Skip to main content
SpringerLink
Log in

Social Origin of Vocal Communication in Rodents

  • Chapter
  • First Online:
Biocommunication of Animals

Abstract

The Chapter is focused on evolutionary origin of vocal communication in rodents, and particularly ultrasonic vocalization in rats. Several hypotheses are discussed, including mother-infant interaction and expression of emotional/motivational states as mechanisms initiating vocal communication. Other hypotheses or contributing factors to evolution of vocal signalling are also presented, as predator pressure and habitat type, size and complexity of the social group, and security motivation system. Rats developed several ultrasonic calls that are explained and categorized into five types: short and long 22 kHz calls, flat 50 kHz calls and frequency-modulated 50 kHz calls with or without trills. It is concluded that mammalian vocalizations serve as ethological transmitter, termed ethotransmitter, that is produced by specialized organ (larynx), selectively recognized and decoded by the brain of conspecifics, and capable of changing emotional state and behavior of the receivers.

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 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Hardcover Book
USD 169.99
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

  • Alberts JR (2007) Huddling by rat pups: ontogeny of individual and group behavior. Dev Psychobiol 49(1):22–32

    Article  PubMed  Google Scholar 

  • Barfield RJ, Geyer LA (1975) The ultrasonic postejaculatory vocalization and the postejaculatory refractory period of the male rat. J Comp Physiol Psychol 88(2):723–734

    Article  PubMed  CAS  Google Scholar 

  • Basken JN, Connor NP, Ciucci MR (2012) Effect of aging on ultrasonic vocalizations and laryngeal sensorimotor neurons in rats. Exp Brain Res 219(3):351–361

    Article  PubMed  Google Scholar 

  • Bass AH, Chagnaud BP (2012) Shared developmental and evolutionary origins for neural basis of vocal-acoustic and pectoral-gestural signaling. Proc Natl Acad Sci USA 109(Suppl 1):10677–10684

    Article  PubMed  CAS  Google Scholar 

  • Bass AH, Gilland EH, Baker R (2008) Evolutionary origins for social vocalization in a vertebrate hindbrain-spinal compartment. Science 321(5887):417–421

    Article  PubMed  CAS  Google Scholar 

  • Blanchard RJ, Blanchard DC (1989) Antipredator defensive behaviors in a visible burrow system. J Comp Psychol 103(1):70–82

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Blanchard RJ, Agullana R, McGee L, Weiss S, Blanchard DC (1992) Sex differences in the incidence and sonographic characteristics of antipredator ultrasonic cries in the laboratory rat (Rattus norvegicus). J Comp Psychol 106(3):270–277

    Article  PubMed  CAS  Google Scholar 

  • Blumstein DT (1999) The evolution of functionally referential alarm communication. Multiple adaptations; multiple constraints. Evol Commun 3(2):135–147

    Article  Google Scholar 

  • Blumstein DT, Armitage KB (1997a) Alarm calling in yello-bellied marmots. I. The meaning of situationally variable alarm calls. Anim Behav 53:143–171

    Article  Google Scholar 

  • Blumstein DT, Armitage KB (1997b) Does sociality drive the evolution of communicative complexity? A comparative test with ground-dwelling sciurid alarm calls. Am Nat 150(2):179–200

    Article  PubMed  CAS  Google Scholar 

  • Bronson FH (1979) The reproductive ecology of the house mouse. Q Rev Biol 54(3):265–299

    Article  PubMed  CAS  Google Scholar 

  • Brudzynski SM (1994) Ultrasonic vocalization induced by intracerebral carbachol in rats: localization and a dose–response study. Behav Brain Res 63(2):133–143

    Article  PubMed  CAS  Google Scholar 

  • Brudzynski SM (2005) Principles of rat communication: quantitative parameters of ultrasonic calls in rats. Behav Genet 35(1):85–92

    Article  PubMed  Google Scholar 

  • Brudzynski SM (2007) Ultrasonic calls of rats as indicator variables of negative or positive states: acetylcholine-dopamine interaction and acoustic coding. Behav Brain Res 182(2):261–273

    Article  PubMed  CAS  Google Scholar 

  • Brudzynski SM (2009) Communication of adult rats by ultrasonic vocalization: biological, sociobiological, and neuroscience approaches. ILAR J 50(1):43–50

    Article  PubMed  CAS  Google Scholar 

  • Brudzynski SM (2010) Vocalization as an ethotransmitter: introduction to the Handbook of Mammalian Vocalization. (Chapter 1.1). In: Brudzynski SM (ed) Handbook of mammalian vocalization. An integrative neuroscience approach, 1st edn. Academic/Elsevier, Amsterdam, pp 3–9

