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Ultrasonic Vocalizations by Infant Mice: An Ethological Expression of Separation Anxiety

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Mood and Anxiety Related Phenotypes in Mice

Part of the book series: Neuromethods ((NM,volume 42))

Abstract

The ultrasonic vocalization, or isolation calling, of infant rats and mice has been studied as a measure of anxious affective state and as an early communicative behavior between a pup and mother. The protocol described herein is the typical separation testing procedure. Also included are procedures used to modulate crying by providing contact with littermates and/or dam and increased isolation calling response by a prior brief maternal interaction. These procedures provide the basis for experimental research on the early development of emotion and communication in a critically important experimental model species – the mouse.

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References

  1. Newman JD. Neural circuits underlying crying and cry responding in mammals. Behavioural Brain Research 2007;182:155–65.

    Article  PubMed  Google Scholar 

  2. Dunn PM. Aristotle (384–322 BC): philosopher and scientist of ancient Greece. Archives of Disease in Childhood 2006;91:F75-7.

    PubMed  CAS  Google Scholar 

  3. Blumberg MS, Alberts JR. Ultrasonic vocalizations by rat pups in the cold: an acoustic by-product of laryngeal braking? Behavioral Neuroscience 1990;104:808–17.

    Article  PubMed  CAS  Google Scholar 

  4. Blumberg MS, Sokoloff G. Do infant rats cry? Psychological Review 2001;108:83–95.

    Article  PubMed  CAS  Google Scholar 

  5. Panksepp J. Can anthropomorphic analyses of separation cries in other animals inform us about the emotional nature of social loss in humans? Comment on Blumberg and Sokoloff (2001). Psychological Review 2003;110:376–88; discussion 89–96.

    Google Scholar 

  6. Hofer MA, Shair HN. Ultrasonic vocalization, laryngeal braking, and thermogenesis in rat pups: a reappraisal. Behavioral Neuroscience 1993;107:354–62.

    Article  Google Scholar 

  7. Noirot E. Ultrasounds and maternal behavior in small rodents. Developmental Psychobiology 1972;5:371–87.

    Article  PubMed  CAS  Google Scholar 

  8. Nitschke W, Bell RW, Zachman T. Distress vocalizations of young in three inbred strains of mice. Developmental Psychobiology 1972;5:363–70.

    Article  PubMed  CAS  Google Scholar 

  9. Motomura N, Shimizu K, Shimizu M, et al. A comparative study of isolation-induced ultrasonic vocalization in rodent pups. Experimental Animals 2002;51:187–90.

    Article  PubMed  CAS  Google Scholar 

  10. Shair HN, Brunelli SA, Masmela JR, Boone E, Hofer MA. Social, thermal, and temporal influences on isolation-induced and maternally potentiated ultrasonic vocalizations of rat pups. Developmental Psychobiology 2003;42:206–22.

    Article  PubMed  Google Scholar 

  11. Winslow JT, Insel TR. The infant rat separation paradigm: a novel test for novel anxiolytics. Trends in Pharmacological Sciences 1991;12:402–4.

    Article  PubMed  CAS  Google Scholar 

  12. Hofer MA, Masmela JR, Brunelli SA, Shair HN. The ontogeny of maternal potentiation of the infant rats' isolation call. Developmental Psychobiology 1998;33:189–201.

    Article  PubMed  CAS  Google Scholar 

  13. Hofer MA. Multiple regulators of ultrasonic vocalization in the infant rat. Psychoneuroendocrinology 1996;21:203–17.

    Article  PubMed  CAS  Google Scholar 

  14. Brudzynski SM. Principles of rat communication: quantitative parameters of ultrasonic calls in rats. Behavior Genetics 2005;35:85–92.

    Google Scholar 

  15. Brudzynski SM, Kehoe P, Callahan M. Sonographic structure of isolation-induced ultrasonic calls of rat pups. Developmental Psychobiology 1999;34:195–204.

    Article  PubMed  CAS  Google Scholar 

  16. Olivier B, Molewijk E, van Oorschot R, et al. New animal models of anxiety. European Neuropsychopharmacology 1994;4:93–102.

    Article  PubMed  CAS  Google Scholar 

  17. Rodgers RJ. Animal models of 'anxiety': where next? Behavioural Pharmacology 1997;8:477–96; discussion 97–504.

    Article  PubMed  CAS  Google Scholar 

  18. Moriceau S, Sullivan RM. Neurobiology of infant attachment. Developmental Psychobiology 2005;47:230–42.

    Article  PubMed  Google Scholar 

  19. Hofer MA. Early relationships as regulators of infant physiology and behavior. Acta Paediatrica Supplementum 1994;397:9–18.

