Behavior Genetics

, Volume 35, Issue 1, pp 19–29 | Cite as

Infant Rodent Ultrasounds – A Gate to the Understanding of Sound Communication

  • Günter Ehret


Components of the communication system between infant and adult rodents based on ultrasonic vocalizations (USVs) of infants are analyzed. USVs are most often emitted from a pup lost outside the nest in response to changes of: (i) body temperature, (ii) contact with adults/littermates, (iii) handling, and (iv) smell. These changes modulate the state of arousal and the emotional/motivational states and, as a result, USVs are produced. Acoustic properties of USVs seem to reflect the degrees of changes in arousal and emotion/motivation. Adult rodents are aroused by perceiving the USVs, locate the sender and show a phonotaxic approach to the sender. Acoustic properties of USVs in the frequency and time domains are described based on which adult rodents discriminate the USVs from other ultrasounds and take the USVs or adequate models of them as preferred goals of their phonotaxic approach. The preferred approach to adequate USVs is modulated by emotions/motivations, the sex of the receiver, hormonal states, experience with pups and neurotransmitter systems of the brain. The phonotaxis can be understood as the appetitive component of a pup-caring instinct. The consummatory act of the instinct is the retrieval of the lost pup. This retrieval is independent of USV presence, but it closes the communication loop activated by the emission of USVs. Communication with USVs can be used as a tool to investigate genetic and brain mechanisms of behavioral control.


Arousal auditory perception instinctive behavior mouse phonotaxis ultrasound communication 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Allin, J. T., Banks, E. M. 1971Effects of temperature on ultrasound production by infant albino ratsDev. Psychobiol.4149156CrossRefPubMedGoogle Scholar
  2. Bell, R. W. 1974Ultrasounds in small rodents: arousal-produced and arousal-producingDev. Psychobiol.73942CrossRefPubMedGoogle Scholar
  3. Bell, R. W., Nitschke, W., Zachmann, T. A. 1972Ultrasounds in three inbred strains of young miceBehav. Biol.7805814PubMedGoogle Scholar
  4. Blumberg, M. S., Alberts, J. R. 1991On the significance of similarities between ultrasonic vocalizations of infant and adult ratsNeurosci. Biobehav. Rev.15383390PubMedGoogle Scholar
  5. Blumberg, M. S., Efiemova, I. V., Alberts, J. R. 1992Ultrasonic vocalizations by rat pups: the primary importance of ambient temperature and the thermal significance of the contact comfortDev. Psychobiol.25229250CrossRefPubMedGoogle Scholar
  6. Blumberg, M.S., Sokoloff, G. 2001Do infant rats cry?Psychol. Rev.1088395PubMedGoogle Scholar
  7. Bolivar, V. J., Brown, R. E. 1994The ontogeny of ultrasonic vocalizations and other behaviors in male jimpy (jp/Y) mice and their normal male littermatesDev. Psychobiol.27101110CrossRefPubMedGoogle Scholar
  8. Brown, R. E., Mathieson, W. B., Stapleton, J., Neumann, P. E. 1999Maternal behavior in female C57BL/6J and DBA/2J inbred micePhysiol. Behav.67599605CrossRefPubMedGoogle Scholar
  9. Brudzynski, S. M., Bihari, F., Ociepa, D., Fu, X.-W. 1993Analysis of 22 kHz ultrasonic vocalization in laboratory rats : long and short callsPhysiol. Behav.54215221CrossRefPubMedGoogle Scholar