    Chapter  Google Scholar 

  • Brudzynski SM (2013) Ethotransmission: communication of emotional states through ultrasonic vocalization in rats. Curr Opin Neurobiol 23:1–8. doi:10.1016/j.conb.2013.01.014

    Article  Google Scholar 

  • Brudzynski SM, Chiu EM (1995) Behavioural responses of laboratory rats to playback of 22 kHz ultrasonic calls. Physiol Behav 57(6):1039–1044

    Article  PubMed  CAS  Google Scholar 

  • Brudzynski SM, Holland G (2005) Acoustic characteristics of air puff-induced 22-kHz alarm calls in direct recordings. Neurosci Biobehav Rev 29(8):1169–1180

    Article  PubMed  Google Scholar 

  • Brudzynski SM, Ociepa D (1992) Ultrasonic vocalization of laboratory rats in response to handling and touch. Physiol Behav 52(4):655–660

    Article  PubMed  CAS  Google Scholar 

  • Brudzynski SM, Bihari F, Ociepa D, Fu XW (1993) Analysis of 22 kHz ultrasonic vocalization in laboratory rats: long and short calls. Physiol Behav 54(2):215–221

    Article  PubMed  CAS  Google Scholar 

  • Brudzynski SM, Kehoe P, Callahan M (1999) Sonographic structure of isolation-induced ultrasonic calls of rat pups. Dev Psychobiol 34(3):195–204

    Article  PubMed  CAS  Google Scholar 

  • Brudzynski SM, Silkstone M, Komadoski M, Scullion K, Duffus S, Burgdorf J, Kroes RA, Moskal JR, Panksepp J (2011) Effects of intraaccumbens amphetamine on production of 50 kHz vocalizations in three lines of selectively bred Long-Evans rats. Behav Brain Res 217(1):32–40

    Article  PubMed  CAS  Google Scholar 

  • Brudzynski SM, Komadoski M, St Pierre J (2012) Quinpirole-induced 50 kHz ultrasonic vocalization in the rat: role of D2 and D3 dopamine receptors. Behav Brain Res 226(2):511–518

    Article  PubMed  CAS  Google Scholar 

  • Burgdorf J, Moskal JR (2010) Frequency modulated 50 kHz ultrasonic vocalizations reflect a positive emotional state in the rat: neural substrates and therapeutic implications. (Chapter 6.2). In: Brudzynski SM (ed) Handbook of mammalian vocalization. An integrative neuroscience approach, 1st edn. Academic/Elsevier, Amsterdam, pp 209–214

    Chapter  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(4):357–367

    Article  PubMed  Google Scholar 

  • Burgdorf J, Panksepp J, Brudzynski SM, Beinfeld MC, Cromwell HC, Kroes RA, Moskal JR (2009) The effects of selective breeding for differential rates of 50-kHz ultrasonic vocalizations on emotional behavior in rats. Dev Psychobiol 51(1):34–46

    Article  PubMed  Google Scholar 

  • Burgdorf J, Panksepp J, Moskal JR (2011) Frequency-modulated 50 kHz ultrasonic vocalizations: a tool for uncovering the molecular substrates of positive affect. Neurosci Biobehav Rev 35(9):1831–1836

    Article  PubMed  Google Scholar 

  • Calhoun JB (1950) The study of wild animals under controlled conditions. Ann N Y Acad Sci 39:1113–1122

    Article  Google Scholar 

  • Carleton MD, Musser GG (2005) Order rodentia. In: Wilson DE, Reeder DM (eds) Mammal species of the world. A taxonomic geographic reference, vol 1, 3rd edn. John Hopkins University Press, Baltimore, pp 745–752

    Google Scholar 

  • Edmunds M (1974) Defence in animals. A survey of anti-predator defences. Longman Group, Ltd., New York

    Google Scholar 

  • Freeberg TM, Dunbar RIM, Ord TJ (2012) Social complexity as a proximate and ultimate factor in communicative complexity. Philos Trans R Soc Lond B Biol Sci 367:1785–1801

    Article  PubMed  Google Scholar 

  • Furrer RD, Manser MB (2009) The evolution of urgency-based and functionally referential alarm calls in ground-dwelling species. Am Nat 173(3):400–410

    Article  PubMed  Google Scholar 

  • Galler JR, Propert KJ (1982) Early maternal behaviors predictive of the survival of suckling rats with intergenerational malnutrition. J Nutr 112(2):332–337