    Article  CAS  Google Scholar 

  20. Hofer MA. Early social relationships: a psychobiologist's view. Child Development 1987;58:633–47.

    Article  PubMed  CAS  Google Scholar 

  21. Masi G, Mucci M, Millepiedi S. Separation anxiety disorder in children and adolescents: epidemiology, diagnosis and management. CNS Drugs 2001;15:93–104.

    Article  PubMed  CAS  Google Scholar 

  22. Hofer MA, Shair HN, Brunelli SA. Ultrasonic vocalizations in rat and mouse pups. Current protocols in neuroscience/editorial board, Jacqueline N Crawley [et al. 2002;Chapter 8 Unit 8 14].

    Google Scholar 

  23. Blumberg MS, Sokoloff G, Kent KJ. Cardiovascular concomitants of ultrasound production during cold exposure in infant rats. Behavioral Neuroscience 1999;113:1274–82.

    Article  PubMed  CAS  Google Scholar 

  24. Hofer MA, Shair HN. Ultrasonic vocalization by rat pups during recovery from deep hypothermia. Developmental Psychobiology 1992;25:511–28.

    Article  PubMed  CAS  Google Scholar 

  25. Brunelli SA, Hofer MA. Development of ultrasonic vocalization responses in genetically heterogeneous National Institute of Health (N:NIH) rats. II. Associations among variables and behaviors. Developmental Psychobiology 1996;29:517–28.

    CAS  Google Scholar 

  26. Brunelli SA, Shair HN, Hofer MA. Hypothermic vocalizations of rat pups (Rattus norvegicus) elicit and direct maternal search behavior. Journal of Comparative Psychology 1994;108:298–303.

    Article  PubMed  CAS  Google Scholar 

  27. Allin JT, Banks EM. Functional aspects of ultrasound production by infant albino rats (Rattus norvegicus).Animal Behaviour 1972;20:175–85.

    Article  PubMed  CAS  Google Scholar 

  28. Benton D, Nastiti K. The influence of psychotropic drugs on the ultrasonic calling of mouse pups. Psychopharmacology (Berl) 1988;95:99–102.

    Article  CAS  Google Scholar 

  29. Newman JD, Winslow JT, Murphy DL. Modulation of vocal and nonvocal behavior in adult squirrel monkeys by selective MAO-A and MAO-B inhibition. Brain Reseach 1991;538:24–8.

    Article  CAS  Google Scholar 

  30. Brunelli SA, Hofer MA, Weller A. Selective breeding for infant vocal response: a role for postnatal maternal effects? Developmental Psychobiology 2001;38:221–8.

    Article  PubMed  CAS  Google Scholar 

  31. Brunner D, Buhot MC, Hen R, Hofer M. Anxiety, motor activation, and maternal-infant interactions in 5HT1B knockout mice.Behavioral Neuroscience 1999;113:587–601.

    Article  PubMed  CAS  Google Scholar 

  32. Winslow JT, Hearn EF, Ferguson J, Young LJ, Matzuk MM, Insel TR. Infant vocalization, adult aggression, and fear behavior of an oxytocin null mutant mouse. Hormones and Behavior 2000;37:145–55.

    Article  PubMed  CAS  Google Scholar 

  33. Crawley JN. Designing mouse behavioral tasks relevant to autistic-like behaviors. Mental retardation and developmental disabilities Research Reviews 2004;10:248–58.

    Article  PubMed  Google Scholar 

  34. Ehret G, Buckenmaier J. Estrogen-receptor occurrence in the female mouse brain: effects of maternal experience, ovariectomy, estrogen and anosmia. Journal of Physiology, Paris 1994;88:315–29.

    Article  PubMed  CAS  Google Scholar 

  35. Koch M, Ehret G. Estradiol and parental experience, but not prolactin are necessary for ultrasound recognition and pup-retrieving in the mouse. Physiology & Behavior 1989;45:771–6.

    Article  CAS  Google Scholar 

  36. Smotherman WP, Bell RW, Starzec J, Elias J, Zachman TA. Maternal responses to infant vocalizations and olfactory cues in rats and mice. Behavioral Biology 1974;12:55–66.

    Article  PubMed  CAS  Google Scholar 

  37. Hahn ME, Hewitt JK, Adams M, Tully T. Genetic influences on ultrasonic vocalizations in young mice. Behavior Genetics 1987;17:155–66.

    Article  PubMed  CAS  Google Scholar 

  38. Thornton LM, Hahn ME, Schanz N. Genetic and developmental influences on infant mouse ultrasonic calling. III. Patterns of inheritance in the calls of mice 3–9 days of age. Behavior Genetics 2005;35:73–83.

