Advertisement

Why the Caged Mouse Sings: Studies of the Mouse Ultrasonic Song System and Vocal Behavior

  • Gustavo Arriaga
Chapter

Abstract

Laboratory rodents participate in a significant amount of communication using ultrasonic vocalizations (USVs), and two types of USVs have been studied extensively as measures of internal states: pup isolation calls; and adult USVs in aversive, rewarding or social conditions. Mouse (Mus musculus) USVs do not appear to signal affect but are used primarily during non-aggressive social encounters and may facilitate social interactions. The most well characterized adult mouse USVs are those produced by males when they detect the presence of a sexually mature female and after copulation. Although the general occurrence of these male mouse USVs has been known for decades, in depth analyses of their spectro-temporal and syntactic features and the supporting neural substrate have only recently begun. Nevertheless, the field of mouse ultrasonic vocal communication is advancing rapidly on multiple fronts: discoveries at the molecular level; initial descriptions of the neural systems for vocal production and control; characterization of mouse models of social communication disorders and neuropsychiatric dysfunction; and ethological perspectives on the social function of ultrasonic communication in mice. As the mechanisms of mouse USV production become better understood, it is becoming possible to employ mouse vocalizations for purposes of behavioral phenotyping in mouse models of various neurological disorders and investigating the basic mechanisms of neural control of social communication in mammals. This chapter will describe some of the recent findings related to mouse vocal communication, with an emphasis on adult ultrasounds, and discuss the current interpretations and potential opportunities for advances in the field.

Keywords

Vocal Behavior Male Song Vocal Communication Nucleus Ambiguus Syllable Type 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

References

  1. Arnold K, Zuberbühler K (2008) Meaningful call combinations in a non-human primate. Curr Biol 18:R202–R203. doi: 10.1016/j.cub.2008.01.040 PubMedGoogle Scholar
  2. Arriaga G, Jarvis ED (2013) Mouse vocal communication system: are ultrasounds learned or innate? Brain Lang 124:96. doi: 10.1016/j.bandl.2012.10.002 PubMedGoogle Scholar
  3. Arriaga G, Zhou EP, Jarvis ED (2012) Of mice, birds, and men: the mouse ultrasonic song system has some features similar to humans and song-learning birds. PLoS One 7:e46610. doi: 10.1371/journal.pone.0046610 PubMedGoogle Scholar
  4. Barnes TD, Kubota Y, Hu D et al (2005) Activity of striatal neurons reflects dynamic encoding and recoding of procedural memories. Nature 437:1158–1161. doi: 10.1038/nature04053 PubMedGoogle Scholar
  5. Bean NJ (1982) Olfactory and vomeronasal mediation of ultrasonic vocalizations in male mice. Physiol Behav 28:31–37. doi: 10.1016/0031-9384(82)90097-X PubMedGoogle Scholar
  6. Berquist SW, Ho JP, Metzner W (2010) Sound production in the isolated mouse larynx. In: Society for Neuroscience annual meeting, San DiegoGoogle Scholar
  7. Brainard MS, Doupe AJ (2000) Interruption of a basal ganglia-forebrain circuit prevents plasticity of learned vocalizations. Nature 404:762–766. doi: 10.1038/35008083 PubMedGoogle Scholar
  8. Branchi I, Santucci D, Alleva E (2001) Ultrasonic vocalisation emitted by infant rodents: a tool for assessment of neurobehavioural development. Behav Brain Res 125:49–56PubMedGoogle Scholar
  9. Brecht M, Krauss A, Muhammad S et al (2004) Organization of rat vibrissa motor cortex and adjacent areas according to cytoarchitectonics, microstimulation, and intracellular stimulation of identified cells. J Comp Neurol 479:360–373. doi: 10.1002/cne.20306 PubMedGoogle Scholar
  10. Broughton WP (1963) Acoustic behavior of animals. Elsevier, BostonGoogle Scholar