    PubMed  CAS  Google Scholar 

  • Gifford GW 3rd, Hauser MD, Cohen YE (2003) Discrimination of functionally referential calls by laboratory-housed rhesus macaques: implications for neuroethological studies. Brain Behav Evol 61(4):213–224

    Article  PubMed  Google Scholar 

  • Groenink L, Verdouw PM, van Oorschot R, Olivier B (2008) Models of anxiety: ultrasonic vocalizations of isolated rat pups. Curr Protoc Pharmacol Chapter 5:Unit 5.18. doi:10.1002/0471141755.ph0518s43

  • Gubernick DJ, Alberts JR (1983) Maternal licking of young: resource exchange and proximate controls. Physiol Behav 31(5):593–601

    PubMed  CAS  Google Scholar 

  • Haney M, Miczek KA (1993) Ultrasounds during agonistic interactions between female rats (Rattus norvegicus). J Comp Psychol 107(4):373–379

    Article  PubMed  CAS  Google Scholar 

  • Harmon KM, Cromwell HC, Burgdorf J, Moskal JR, Brudzynski SM, Kroes RA, Panksepp J (2008) Rats selectively bred for low levels of 50 kHz ultrasonic vocalizations exhibit alterations in early social motivation. Dev Psychobiol 50(4):322–331

    Article  PubMed  CAS  Google Scholar 

  • Hinds AL, Woody EZ, Drandic A, Schmidt LA, Van Ameringen M, Coroneos M, Szechtman H (2010) The psychology of potential threat: properties of the security motivation system. Biol Psychol 85(2):331–337

    Article  PubMed  Google Scholar 

  • Hofer MA (1996) Multiple regulators of ultrasonic vocalization in the infant rat. Psychoneuroendocrinology 21(2):203–217

    Article  PubMed  CAS  Google Scholar 

  • Hofer MA (2010) Evolution of the infant separation call: rodent ultrasonic vocalization. In: Brudzynski SM (ed) Handbook of mammalian vocalization. An integrative neuroscience approach, 1st edn. Academic/Elsevier, Amsterdam, pp 29–35

    Chapter  Google Scholar 

  • Hofer MA, Masmela JR, Brunelli SA, Shair HN (1999) Behavioral mechanisms for active maternal potentiation of isolation calling in rat pups. Behav Neurosci 113(1):51–61

    Article  PubMed  CAS  Google Scholar 

  • Hofer MA, Shair HN, Brunelli SA (2002) Ultrasonic vocalizations in rat and mouse pups. Curr Protoc Neurosci Chapter 8:Unit 8.14. doi: 10.1002/0471142301.ns0814s17

  • Kaltwasser MT (1990) Startle-inducing acoustic stimuli evoke ultrasonic vocalization in the rat. Physiol Behav 48(1):13–17

    Article  PubMed  CAS  Google Scholar 

  • Kaltwasser MT (1991) Acoustic startle induced ultrasonic vocalization in the rat: a novel animal model of anxiety? Behav Brain Res 43(2):133–137

    Article  PubMed  CAS  Google Scholar 

  • Kelley DB, Bass AH (2010) Neurobiology of vocal communication: mechanisms for sensorimotor integration and vocal patterning. Curr Opin Neurobiol 20(6):748–753

    Article  PubMed  CAS  Google Scholar 

  • Kim EJ, Kim ES, Covey E, Kim JJ (2010) Social transmission of fear in rats: the role of 22-kHz ultrasonic distress vocalization. PLoS One 5(12):e15077. doi:10.1371/journal.pone.0015077

    Article  PubMed  CAS  Google Scholar 

  • Litvin Y, Blanchard DC, Blanchard RJ (2007) Rat 22kHz ultrasonic vocalizations as alarm cries. Behav Brain Res 182(2):166–172

    Article  PubMed  Google Scholar 

  • Ma ST, Maier EY, Ahrens AM, Schallert T, Duvauchelle CL (2010) Repeated intravenous cocaine experience: development and escalation of pre-drug anticipatory 50-kHz ultrasonic vocalizations in rats. Behav Brain Res 212(1):109–114

    Article  PubMed  CAS  Google Scholar 

  • MacLean PD (1985) Brain evolution relating to family, play, and the separation call. Arch Gen Psychiatry 42(4):405–417

    Article  PubMed  CAS  Google Scholar 

  • Manser MB (2001) The acoustic structure of suricates’ alarm calls varies with predator type and the level of response urgency. Proc Biol Sci 268(1483):2315–2324