  10. Brudzynski, S. M., Kehoe, P., Callahan, M. 1999Sonagraphic structure of isolation-induced ultrasonic calls of rat pupsDev. Psychobiol.34195204CrossRefPubMedGoogle Scholar
  11. Brudzynski, S. M., Ociepa, D. 1992Ultrasonic vocalization of laboratory rats in response to handling and touchPhysiol. Behav.52655660CrossRefPubMedGoogle Scholar
  12. Brunelli, S. A., Myers, M. M., Asekoff, S. L, Hofer, M. A. 2002Effects of selective breeding for infant rat ultrasonic vocalization on cardiac responses to isolationBehav. Neurosci..116612623CrossRefPubMedGoogle Scholar
  13. Brunelli, S. A., Vinocur, D. D., Soo-Hoo, D., Hofer, M. A. 1997Five generations of selective breeding for ultrasonic vocalization (USV) responses in N : NIH strain ratsDev. Psychobiol.312551265Google Scholar
  14. Carden, S. E., Hofer, M. A. 1992Effect of a social companion of the ultrasonic vocalizations and contact responses of 3-day-old rat pupsBehav. Neurosci.106421426CrossRefPubMedGoogle Scholar
  15. Carlier, M., Roubertoux, P., Cohen-Salmon, C. 1982Differences in patterns of pup care inMus musculus domesticus. I – Comparisons between eleven inbred strainsBehav. Neurol. Biol.35205210CrossRefGoogle Scholar
  16. Cohen-Salmon, C., Carlier, M., Roubertoux, P., Jouhaneau, J., Sema1, C., Paillette, M. 1985Differences in patterns of pup care in mice. V – Pup ultrasonic emissions and pup care behaviorPhysiol. Behav.35167174CrossRefPubMedGoogle Scholar
  17. Conely, L., Bell, R. W. 1978Neonatal ultrasounds elicited by odor cuesDev. Psychobiol.11193197CrossRefPubMedGoogle Scholar
  18. Cuomo, V., Cagiano, R., Renna, G., De Salvia, M. A., Racangi, G. 1987Ultrasonic vocalization in rat pups: effects of early postnatal exposure to SCH23390 (a DA1-receptor antagonist) and sulpiride (a DA2-receptor antagonist)Neuropharmacology26701705CrossRefPubMedGoogle Scholar
  19. D’Amato, F. R., Moles, A. 2001Ultrasonic vocalizations as an index of social memory in female miceBehav. Neurosci.115834840CrossRefPubMedGoogle Scholar
  20. D’Amato, F. R., Populin, R. 1987Mother-offspring interaction and pup development in genetically deaf miceBehav. Genet.17465475PubMedGoogle Scholar
  21. D’Udine, B., Robinson, D. J., Oliverio, A. 1982An analysis of single-gene effects on audible and ultrasonic vocalizations in the mouseBehav. Neurol. Biol.36197203CrossRefGoogle Scholar
  22. Egorova, M. A., Ehret, G 1994Ultrasound production of mouse pups is affected by dopamine agonists (apomorphine) and antagonists (haloperidol)Elsner, H.Breer, N. eds. Sensory TransductionThiemeStuttgart770Google Scholar
  23. Ehret, G. 1974Age-dependent hearing loss in normal hearing miceNaturwissenschaften61506507CrossRefPubMedGoogle Scholar
  24. Ehret, G. 1975Schallsignale der Hausmaus (Mus musculus)Behaviour523856Google Scholar
  25. Ehret, G. 1980Development of sound communication in mammalsAdv. Study Behav.11179225CrossRefGoogle Scholar
  26. Ehret, G 1983aAuditory processing and perception of ultrasound in house miceEwert, J. P.Capranica, R. R.Ingle, D. J. eds. Advances in Vertebrate NeuroethologyPlenum PressNew York911918Google Scholar
  27. Ehret, G. 1983bPsychophysicsWillott, J. F. eds. The Auditory Psychobiology of the MouseThomasSpringfieldIl.1356Google Scholar
  28. Ehret, G. 1987aLeft hemisphere advantage in the mouse brain for ultrasound recognition in a communicative contextNature.325249251CrossRefGoogle Scholar