  11. Brown S, Ngan E, Liotti M (2008) A larynx area in the human motor cortex. Cereb Cortex 18:837–845. doi: 10.1093/cercor/bhm131 PubMedGoogle Scholar
  12. Brudzynski SM (2007) Ultrasonic calls of rats as indicator variables of negative or positive states: acetylcholine-dopamine interaction and acoustic coding. Behav Brain Res 182:261–273. doi: 10.1016/j.bbr.2007.03.004 PubMedGoogle Scholar
  13. Brudzynski SM (2009) Communication of adult rats by ultrasonic vocalization: biological, sociobiological, and neuroscience approaches. ILAR J 50:43–50PubMedGoogle Scholar
  14. Brudzynski SM, Kehoe P, Callahan M (1999) Sonographic structure of isolation-induced ultrasonic calls of rat pups. Dev Psychobiol 34:195–204PubMedGoogle Scholar
  15. Burgdorf J, Wood PL, Kroes RA et al (2007) Neurobiology of 50-kHz ultrasonic vocalizations in rats: electrode mapping, lesion, and pharmacology studies. Behav Brain Res 182:274–283PubMedGoogle Scholar
  16. Campbell P, Reep RL, Stoll ML et al (2009) Conservation and diversity of Foxp2 expression in muroid rodents: functional implications. J Comp Neurol 512:84–100. doi: 10.1002/cne.21881 PubMedGoogle Scholar
  17. Chabout J, Serreau P, Ey E et al (2012) Adult male mice emit context-specific ultrasonic vocalizations that are modulated by prior isolation or group rearing environment. PLoS One 7:e29401. doi: 10.1371/journal.pone.0029401 PubMedGoogle Scholar
  18. Constantini F, D’Amato FR (2006) Ultrasonic vocalizations in mice and rats: social contexts and functions. Acta Zool Sin 52:619–633Google Scholar
  19. Coudé G, Ferrari PF, Rodà F et al (2011) Neurons controlling voluntary vocalization in the macaque ventral premotor cortex. PLoS One 6:e26822. doi: 10.1371/journal.pone.0026822 PubMedGoogle Scholar
  20. D’Amato FR, Scalera E, Sarli C, Moles A (2005) Pups call, mothers rush: does maternal responsiveness affect the amount of ultrasonic vocalizations in mouse pups? Behav Genet 35:103–112PubMedGoogle Scholar
  21. Deacon TW (2007) The evolution of language systems in the human brain. In: Kaas J (ed) Evolution of nervous systems. Elsevier, Amsterdam, pp 529–547Google Scholar
  22. Depaulis A, Keay KA, Bandler R (1992) Longitudinal neuronal organization of defensive reactions in the midbrain periaqueductal gray region of the rat. Exp Brain Res 90:307–318PubMedGoogle Scholar
  23. Dirks A, Fish EW, Kikusui T et al (2002) Effects of corticotropin-releasing hormone on distress vocalizations and locomotion in maternally separated mouse pups. Pharmacol Biochem Behav 72:993–999PubMedGoogle Scholar
  24. Doupe AJ, Kuhl PK (1999) Birdsong and human speech: common themes and mechanisms. Annu Rev Neurosci 22:567–631. doi: 10.1146/annurev.neuro.22.1.567 PubMedGoogle Scholar
  25. Dujardin E, Jürgens U (2005) Afferents of vocalization-controlling periaqueductal regions in the squirrel monkey. Brain Res 1034:114–131. doi: 10.1016/j.brainres.2004.11.048 PubMedGoogle Scholar
  26. Düsterhöft F, Häusler U, Jürgens U (2003) Neuronal activity in the periaqueductal gray and bordering structures during vocal communication in the squirrel monkey. Neuroscience 123:53–60Google Scholar
  27. Ehret G (1976) Development of absolute auditory thresholds in the house mouse (Mus musculus). J Am Audiol Soc 1:179–184PubMedGoogle Scholar
  28. El-Kordi A, Winkler D, Hammerschmidt K et al (2012) Development of an autism severity score for mice using Nlgn4 null mutants as a construct-valid model of heritable monogenic autism. Behav Brain Res. doi: 10.1016/j.bbr.2012.11.016 PubMedGoogle Scholar
  29. Elwood RW, Keeling F (1982) Temporal organization of ultrasonic vocalizations in infant mice. Dev Psychobiol 15:221–227PubMedGoogle Scholar
  30. Enard W, Gehre S, Hammerschmidt K et al (2009) A humanized version of Foxp2 affects cortico-basal ganglia circuits in mice. Cell 137:961–971. doi: 10.1016/j.cell.2009.03.041 PubMedGoogle Scholar
