasonic vocalizations. Neurobiol Learn Mem 98:154–164CrossRefPubMedGoogle Scholar
  54. Wöhr M, Houx B, Schwarting RKW, Spruijt B (2008) Effects of experience and context on 50-kHz vocalizations in rats. Physiol Behav 93:766–776CrossRefPubMedGoogle Scholar
  55. Wöhr M, Schwarting RKW (2013) Affective communication in rodents: ultrasonic vocalizations as a tool for research on emotion and motivation. Cell Tissue Res 354:81–97CrossRefPubMedGoogle Scholar

Copyright information

© Springer International Publishing Switzerland AG 2015

Authors and Affiliations

  • Markus Wöhr
    • 1
  • K. Alexander Engelhardt
    • 1
  • Dominik Seffer
    • 1
  • A. Özge Sungur
    • 1
  • Rainer K. W. Schwarting
    • 1
  1. 1.Behavioral Neuroscience, Experimental and Biological PsychologyPhilipps-University of MarburgMarburgGermany

Personalised recommendations