  29. Ehret, G. 1987bCategorical perception of sound signals: facts and hypotheses from animal studiesHamad, S. eds. Categorical PerceptionCambridge University PressCambridge301331Google Scholar
  30. Ehret, G 1992aCategorical perception of mouse-pup ultra sounds in the temporal domainAnim. Behav.43409416Google Scholar
  31. Ehret, G. 1992bPreadaptations in the auditory system of mammals for phoneme perceptionSchouten, M. E. H. eds. The Auditory Processing of Speech: From Sounds to WordsMouton de GruyterBerlin99112Google Scholar
  32. Ehret, G., Buckenmaier, J. 1994Estrogen-receptor occurrence in the female mouse brain: effects of maternal experienceovariectomy, estrogen and anosmiaJ. Physiol. Paris88315329CrossRefPubMedGoogle Scholar
  33. Ehret, G., Haack, B. 1981Categorical perception of mouse pup ultrasound by lactating femalesNaturwissenschaften68208209CrossRefPubMedGoogle Scholar
  34. Ehret, G., Haack, B. 1982Ultrasound recognition in house mice: Key-stimulus configuration and recognition mechanismsJ. Comp. Physiol.A148245251CrossRefGoogle Scholar
  35. Ehret, G., Haack, B. 1984Motivation and arousal influence sound-induced maternal pup-retrieving behavior in lactating house miceZ. Tierpsychol.652539Google Scholar
  36. Ehret, G., Jürgens, A., Koch, M. 1993Oestrogen-receptor occurrence in the male mouse brain : modulation by panal experienceNeuroReport412471250PubMedGoogle Scholar
  37. Ehret, G., Koch, M. 1989Ultrasound-induced parental behaviour in house mice is controlled by female sex hormones and parental experienceEthology808193CrossRefGoogle Scholar
  38. Ehret, G., Koch, M., Markl, H., Haack, B. 1987Sex and parental experience determine the onset of an instinctive behavior in miceNaturwissenschaften7447CrossRefPubMedGoogle Scholar
  39. Ehret, G., Merzenich, M. M. 1985Auditory midbrain responses parallel spectral integration phenomenaScience22712451247PubMedGoogle Scholar
  40. Ehret, G., Merzenich, M. M. 1988Complex sound analysis (frequency resolution, filtering and spectral integration) by single units of the inferior colliculus of the catBrain Res. Revs.13139163CrossRefGoogle Scholar
  41. Ehret, G., Schreiner, C. E. 2005Spectral and intensity codingWiner, J. A.Schreiner, C. E. eds. The Inferior ColliculusSpringer-VerlagNew-Yorkin pressGoogle Scholar
  42. Elwood, R. W., Keeling, F. 1982Temporal organization of ultrasonic vocalizations in infant miceDev. Psychobiol.15221227CrossRefPubMedGoogle Scholar
  43. Geissler, D. B., Ehret, G. 2002Time-critical formant integration of formants for perception of communication calls in miceProc. Natl. Acad. Sci. USA.9990219025CrossRefPubMedGoogle Scholar
  44. Geyer, L. A. 1979Olfactory and thermal influences on ultrasonic vocalization during development in rodentsAm. Zool.19420431Google Scholar
  45. Graham, M., Letz, R. 1979Within-species variation in the development of ultrasonic signaling of pre weaning ratsDev. Psychobiol.12129136CrossRefPubMedGoogle Scholar
  46. Gray, J. A. 1995A model of the limbic system and basal ganglia: applications to anxiety and schizophreniaGazzaniga, M. S. eds. The Cognitive NeurosciencesMIT PressCambridgeMass11651176Google Scholar