  31. Ennis M, Xu S-J, Rizvi TA et al (1997) Discrete subregions of the rat midbrain periaqueductal gray project to nucleus ambiguus and the periambigual region. Neuroscience 80:829–845PubMedGoogle Scholar
  32. Fischer J, Hammerschmidt K (2010) Ultrasonic vocalizations in mouse models for speech and socio-cognitive disorders: insights into the evolution of vocal communication. Genes Brain Behav 10:17–27. doi: 10.1111/j.1601-183X.2010.00610.x Google Scholar
  33. Fish EW, Sekinda M, Ferrari PF et al (2000) Distress vocalizations in maternally separated mouse pups: modulation via 5-HT1A, 5-HT1B and GABAA receptors. Psychopharmacology 149:277–285PubMedGoogle Scholar
  34. Fish EW, Faccidomo S, Gupta S, Miczek KA (2004) Anxiolytic-like effects of escitalopram, citalopram, and R-citalopram in maternally separated mouse pups. J Pharmacol Exp Ther 308:474–480PubMedGoogle Scholar
  35. Fitch WT, Huber L, Bugnyar T (2010) Social cognition and the evolution of language: constructing cognitive phylogenies. Neuron 65:795–814. doi: 10.1016/j.neuron.2010.03.011 PubMedGoogle Scholar
  36. French CA, Groszer M, Preece C et al (2007) Generation of mice with a conditional Foxp2 null allele. Genesis 45:440–446. doi: 10.1002/dvg.20305 PubMedGoogle Scholar
  37. Frysztak RJ, Neafsey EJ (1991) The effect of medial frontal cortex lesions on respiration, “freezing”, and ultrasonic vocalizations during conditioned emotional responses in rats. Cereb Cortex 1:418–425PubMedGoogle Scholar
  38. Fujita E, Tanabe Y, Shiota A et al (2008) Ultrasonic vocalization impairment of Foxp2 (R552H) knockin mice related to speech-language disorder and abnormality of Purkinje cells. Proc Natl Acad Sci USA 105:3117–3122. doi: 10.1073/pnas.0712298105 PubMedGoogle Scholar
  39. Gaub S, Groszer M, Fisher SE, Ehret G (2010) The structure of innate vocalizations in Foxp2-deficient mouse pups. Genes Brain Behav 9:390–401. doi: 10.1111/j.1601-183X.2010.00570.x PubMedGoogle Scholar
  40. Gourbal BEF, Barthelemy M, Petit G, Gabrion C (2004) Spectrographic analysis of the ultrasonic vocalisations of adult male and female BALB/c mice. Naturwissenschaften 91:381–385. doi: 10.1007/s00114-004-0543-7 PubMedGoogle Scholar
  41. Graybiel AM (2005) The basal ganglia: learning new tricks and loving it. Curr Opin Neurobiol 15:638–644. doi: 10.1016/j.conb.2005.10.006 PubMedGoogle Scholar
  42. Grimsley JMS, Monaghan JJM, Wenstrup JJ (2011) Development of social vocalizations in mice. PLoS One 6:e17460. doi: 10.1371/journal.pone.0017460 PubMedGoogle Scholar
  43. Groszer M, Keays DA, Deacon RMJ et al (2008) Impaired synaptic plasticity and motor learning in mice with a point mutation implicated in human speech deficits. Curr Biol 18:354–362. doi: 10.1016/j.cub.2008.01.060 PubMedGoogle Scholar
  44. Guo Z, Holy TE (2007) Sex selectivity of mouse ultrasonic songs. Chem Senses 32:463–473. doi: 10.1093/chemse/bjm015 PubMedGoogle Scholar
  45. Gyger MG, Marler P, Pickert R (1987) Semantics of an avian alarm call system: the male domestic fowl, Gallus domesticus. Behaviour 102:15–39. doi: 10.1163/156853986X00027 Google Scholar
  46. Haesler S, Wada K, Nshdejan A et al (2004) FoxP2 expression in avian vocal learners and non-learners. J Neurosci 24:3164–3175. doi: 10.1523/JNEUROSCI.4369-03.2004 PubMedGoogle Scholar
  47. Haesler S, Rochefort C, Georgi B et al (2007) Incomplete and inaccurate vocal imitation after knockdown of FoxP2 in songbird basal ganglia nucleus Area X. PLoS Biol 5:e321. doi: 10.1371/journal.pbio.0050321 PubMedGoogle Scholar
  48. Hage SR, Jürgens U (2006a) Localization of a vocal pattern generator in the pontine brainstem of the squirrel monkey. Eur J Neurosci 23:840–844. doi: 10.1111/j.1460-9568.2006.04595.x PubMedGoogle Scholar
  49. Hage SR, Jürgens U (2006b) On the role of the pontine brainstem in vocal pattern generation: a telemetric single-unit recording study in the squirrel monkey. J Neurosci 26:7105–7115. doi: 10.1523/JNEUROSCI.1024-06.2006 PubMedGoogle Scholar