    Article  PubMed  CAS  Google Scholar 

  • McComb K, Semple S (2005) Coevolution of vocal communication and sociality in primates. Biol Lett 1(4):381–385

    Article  PubMed  Google Scholar 

  • McFarland D (1987) The oxford companion to animal behavior. Oxford University Press, Oxford/New York

    Google Scholar 

  • Moore CL, Chadwick-Dias AM (1986) Behavioral responses of infant rats to maternal licking: variations with age and sex. Dev Psychobiol 19(5):427–438

    Article  PubMed  CAS  Google Scholar 

  • Nagasawa M, Okabe S, Mogi K, Kikusui T (2012) Oxytocin and mutual communication in mother-infant bonding. Front Hum Neurosci 6:31. doi:10.3389/fnhum.2012.00031

    Article  PubMed  Google Scholar 

  • Naito H, Inoue M, Makino J (2000) Ultrasonic isolation calls in genetically high- and low-emotional rat pups. Exp Anim 49(4):289–294

    Article  PubMed  CAS  Google Scholar 

  • Newman JD (2007) Neural circuits underlying crying and cry responding in mammals. Behav Brain Res 182(2):155–165

    Article  PubMed  Google Scholar 

  • Nyby J (2010) Adult house mouse (Mus musculus) ultrasonic calls: hormonal and pheromonal regulation. In: Brudzynski SM (ed) Handbook of mammalian vocalization. An integrative neuroscience approach, 1st edn. Academic/Elsevier, Amsterdam, pp 303–310

    Chapter  Google Scholar 

  • Nyby J, Whitney G (1978) Ultrasonic communication of adult myomorph rodents. Neurosci Biobehav Rev 2:1–14

    Article  Google Scholar 

  • Parsana AJ, Li N, Brown TH (2012) Positive and negative ultrasonic social signals elicit opposing firing patterns in rat amygdala. Behav Brain Res 226(1):77–86

    Article  PubMed  Google Scholar 

  • Pérez-Cano FJ, Franch À, Castellote C, Castell M (2012) The suckling rat as a model for immunonutrition studies in early life. Clin Dev Immunol 2012:537310. doi: 10.1155/2012/537310

  • Pollard KA, Blumstein DT (2011) Social group size predicts the evolution of individuality. Curr Biol 21(5):413–417

    Article  PubMed  CAS  Google Scholar 

  • Pollard KA, Blumstein DT (2012) Evolving communicative complexity: insights from rodents and beyond. Philos Trans R Soc Lond B Biol Sci 367(1597):1869–1878

    Article  PubMed  Google Scholar 

  • Porges SW (2001) The polyvagal theory: phylogenetic substrates of a social nervous system. Int J Psychophysiol 42(2):123–146

    Article  PubMed  CAS  Google Scholar 

  • Porges SW (2003) The polyvagal theory: phylogenetic contributions to social behavior. Physiol Behav 79(3):503–513

    Article  PubMed  CAS  Google Scholar 

  • Portfors CV (2007) Types and functions of ultrasonic vocalizations in laboratory rats and mice. J Am Assoc Lab Anim Sci 46(1):28–34

    PubMed  CAS  Google Scholar 

  • Randall JA, McCowan B, Collins KC, Hooper SL, Rogovin K (2005) Alarm signals of the great gerbil: acoustic variation by predator context, sex, age, individual, and family group. J Acoust Soc Am 118(4):2706–2714

    Article  PubMed  Google Scholar 

  • Remage-Healey L, Bass AH (2006) From social behavior to neural circuitry: steroid hormones rapidly modulate advertisement calling via a vocal pattern generator. Horm Behav 50(3):432–441

    Article  PubMed  CAS  Google Scholar 

  • Robinson SR (1981) Alarm communication in Belding’s ground squirrels. Z Tierpsych 55(2):150–168

    Google Scholar 

  • Rosenthal GG, Ryan MJ (2000) Visual and acoustic communication in non-human animals: a comparison. J Biosci 25(3):285–290

    Article  PubMed  CAS  Google Scholar 

  • Sachs MB, Sinnott JM, Hienz RD (1978) Behavioral and physiological studies of hearing in birds. Fed Proc 37(10):2329–2335

    PubMed  CAS  Google Scholar 

  • Sales GD (2010) Ultrasonic calls of wild and wild-type rodents. In: Brudzynski SM (ed) Handbook of mammalian vocalization. An integrative neuroscience approach, 1st edn. Academic/Elsevier, Amsterdam, pp 77–88