  47. Haack, B., Markl, H., Ehret, G. 1983Sound communication between parents and offspringWillott, J. F. eds. The Auditory Psychobiology of the MouseThomasSpringfieldIL5797Google Scholar
  48. Hahn, M. E., Benno, R. H., Schanz, N., Phadia, E. 2000The effects of prenatal cocaine exposure and genotype on the ultrasonic calls of infant micePharmacol. Biochem. Behav.67729738CrossRefPubMedGoogle Scholar
  49. Hahn, M. E., Hewitt, J. K., Adams, M., Tully, T. 1987Genetic influences on ultrasonic vocalizations in young miceBehav. Genet.17155166PubMedGoogle Scholar
  50. Hahn, M. E., Hewitt, J. K., Schanz, N., Weinreb, L., Henry, A. 1997Genetic and developmental influences of infant mouse ultrasonic calling – I. A diallel analysis of the calls of 3-day oldsBehav. Genet.27133143CrossRefPubMedGoogle Scholar
  51. Hahn, M. E., Karkowski, L., Weinreb, L., Henry, A., Schanz, N. 1998Genetic and developmental influences on infant mouse ultrasonic calling. II. Developmental patterns in the calls of mice 2–12 days of ageBehav. Genet.82315325CrossRefGoogle Scholar
  52. Hahn, M. E., Schanz, N. 2002The effects of coldrotation, and genotype on the production of ultrasonic calls in infant miceBehav. Genet.32267273CrossRefPubMedGoogle Scholar
  53. Hofer, M. A. 1996Multiple regulators of ultrasonic vocalization in the infant ratPsychoneuroendocrinology21203217CrossRefPubMedGoogle Scholar
  54. Hofer, M. A., Shair, H. N. 1978Ultrasonic vocalization during social interaction and isolation in 2-week-old ratsDev. Psychobiol.11495504CrossRefPubMedGoogle Scholar
  55. Hofer, M. A., Shair, H. N. 1987Isolation distress in two-week-old rats: influence of home cagesocial companions, and prior experience with littermatesDev. Psychobiol.20465476CrossRefPubMedGoogle Scholar
  56. Hofer, M. A., Shair, H. N. 1992Ultrasonic vocalization by rat pups during recovery from deep hypothermiaDev. Psychobiol.25511528CrossRefPubMedGoogle Scholar
  57. Hofer, M. A., Shair, H. N. 1993Ultrasonic vocalization, laryngal braking and thermogenesis in rat pups: a reappraisalBehav. Neurosci.107354362CrossRefPubMedGoogle Scholar
  58. Hofer, M.A., Shair, H. N., Masmela, J. R., Brunelli, S. 2001Developmental effects of selective breeding for an infantile trait: the rat pup ultrasonic isolation callDev. Psychobiol.39231246CrossRefPubMedGoogle Scholar
  59. Hunt, L.E., Smotherman, W.P., Wiener, S.G., Levine, S. 1976Nutritional variables and their effect on the development of ultrasonic vocalizations in rat pupsPhysiol. Behav.1710371039CrossRefPubMedGoogle Scholar
  60. Jürgens, U. 1979Vocalization as emotional indicator. A neuroethological study in the squirrel monkeyBehaviour.6988117PubMedGoogle Scholar
  61. Jürgens, U. 2002Neural pathways underlying vocal controlNeurosci. Biobehav. Revs.26235258CrossRefGoogle Scholar
  62. Kerchner, M., Vatza, E. J., Nyby, J. 1986Ultrasonic vocalizations by male house mice (Mus musculus) to novel odors: roles of infant and adult experienceJ. Comp. Psychol.100253261CrossRefPubMedGoogle Scholar
  63. Koch, M. 1990Effects of treatement with estradiol and parental experience on the number and distribution of estrogen-binding neurons in the ovariectomized mouse brainNeuroendocrinology.51505514PubMedGoogle Scholar
  64. Koch, M., Ehret, G. 1989Estradiol and parental experiencebut not prolactin are necessary for ultrasound recognition and pup-retrieving in the mousePhysiol. Behav.45771776CrossRefPubMedGoogle Scholar