  50. Hahn ME, Hewitt JK, Adams M, Trully T (1987) Genetic influences on ultrasonic vocalizations in young mice. Behav Genet 17:155–166PubMedGoogle Scholar
  51. Hammerschmidt K, Radyushkin K, Ehrenreich H, Fischer J (2009) Female mice respond to male ultrasonic “songs” with approach behaviour. Biol Lett 5:589–592. doi: 10.1098/rsbl.2009.0317 PubMedGoogle Scholar
  52. Hammerschmidt K, Radyushkin K, Ehrenreich H, Fischer J (2012a) The structure and usage of female and male mouse ultrasonic vocalizations reveal only minor differences. PLoS One 7:e41133. doi: 10.1371/journal.pone.0041133 PubMedGoogle Scholar
  53. Hammerschmidt K, Reisinger E, Westekemper K et al (2012b) Mice do not require auditory input for the normal development of their ultrasonic vocalizations. BMC Neurosci 13:40. doi: 10.1186/1471-2202-13-40 PubMedGoogle Scholar
  54. Hannig S, Jürgens U (2005) Projections of the ventrolateral pontine vocalization area in the squirrel monkey. Exp Brain Res 169:92–105. doi: 10.1007/s00221-005-0128-5 PubMedGoogle Scholar
  55. Hanson JL, Hurley LM (2012) Female presence and estrous state influence mouse ultrasonic courtship vocalizations. PLoS One 7:e40782. doi: 10.1371/journal.pone.0040782 PubMedGoogle Scholar
  56. Harmon KM, Cromwell HC, Burgdorf J et al (2008) Rats selectively bred for low levels of 50 kHz ultrasonic vocalizations exhibit alterations in early social motivation. Dev Psychobiol 50:322–331. doi: 10.1002/dev.20294 PubMedGoogle Scholar
  57. Harrison DFN (1995) The anatomy and physiology of the mammalian larynx. Cambridge University Press, CambridgeGoogle Scholar
  58. Heaton JT, Dooling RJ, Farabaugh SM (1999) Effects of deafening on the calls and warble song of adult budgerigars (Melopsittacus undulatus). J Acoust Soc Am 105:2010–2019PubMedGoogle Scholar
  59. Hofer MA, Shair HN (1992) Ultrasonic vocalization by rat pups during recovery from deep hypothermia. Dev Psychobiol 25:511–528. doi: 10.1002/dev.420250705 PubMedGoogle Scholar
  60. Hoffmann F, Musolf K, Penn DJ (2009) Freezing urine reduces its efficacy for eliciting ultrasonic vocalizations from male mice. Physiol Behav 96:602–605. doi: 10.1016/j.physbeh.2008.12.014 PubMedGoogle Scholar
  61. Hoffmann F, Musolf K, Penn DJ (2012) Spectrographic analyses reveal signals of individuality and kinship in the ultrasonic courtship vocalizations of wild house mice. Physiol Behav 105:766–771. doi: 10.1016/j.physbeh.2011.10.011 PubMedGoogle Scholar
  62. Holy TE, Guo Z (2005) Ultrasonic songs of male mice. PLoS Biol 3:e386. doi: 10.1371/journal.pbio.0030386 PubMedGoogle Scholar
  63. Holy TE, Dulac C, Meister M (2000) Responses of vomeronasal neurons to natural stimuli. Science 289:1569–1572PubMedGoogle Scholar
  64. Ise S, Ohta H (2009) Power spectrum analysis of ultrasonic vocalization elicited by maternal separation in rat pups. Brain Res 1283:58–64. doi: 10.1016/j.brainres.2009.06.003 PubMedGoogle Scholar
  65. Jamain S, Radyushkin K, Hammerschmidt K et al (2008) Reduced social interaction and ultrasonic communication in a mouse model of monogenic heritable autism. Proc Natl Acad Sci USA 105:1710–1715. doi: 10.1073/pnas.0711555105 PubMedGoogle Scholar
  66. Jarvis ED (2004) Learned birdsong and the neurobiology of human language. Ann NY Acad Sci 1016:749–777PubMedGoogle Scholar
  67. Jürgens U (1982) Afferents to the cortical larynx area in the monkey. Brain Res 239:377–389PubMedGoogle Scholar
  68. Jürgens U (1983) Afferent fibers to the cingular vocalization region in the squirrel monkey. Exp Neurol 80:395–409PubMedGoogle Scholar
  69. Jürgens U (1984) The efferent and afferent connections of the supplementary motor area. Brain Res 300:63–81PubMedGoogle Scholar
  70. Jürgens U (1998) Neuronal control of mammalian vocalization, with special reference to the squirrel monkey. Naturwissenschaften 85:376–388PubMedGoogle Scholar
  71. Jürgens U (2002a) Neural pathways underlying vocal control. Neurosci Biobehav R 26:235–258Google Scholar