    Google Scholar 

  39. Roubertoux PL, Martin B, Le Roy I, et al. Vocalizations in newborn mice: genetic analysis. Behavior Genetics 1996;26:427–37.

    Article  PubMed  CAS  Google Scholar 

  40. Brunelli SA, Hofer MA. Selective breeding for infant rat separation-induced ultrasonic vocalizations: developmental precursors of passive and active coping styles. Behavioural Brain Research 2007;182:193–207.

    Article  PubMed  Google Scholar 

  41. Brunelli SA, Myers MM, Asekoff SL, Hofer MA. Effects of selective breeding for infant rat ultrasonic vocalization on cardiac responses to isolation. Behavioral Neuroscience 2002;116:612–23.

    Article  PubMed  Google Scholar 

  42. Brunelli SA, Vinocur DD, Soo-Hoo D, Hofer MA. Five generations of selective breeding for ultrasonic vocalization (USV) responses in N:NIH strain rats. Developmental Psychobiology 1997;31:255–65.

    Article  PubMed  CAS  Google Scholar 

  43. Winslow JT, Insel TR. Endogenous opioids: do they modulate the rat pup's response to social isolation? Behavioral Neuroscience 1991;105:253–63.

    Article  PubMed  CAS  Google Scholar 

  44. Shair HN, Brunelli SA, Hofer MA. Lack of evidence for mu-opioid regulation of a socially mediated separation response. Physiology & Behavior 2005;83:767–77.

    Article  CAS  Google Scholar 

  45. Hofer MA, Brunelli SA, Shair HN. Potentiation of isolation-induced vocalization by brief exposure of rat pups to maternal cues. Developmental Psychobiology 1994;27:503–17.

    Article  PubMed  CAS  Google Scholar 

  46. Ricceri L, Moles A, Crawley J. Behavioral phenotyping of mouse models of neurodevelopmental disorders: relevant social behavior patterns across the life span. Behavioural brain research 2007;176:40–52.

    Article  PubMed  Google Scholar 

  47. Scattoni ML, Crawley J, Ricceri L. Ultrasonic vocalizations: A tool for behavioural phenotyping of mouse models of neurodevelopmental disorders. Neuroscience and biobehavioral reviews 2008.

    Google Scholar 

  48. cattoni ML, Gandhy SU, Ricceri L, Crawley JN. Unusual repertoire of vocalizations in the BTBR T+tf/J mouse model of autism. PLoS ONE 2008;3:e3067.

    Google Scholar 

  49. Gaub S, Ehret G. Grouping in auditory temporal perception and vocal production is mutually adapted: the case of wriggling calls of mice. Journal of Comparative Physiology. A, Neuroethology, Sensory, Neural, and Behavioral Physiology 2005;191:1131–5.

    Article  Google Scholar 

  50. Roberts LH. The rodent ultrasound production mechanism.Ultrasonics 1975;13:83–8.

    Article  PubMed  CAS  Google Scholar 

  51. Goodrich CA. Measurement of body temperature in neonatal mice. Journal of Applied Physiology 1977;43:1102–5.

    PubMed  CAS  Google Scholar 

  52. Hofer MA, Shair H. Sensory processes in the control of isolation-induced ultrasonic vocalization by 2-week-old rats. Journal of Comparative and Physiological Psychology 1980;94:271–9.

    Article  PubMed  CAS  Google Scholar 

  53. Liu RC. Prospective contributions of transgenic mouse models to central auditory research. Brain Research 2006;1091:217–23.

    Article  PubMed  CAS  Google Scholar 

  54. Naito H, Tonoue T. Sex difference in ultrasound distress call by rat pups. Behavioural Brain Research 1987;25:13–21.

    Article  PubMed  CAS  Google Scholar 

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Author information

Authors and Affiliations

  1. NIMH IRP Neurobiology, Primate Core, National Institutes of Health (NIH), Bethesda, MD, USA

    James T. Winslow

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  1. James T. Winslow
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Editor information

Editors and Affiliations

  1. School of Medicine, University of Maryland, W. Baltimore Street 685, Baltimore, 21201, U.S.A.

    Todd D. Gould

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© 2009 Humana Press, a part of Springer Science+Business Media, LLC

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Winslow, J.T. (2009). Ultrasonic Vocalizations by Infant Mice: An Ethological Expression of Separation Anxiety. In: Gould, T. (eds) Mood and Anxiety Related Phenotypes in Mice. Neuromethods, vol 42. Humana Press, Totowa, NJ. https://doi.org/10.1007/978-1-60761-303-9_5

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  • DOI: https://doi.org/10.1007/978-1-60761-303-9_5

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  • Publisher Name: Humana Press, Totowa, NJ

  • Print ISBN: 978-1-60761-302-2

  • Online ISBN: 978-1-60761-303-9

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