  65. Koch, M., Ehret, G. 1991Parental behavior in the mouse : effects of lesions in the entorhinal/piriform cortexBehav. Brain Res.4299105PubMedGoogle Scholar
  66. Kopp, C., Vogel, E., Misslin, R. 1999Comparative study of emotional behaviour in three inbred strains of miceBehav. Proc.47161174CrossRefGoogle Scholar
  67. Knutson, B., Burgdorf, J., Panksepp, J. 1998Anticipation of play elicits high-frequency ultrasonic vocalizations in young ratsJ. Comp. Psychol.1126573CrossRefPubMedGoogle Scholar
  68. Knutson, B., Burgdorf, J., Panksepp, J. 1999High-frequency ultrasonic vocalizations index conditioned pharmacological reward in ratsPhysiol. Behav.66639643CrossRefPubMedGoogle Scholar
  69. Liu, R. C., Miller, K. D., Merzenich, M. M., Schreiner, C. E. 2003Acoustic variability and distinguishability among mouse ultrasound vocalizationsJ. Acoust. Soc. Am.11434123422CrossRefPubMedGoogle Scholar
  70. Lorenz, K. 1978Vergleichende Verhaltensforschung: Grundlagen der EthologieSpringer-VerlagWienGoogle Scholar
  71. Maggio, J. C., Whitney, G. 1985Ultrasonic vocalizing by adult female mice (Mus musculus)J. Comp. Psychol.99420436CrossRefPubMedGoogle Scholar
  72. Marchlewska-Koj, A., Olejniczak, J., Kapusta, P. 1999Ultrasonic response of CBA newborn mice to bedding odourBehaviour136269278CrossRefGoogle Scholar
  73. Naito, H., Tonoue, T. 1987Sex difference in ultrasound distress call by rat pupsBehav. Brain Res.251321CrossRefPubMedGoogle Scholar
  74. Nieuwenhuys, R., Voogd, J., van Huijzen, C. 1981The Human Central Nervous System2nd edSpringerBerlinGoogle Scholar
  75. Noirot, E. 1972Ultrasounds and maternal behavior in small rodentsDev. Psychobiol.5371387CrossRefPubMedGoogle Scholar
  76. Noirot, E., Pye, D. 1969Sound analysis of ultrasonic distress calls of mouse pups as a function of their ageAnim. Behav.17340349CrossRefGoogle Scholar
  77. Numan, M., Sheehan, T. P. 1997Neuroanatomical circuitry for mammalian maternal behaviorAnn. NY. Acad. Sci..807101125PubMedGoogle Scholar
  78. Okon, E.E. 1970The effect of environmental temperature on the production of ultrasounds by isolated non-handled albino mouse pupsJ. Zool. Lond.1627183Google Scholar
  79. Okon, E. E. 1972Factors affecting ultrasound production in infant rodentsJ. Zool.168139148Google Scholar
  80. Olivier, B., Molewijk, H. E., der Heyden, J. A. M., van Oorschot, R., Ronken, E., Mos, J., Miczek, K. A. 1998Ultrasonic vocalizations in rat pups: effects of serotonergic ligandsNeurosci. Biobehav. Revs.23215227CrossRefGoogle Scholar
  81. Oswalt, G. L., Meier, G. W. 1975Olfactory, thermal, and tactual influences on infantile ultrasonic vocalization in ratsDev. Psychobiol.8129135CrossRefPubMedGoogle Scholar
  82. Reisert, I., Karolczak, M., Beyer, C., Just, W., Maxson, S., Ehret, G. 2002Sry does not fully sex-reverse female into male behavior towards pupsBehav. Genet.32103111CrossRefPubMedGoogle Scholar
  83. Robinson, D. J., D’Udine, B. 1982Ultrasonic calls produced by three laboratory strains of Mus musculusJ. Zool. Lond.197383389Google Scholar
  84. Roubertoux, P. L., Martin, B., LeRoi, I., Beau, J., Marchaland, C., Perez-Diaz, F., Cohen Salmon, C., Carlier, M. 1996Vocalizations in newborn mice: genetic analysisBehav. Genet.26427437PubMedGoogle Scholar