  72. Jürgens U (2002b) A study of the central control of vocalization using the squirrel monkey. Med Eng Phys 24:473–477PubMedGoogle Scholar
  73. Jürgens U (2009) The neural control of vocalization in mammals: a review. J Voice 23:1–10. doi: 10.1016/j.jvoice.2007.07.005 PubMedGoogle Scholar
  74. Jürgens U, Alipour M (2002) A comparative study on the cortico-hypoglossal connections in primates, using biotin dextranamine. Neurosci Lett 328:245–248PubMedGoogle Scholar
  75. Jürgens U, Ehrenreich L (2007) The descending motorcortical pathway to the laryngeal motoneurons in the squirrel monkey. Brain Res 1148:90–95. doi: 10.1016/j.brainres.2007.02.020 PubMedGoogle Scholar
  76. Jürgens U, Ploog D (1970) Cerebral representation of vocalization in the squirrel monkey. Exp Brain Res 10:532–554PubMedGoogle Scholar
  77. Jürgens U, Pratt R (1979) Role of the periaqueductal grey in vocal expression of emotion. Brain Res 167:367–378PubMedGoogle Scholar
  78. Jürgens U, Kirzinger A, von Cramon D (1982) The effects of deep-reaching lesions in the cortical face area on phonation: a combined case report and experimental monkey study. Cortex 18:125–139PubMedGoogle Scholar
  79. Jürgens U, Ehrenreich L, de Lanerolle NC (2002) 2-Deoxyglucose uptake during vocalization in the squirrel monkey brain. Behav Brain Res 136:605–610PubMedGoogle Scholar
  80. Kang C, Drayna D (2011) Genetics of speech and language disorders. Annu Rev Genomics Hum Genet 12:145–164. doi: 10.1146/annurev-genom-090810-183119 PubMedGoogle Scholar
  81. Kao MH, Doupe AJ, Brainard MS (2005) Contributions of an avian basal ganglia-forebrain circuit to real-time modulation of song. Nature 433:638–643. doi: 10.1038/nature03127 PubMedGoogle Scholar
  82. Kaplan G (2008) Alarm calls and referentiality in Australian magpies: between midbrain and forebrain, can a case be made for complex cognition? Brain Res Bull 76:253–263. doi: 10.1016/j.brainresbull.2008.02.006 PubMedGoogle Scholar
  83. Karakashian SJ, Gyger MG, Marler P (1988) Audience effects on alarm calling in chickens (Gallus gallus). J Comp Psychol 102:129–135PubMedGoogle Scholar
  84. Kikusui T, Nakanishi K, Nakagawa R et al (2011) Cross fostering experiments suggest that mice songs are innate. PLoS One 6:e17721. doi: 10.1371/journal.pone.0017721 PubMedGoogle Scholar
  85. Kimchi T, Xu J, Dulac C (2007) A functional circuit underlying male sexual behaviour in the female mouse brain. Nature 448:1009–1014. doi: 10.1038/nature06089 PubMedGoogle Scholar
  86. Kirzinger A (1985) Cerebellar lesion effects on vocalization of the squirrel monkey. Behav Brain Res 16:177–181PubMedGoogle Scholar
  87. Kirzinger A, Jürgens U (1982) Cortical lesion effects and vocalization in the squirrel monkey. Brain Res 233:299–315PubMedGoogle Scholar
  88. Kirzinger A, Jürgens U (1985) The effects of brainstem lesions on vocalization in the squirrel monkey. Brain Res 358:150–162PubMedGoogle Scholar
  89. Knutson B, Burgdorf J, Panksepp J (2002) Ultrasonic vocalizations as indices of affective states in rats. Psychol Bull 128:961–977PubMedGoogle Scholar
  90. Kuypers H (1958) Some projections from the peri-central cortex to the pons and lower brain stem in monkey and chimpanzee. J Comp Neurol 110:221–255PubMedGoogle Scholar
  91. Lai CSL, Gerrelli D, Monaco AP et al (2003) FOXP2 expression during brain development coincides with adult sites of pathology in a severe speech and language disorder. Brain 126:2455–2462. doi: 10.1093/brain/awg247 PubMedGoogle Scholar
  92. Lu CL, Jürgens U (1993) Effects of chemical stimulation in the periaqueductal gray on vocalization in the squirrel monkey. Brain Res Bull 32:143–151PubMedGoogle Scholar
  93. Lüthe L, Häusler U, Jürgens U (2000) Neuronal activity in the medulla oblongata during vocalization. A single-unit recording study in the squirrel monkey. Behav Brain Res 116:197–210PubMedGoogle Scholar
  94. Mantyh PW (1983) Connections of midbrain periaqueductal gray in the monkey. I. Ascending efferent projections. J Neurophysiol 49:567–581PubMedGoogle Scholar