    Chapter  Google Scholar 

  • Schank JC, Alberts JR (2000) The developmental emergence of coupled activity as cooperative aggregation in rat pups. Proc Biol Sci 267(1459):2307–2315

    Article  PubMed  CAS  Google Scholar 

  • Schwarting RK, Jegan N, Wöhr M (2007) Situational factors, conditions and individual variables which can determine ultrasonic vocalizations in male adult Wistar rats. Behav Brain Res 182(2):208–222

    Article  PubMed  Google Scholar 

  • Sherman PW (1985) Alarm calls of Belding’s ground squirrels to aerial predators: nepotism and self-preservation? Behav Ecol Sociobiol 17:313–323

    Article  Google Scholar 

  • Slocombe KE, Zuberbühler K (2005) Functionally referential communication in a chimpanzee. Curr Biol 15(19):1779–1784

    Article  PubMed  CAS  Google Scholar 

  • Stephan C, Zuberbühler K (2008) Predation increases acoustic complexity in primate alarm calls. Biol Lett 4(6):641–644

    Article  PubMed  Google Scholar 

  • Szechtman H, Woody E (2004) Obsessive-compulsive disorder as a disturbance of security motivation. Psychol Rev 111(1):111–127

    Article  PubMed  Google Scholar 

  • Takahashi N, Kashino M, Hironaka N (2010) Structure of rat ultrasonic vocalizations and its relevance to behavior. PLoS One 5(11):e14115. doi:10.1371/journal.pone.0014115

    Article  PubMed  CAS  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(3):201–206

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Wheeler BC, Fischer J (2012) Functionally referential signals: a promising paradigm whose time has passed. Evol Anthropol 21(5):195–205

    Article  PubMed  Google Scholar 

  • Wöhr M, Schwarting RK (2008) Maternal care, isolation-induced infant ultrasonic calling, and their relations to adult anxiety-related behavior in the rat. Behav Neurosci 122(2):310–330

    Article  PubMed  Google Scholar 

  • Wöhr M, Houx B, Schwarting RK, Spruijt B (2008) Effects of experience and context on 50-kHz vocalizations in rats. Physiol Behav 93(4–5):766–776

    Article  PubMed  Google Scholar 

  • Woody EZ, Szechtman H (2011) Adaptation to potential threat: the evolution, neurobiology, and psychopathology of the security motivation system. Neurosci Biobehav Rev 35(4):1019–1033

    Article  PubMed  Google Scholar 

  • Wright JM, Gourdon JC, 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. Psychopharmacology (Berl) 211(1):1–13

    Article  CAS  Google Scholar 

  • Würbel H, Burn C, Latham N (2009) The behaviour of rats and mice. In: Jensen P (ed) The ethology of domestic animals. An introductory text, 2nd edn. CAB International, Wallingford/Cambridge, pp 217–235

    Google Scholar 

  • Young BA (2003) Snake bioacoustics: toward a richer understanding of the behavioral ecology of snakes. Q Rev Biol 78(3):303–325

    Article  PubMed  Google Scholar 

  • Zimmerberg B, Kim JH, Davidson AN, Rosenthal AJ (2003) Early deprivation alters the vocalization behavior of neonates directing maternal attention in a rat model of child neglect. Ann N Y Acad Sci 1008:308–313

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

The experimental part of this chapter originating from the author’s laboratory and preparation of this text were supported by the discovery grant from the Natural Sciences and Engineering Research Council of Canada. The author would like to thank Dr. Henry Szechtman for his comments on the manuscript.

Author information

Authors and Affiliations

  1. Department of Psychology, Brock University, 500 Glenridge Avenue, L2S 3A1, St. Catharines, ON, Canada

    Stefan M. Brudzynski Ph.D., D.Sc.

Authors
  1. Stefan M. Brudzynski Ph.D., D.Sc.
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Stefan M. Brudzynski Ph.D., D.Sc. .

Editor information

Editors and Affiliations

  1. Telos - Philosophische Praxis, Bürmoos, Austria

    Guenther Witzany

Rights and permissions

Reprints and permissions

Copyright information

© 2014 Springer Science+Business Media Dordrecht

About this chapter

Cite this chapter

Brudzynski, S.M. (2014). Social Origin of Vocal Communication in Rodents. In: Witzany, G. (eds) Biocommunication of Animals. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-7414-8_5

Download citation

Publish with us

Policies and ethics

Search

Navigation