  85. Sales, G. D. 1972Ultrasound and aggressive behaviour in rats and other small mammalsAnim. Behav.2088100PubMedGoogle Scholar
  86. Sales, G. D. 1979Strain differences in the ultrasonic behavior of rats (Rattus norvergicus)Am. Zool.19513527Google Scholar
  87. Sales, G. D., Pye, D. 1974Ultrasonic Communication in AnimalsChapman & HallLondonGoogle Scholar
  88. Sales, G. D., Skinner, N. C. 1979The effect of ambient temperature on body temperature and on ultrasonic behaviour in litters of albino laboratory mice deprived of their mothersJ. Zool. Lond.187265281CrossRefGoogle Scholar
  89. Sales, G. D., Smith, J. C. 1978Comparative studies of the ultrasonic calls of infant murid rodentsDev. Psychobiol.11595619CrossRefPubMedGoogle Scholar
  90. Santucci, D., Masterson, D., Elwood, R. W. 1994Effects of agesex, and odours from conspecific adult males on ultrasonic vocalizations of infant CS1 miceBehav. Proc.32285296CrossRefGoogle Scholar
  91. Schreiner, C. E., Langner, G. 1997Laminar fme structure of frequency organization in auditory midbrainNature388383386CrossRefPubMedGoogle Scholar
  92. Sewell, G. D. 1970Ultrasonic communication in rodentsNature227410PubMedGoogle Scholar
  93. Smith, J. C. 1975Sound communication in rodentsSymp. Zool. Soc. Lond.37317330Google Scholar
  94. Smith, J. C. 1976Responses of adult mice to models of infant callsJ. Comp. Physiol. Psychol.9011051115Google Scholar
  95. Smith, J. C., Sales, G. D. 1980Ultrasonic behavior and mother-infant interactions in rodentsBell, R. W.Smotherman, W. P. eds. Maternal Influences and Early BehaviorSpectrum PressNew York105133Google Scholar
  96. Smotherman, W. P., Wiener, S. G., Levine, S. 1976Nutritional variables and their effect on the development of ultrasonic vocalizations in rat pupsPhysiol. Behav.1710371039CrossRefPubMedGoogle Scholar
  97. Späth, K. E., Ehret, G. 1994Influence of the serotonergic system on ultrasound production in mouse pupsElsner, N.Breer, H. eds. Sensory TransductionThiemeStuttgart770Google Scholar
  98. Suchecki, D., Nelson, D. Y., van Oers, H., Levine, S. 1995Activation and inhibition of the hypothalamic-pituitary-adrenal axis of the neonatal rat: effects of maternal deprivationPsychoneuroendocrinology20169182CrossRefPubMedGoogle Scholar
  99. Tinbergen, N. 1972The Study of Instinct5th edOxford University PressLondonGoogle Scholar
  100. Wegener, S., Schmidt, W. J., Ehret, G. 1988Haloperidol–and apomorphine – induced changes in pup searching behaviour of house micePsychopharmacology95271275CrossRefPubMedGoogle Scholar
  101. Weller, A., Leguisamo, A. C., Towns, L., Ramboz, S., Bagiella, E., Hofer, M. A., Hen, R., Brunner, D. 2001Maternal effects in infant and adult phenotypes of 5HT1Aand 5HT lB receptor knockout miceDev. Psychobiol.42194205CrossRefGoogle Scholar
  102. Whitney, G., Nyby, J. 1983Sound communication among adultsWillott, J. F. eds. The Auditory Psychobiology of the MouseThomasSpringfieldIL98129Google Scholar
  103. Winslow, J. T., Hearn, E. F., Ferguson, J., Young, L. J., Matzuk, M. M., Insel, T. R. 2000Infant vocalization, adult aggression and fear behavior of an oxytocin null mutant mouseHorm. Behav.37145155PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, Inc. 2005

Authors and Affiliations

  1. 1.Department of NeurobiologyUniversity of UlmUlmGermany

Personalised recommendations