  95. Marler P, Sherman V (1983) Song structure without auditory feedback: emendations of the auditory template hypothesis. J Neurosci 3:517–531PubMedGoogle Scholar
  96. Marler P, Slabbekoorn H (2004) Nature’s music: the science of birdsong. Elsevier Academic Press, San DiegoGoogle Scholar
  97. Miller JE, Spiteri E, Condro MC et al (2008) Birdsong decreases protein levels of FoxP2, a molecule required for human speech. J Neurophysiol 100:2015–2025. doi: 10.1152/jn.90415.2008 PubMedGoogle Scholar
  98. Mizutani A, Matsuzaki A, Momoi MY et al (2007) Intracellular distribution of a speech/language disorder associated FOXP2 mutant. Biochem Biophys Res Commun 353:869–874. doi: 10.1016/j.bbrc.2006.12.130 PubMedGoogle Scholar
  99. Moles A, D’Amato FR (2000) Ultrasonic vocalization by female mice in the presence of a conspecific carrying food cues. Anim Behav 60:689–694. doi: 10.1006/anbe.2000.1504 PubMedGoogle Scholar
  100. Moles A, Costantini F, Garbugino L et al (2007) Ultrasonic vocalizations emitted during dyadic interactions in female mice: a possible index of sociability? Behav Brain Res 182:223–230. doi: 10.1016/j.bbr.2007.01.020 PubMedGoogle Scholar
  101. Müller-Preuss P, Jürgens U (1976) Projections from the “cingular” vocalization area in the squirrel monkey. Brain Res 103:29–43PubMedGoogle Scholar
  102. Müller-Preuss P, Newman JD, Jürgens U (1980) Anatomical and physiological evidence for a relationship between the “cingular” vocalization area and the auditory cortex in the squirrel monkey. Brain Res 202:307–315PubMedGoogle Scholar
  103. Musolf K, Hoffmann F, Penn DJ (2010) Ultrasonic courtship vocalizations in wild house mice, Mus musculus musculus. Anim Behav 79:757–764. doi: 10.1016/j.anbehav.2009.12.034 Google Scholar
  104. Noirot E (1972) Ultrasounds and maternal behavior in small rodents. Dev Psychobiol 5:371–387PubMedGoogle Scholar
  105. Noirot E, Pye D (1969) Sound analysis of ultrasonic distress calls of mouse pups as a function of their age. Anim Behav 17:340–349Google Scholar
  106. Nunez AA, Pomerantz SM, Bean NJ, Youngstrom TG (1985) Effects of laryngeal denervation on ultrasound production and male sexual behavior in rodents. Physiol Behav 34:901–905PubMedGoogle Scholar
  107. Nyby J (1983) Ultrasonic vocalizations during sex behavior of male house mice (Mus musculus): a description. Behav Neural Biol 39:128–134PubMedGoogle Scholar
  108. Okanoya K (2004) Functional and structural pre-adaptations to language: insight from comparative cognitive science into the study of language origin. Jpn Psychol Res 46:207–215Google Scholar
  109. Okanoya K, Yamaguchi A (1997) Adult Bengalese finches (Lonchura striata var. domestica) require real-time auditory feedback to produce normal song syntax. J Neurobiol 33:343–356PubMedGoogle Scholar
  110. Olivier B, Molewijk E, van Oorschot R et al (1994) New animal models of anxiety. Eur Neuropsychopharmacol 4:93–102PubMedGoogle Scholar
  111. Olveczky BP, Andalman AS, Fee MS (2005) Vocal experimentation in the juvenile songbird requires a basal ganglia circuit. PLoS Biol 3:e153. doi: 10.1371/journal.pbio.0030153 PubMedGoogle Scholar
  112. Portfors CV (2007) Types and functions of ultrasonic vocalizations in laboratory rats and mice. J Am Assoc Lab Anim 46:28–34Google Scholar
  113. Pronichev IC, Lenkov DN (1998) Functional mapping of the motor cortex in the white mouse by microstimulation. Neurosci Behav Physiol 28:80–85PubMedGoogle Scholar
  114. Radyushkin K, Hammerschmidt K, Boretius S et al (2009) Neuroligin-3-deficient mice: model of a monogenic heritable form of autism with an olfactory deficit. Genes Brain Behav 8:416–425. doi: 10.1111/j.1601-183X.2009.00487.x PubMedGoogle Scholar
  115. Reimers-Kipping S, Hevers W, Pääbo S, Enard W (2011) Humanized Foxp2 specifically affects cortico-basal ganglia circuits. Neuroscience 175:75–84. doi: 10.1016/j.neuroscience.2010.11.042 PubMedGoogle Scholar
  116. Riede T (2011) Subglottal pressure, tracheal airflow, and intrinsic laryngeal muscle activity during rat ultrasound vocalization. J Neurophysiol 106:2580–2592. doi: 10.1152/jn.00478.2011 PubMedGoogle Scholar
  117. Roberts LH (1975) Evidence for the laryngeal source of ultrasonic and audible cries of rodents. J Zool 175:243–257Google Scholar
  118. Rochefort C, He X, Scotto-Lomassese S, Scharff C (2007) Recruitment of FoxP2-expressing neurons to area X varies during song development. Dev Neurobiol 67:809–817. doi: 10.1002/dneu.20393 PubMedGoogle Scholar
  119. Romand R, Ehret G (1990) development of tonotopy in the inferior colliculus. I. Electrophysiological mapping in house mice. Dev Brain Res 54:221–234. doi: 10.1016/0165-3806(90)90145-O Google Scholar
  120. Sales GD, Smith JC (1978) Comparative studies of the ultrasonic calls of infant murid rodents. Dev Psychobiol 11:595–619PubMedGoogle Scholar
  121. Scattoni ML, Gandhy SU, Ricceri L, Crawley JN (2008a) Unusual repertoire of vocalizations in the BTBR T + tf/J mouse model of autism. PLoS One 3:e3067. doi: 10.1371/journal.pone.0003067 PubMedGoogle Scholar
  122. Scattoni ML, McFarlane HG, Zhodzishsky V et al (2008b) Reduced ultrasonic vocalizations in vasopressin 1b knockout mice. Behav Brain Res 187:371–378. doi: 10.1016/j.bbr.2007.09.034 PubMedGoogle Scholar
  123. Scattoni ML, Crawley JN, Ricceri L (2009) Ultrasonic vocalizations: a tool for behavioural phenotyping of mouse models of neurodevelopmental disorders. Neurosci Biobehav R 33:508–515. doi: 10.1016/j.neubiorev.2008.08.003 Google Scholar
  124. Seyfarth RM, Cheney DL, Marler P (1980) Monkey responses to three different alarm calls: evidence of predator classification and semantic communication. Science 210:801–803PubMedGoogle Scholar
  125. Shiba K, Umezaki T, Zheng Y, Miller AD (1997) The nucleus retroambigualis controls laryngeal muscle activity during vocalization in the cat. Exp Brain Res 115:513–519PubMedGoogle Scholar
  126. Shu W, Cho JY, Jiang Y et al (2005) Altered ultrasonic vocalization in mice with a disruption in the Foxp2 gene. Proc Natl Acad Sci USA 102:9643–9648. doi: 10.1073/pnas.0503739102 PubMedGoogle Scholar
  127. Siebert S, Jürgens U (2003) Vocalization after periaqueductal grey inactivation with the GABA agonist muscimol in the squirrel monkey. Neurosci Lett 340:111–114PubMedGoogle Scholar
  128. Simões CS, Vianney PVR, de Moura MM et al (2010) Activation of frontal neocortical areas by vocal production in marmosets. Front Integr Neurosci. doi: 10.3389/fnint.2010.00123 PubMedGoogle Scholar
  129. Simonyan K, Horwitz B (2011) Laryngeal motor cortex and control of speech in humans. Neuroscientist 17:197–208. doi: 10.1177/1073858410386727 PubMedGoogle Scholar
  130. Simonyan K, Jürgens U (2002) Cortico-cortical projections of the motorcortical larynx area in the rhesus monkey. Brain Res 949:23–31PubMedGoogle Scholar
  131. Simonyan K, Jürgens U (2003) Efferent subcortical projections of the laryngeal motorcortex in the rhesus monkey. Brain Res 974:43–59PubMedGoogle Scholar
  132. Simonyan K, Jürgens U (2004) Afferent subcortical connections into the motor cortical larynx area in the rhesus monkey. Neuroscience 130:119–131. doi: 10.1016/j.neuroscience.2004.06.071 Google Scholar
  133. Simonyan K, Jürgens U (2005) Afferent cortical connections of the motor cortical larynx area in the rhesus monkey. Neuroscience 130:133–149. doi: 10.1016/j.neuroscience.2004.08.031 PubMedGoogle Scholar
  134. Simpson HB, Vicario DS (1990) Brain pathways for learned and unlearned vocalizations differ in zebra finches. J Neurosci 10:1541–1556PubMedGoogle Scholar
  135. Stowers L, Holy TE, Meister M et al (2002) Loss of sex discrimination and male-male aggression in mice deficient for TRP2. Science 295:1493–1500. doi: 10.1126/science.1069259 PubMedGoogle Scholar
  136. Teramitsu I, White SA (2006) FoxP2 regulation during undirected singing in adult songbirds. J Neurosci 26:7390–7394. doi: 10.1523/JNEUROSCI.1662-06.2006 PubMedGoogle Scholar
  137. Thomas LB, Stemple JC, Andreatta RD, Andrade FH (2009) Establishing a new animal model for the study of laryngeal biology and disease: an anatomic study of the mouse larynx. J Speech Lang Hear Res 52:802–811PubMedGoogle Scholar
  138. Thompson RN, Robertson BK, Napier A, Wekesa KS (2004) Sex-specific responses to urinary chemicals by the mouse vomeronasal organ. Chem Senses 29:749–754. doi: 10.1093/chemse/bjh076 PubMedGoogle Scholar
  139. Thoms G, Jürgens U (1987) Common input of the cranial motor nuclei involved in phonation in squirrel monkey. Exp Neurol 95:85–99PubMedGoogle Scholar
  140. Uematsu A, Kikusui T, Kihara T et al (2007) Maternal approaches to pup ultrasonic vocalizations produced by a nanocrystalline silicon thermo-acoustic emitter. Brain Res 1163:91–99. doi: 10.1016/j.brainres.2007.05.056 PubMedGoogle Scholar
  141. Vernes SC, Nicod J, Elahi FM et al (2006) Functional genetic analysis of mutations implicated in a human speech and language disorder. Hum Mol Genet 15:3154–3167. doi: 10.1093/hmg/ddl392 PubMedGoogle Scholar
  142. Waldstein RS (1990) Effects of postlingual deafness on speech production: implications for the role of auditory feedback. J Acoust Soc Am 88:2099–2114PubMedGoogle Scholar
  143. Watanabe A, Eda-Fujiwara H, Kimura T (2006) Auditory feedback is necessary for long-term maintenance of high-frequency sound syllables in the song of adult male budgerigars (Melopsittacus undulatus). J Comp Physiol A 193:81–97. doi: 10.1007/s00359-006-0173-y Google Scholar
  144. White SA, Fisher SE, Geschwind DH et al (2006) Singing mice, songbirds, and more: models for FOXP2 function and dysfunction in human speech and language. J Neurosci 26:10376–10379. doi: 10.1523/JNEUROSCI.3379-06.2006 PubMedGoogle Scholar
  145. Whitney G, Nyby J (1983) Sound communication among adults. In: Willott JF (ed) The auditory psychobiology of the mouse. Charles C Thomas Pub Ltd., SpringfieldGoogle Scholar
  146. Wild JM (1994) The auditory-vocal-respiratory axis in birds. Brain Behav Evol 44:192–209PubMedGoogle Scholar
  147. Wild JM (1997) Neural pathways for the control of birdsong production. J Neurobiol 33:653–670PubMedGoogle Scholar
  148. Wöhr M, Dalhoff M, Wolf E et al (2008a) Effects of genetic background, gender, and early environmental factors on isolation-induced ultrasonic calling in mouse pups: an embryo-transfer study. Behav Genet 38:579–595PubMedGoogle Scholar
  149. Wöhr M, Houx B, Schwarting RK et al (2008b) Effects of experience and context on 50-kHz vocalizations in rats. Physiol Behav 93:766–776. doi: 10.1016/j.physbeh.2007.11.031 PubMedGoogle Scholar
  150. Woolley SMN, Rubel EW (1997) Bengalese finches Lonchura Striata domestica depend upon auditory feedback for the maintenance of adult song. J Neurosci 17:6380–6390PubMedGoogle Scholar
  151. Yajima Y, Hayashi Y, Yoshii N (1982) Ambiguus motoneurons discharging closely associated with ultrasonic vocalization in rats. Brain Res 238:445–450PubMedGoogle Scholar
  152. Zann R (1985) Ontogeny of the zebra finch distance call: I. Effects of cross-fostering to bengalese finches. Z Tierpsychol 68:1–23Google Scholar
  153. Zann R (1990) Song and call learning in wild zebra finches in south-east Australia. Anim Behav 40:811–828Google Scholar
  154. Zufall F (2005) The TRPC2 ion channel and pheromone sensing in the accessory olfactory system. N-S Arch Pharmacol 371:245–250. doi: 10.1007/s00210-005-1028-8 Google Scholar
  155. Zufall F, Ukhanov K, Lucas P, Leinders-Zufall T (2005) Neurobiology of TRPC2: from gene to behavior. Pflug Arch Eur J Physiol 451:61–71. doi: 10.1007/s00424-005-1432-4 Google Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2014

Authors and Affiliations

  1. 1.Department of Life Sciences, Graduate School of Arts and SciencesThe University of TokyoTokyoJapan

Personalised recommendations