Skip to main content
SpringerLink
Log in

Vocal Signals of Sexual Motivation in Male and Female Rodents

  • Preclinical and Psychophysiology (F Guaracci and L Marson, Section Editors)
  • Published:
Current Sexual Health Reports Aims and scope Submit manuscript

Abstract

Purpose of the Review

Rodents produce ultrasonic vocalizations (USV) under different social contexts, including courtship and reproduction. The present review aims to summarize the behavioral, bioacoustical, and physiological evidence that USV are reliable signals of sexual motivation in both male and female rodents.

Recent Findings

USV are actively produced by both sexes during sexual interactions, contrary to earlier assumptions. Male-typical and female-typical vocal behaviors can be identified. Calling rates and acoustic parameters, such as call duration, frequency, and energy, can be modulated rapidly over time by motivational state and sexual context. USV produced in response to sexual context could be regulated by the brain on a moment-to-moment basis through non-classical mechanisms of steroid action. Finally, I provide some practical considerations for the acoustic and statistical analyses of these vocal signals.

Summary

USV can be used as signals of sexual motivation in both sexes to study brain and hormonal mechanisms underlying sexual behavior or sexual differentiation.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

Papers of particular interest, published recently, have been highlighted as: • Of importance •• Of major importance

  1. Guarraci FA, Meerts SH. Does practice make perfect? Sexual experience and psychomotor stimulants influence female sexual motivation through medial preoptic area dopamine. Curr Sex Health Rep. 2017;9:57–64.

    Google Scholar 

  2. Hull EM, Dominguez JM. Sexual behavior in male rodents. Horm Behav. 2007;52:45–55.

    CAS  PubMed  PubMed Central  Google Scholar 

  3. Ventura-Aquino E, Portillo W, Paredes RG. Sexual motivation: a comparative approach in vertebrate species. Curr Sex Health Rep. 2018:1–10.

  4. Sales GD. Ultrasonic calls of wild and wild-type rodents. In: Brudzynski SM, editor. Handbook of Mammalian Vocalization: An Integrative Neuroscience Approach. Academic Press; 2010. p. 77–88.

  5. Sales G, Pye P. Ultrasonic communication by animals. 1974. Chapman and Hall Ltd 281 p.

  6. Scattoni ML, McFarlane H, Zhodzishsky V, Caldwell H, Young W, Ricceri L, et al. Reduced ultrasonic vocalizations in vasopressin 1b knockout mice. Behav Brain Res. 2008;187:371–8.

    CAS  PubMed  Google Scholar 

  7. Scattoni ML, Crawley J, Ricceri L. Ultrasonic vocalizations: a tool for behavioural phenotyping of mouse models of neurodevelopmental disorders. Neurosci Biobehav Rev. 2009;33:508–15.

    PubMed  Google Scholar 

  8. Scattoni 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.

    PubMed  PubMed Central  Google Scholar 

  9. Kroes RA, Burgdorf J, Otto NJ, Panksepp J, Moskal JR. Social defeat, a paradigm of depression in rats that elicits 22-kHz vocalizations, preferentially activates the cholinergic signaling pathway in the periaqueductal gray. Behav Brain Res. 2007;182:290–300.

    CAS  PubMed  PubMed Central  Google Scholar 

  10. Ciucci MR, Ahrens AM, Ma ST, Kane JR, Windham EB, Woodlee MT, et al. Reduction of dopamine synaptic activity: degradation of 50-kHz ultrasonic vocalization in rats. Behav Neurosci. 2009;123:328–36.

    PubMed  PubMed Central  Google Scholar 

  11. Grant LM, Barnett DG, Doll EJ, Leverson G, Ciucci M. Relationships among rat ultrasonic vocalizations, behavioral measures of striatal dopamine loss, and striatal tyrosine hydroxylase immunoreactivity at acute and chronic time points following unilateral 6-hydroxydopamine-induced dopamine depletion. Behav Brain Res. 2015;291:361–71.

    CAS  PubMed  PubMed Central  Google Scholar 

  12. Egnor SR, Seagraves KM. The contribution of ultrasonic vocalizations to mouse courtship. Curr Opin Neurobiol. 2016;38:1–5.

    CAS  PubMed  Google Scholar 

  13. Portfors CV, Perkel DJ. The role of ultrasonic vocalizations in mouse communication. Curr Opin Neurobiol. 2014;28:115–20.

    CAS  PubMed  Google Scholar 

  14. Hoffmann F, Musolf K, Penn DJ. Spectrographic analyses reveal signals of individuality and kinship in the ultrasonic courtship vocalizations of wild house mice. Physiol Behav. 2012;105:766–71.

    CAS  PubMed  Google Scholar 

  15. Kalcounis-Rueppell MC, Petric R, Briggs JR, Carney C, Marshall MM, Willse JT, et al. Differences in ultrasonic vocalizations between wild and laboratory California mice (Peromyscus californicus). PLoS One. 2010;5:e9705.

    PubMed  PubMed Central  Google Scholar 

  16. Musolf K, Hoffmann F, Penn DJ. Ultrasonic courtship vocalizations in wild house mice, Mus musculus musculus. Anim Behav. 2010;79:757–64.

    Google Scholar 

  17. Ehret G. Infant rodent ultrasounds -- a gate to the understanding of sound communication. Behav Genet. 2005;35:19–29.

    PubMed  Google Scholar 

  18. Farrell WJ, Alberts JR. Stimulus control of maternal responsiveness to Norway rat (Rattus norvegicus) pup ultrasonic vocalizations. J Comp Psychol. 2002;116:297–307.

    PubMed  Google Scholar 

  19. Scattoni ML, Branqui I. Vocal repertoire in mouse pups: strain differences. In: Handbook of Mammalian Vocalization. Handbook of Mammalian Vocalization: An Integrative Neuroscience Approach. Academic Press; 2010. p. 89–95.

  20. Burgdorf J, Kroes RA, Moskal JR, Pfaus JG, Brudzynski SM, Panksepp J. Ultrasonic vocalizations of rats (Rattus norvegicus) during mating, play, and aggression: behavioral concomitants, relationship to reward, and self-administration of playback. J Comp Psychol. 2008;122:357–67.

    PubMed  Google Scholar 

  21. Burke CJ, Kisko TM, Swiftwolfe H, Pellis SM, Euston DR. Specific 50-kHz vocalizations are tightly linked to particular types of behavior in juvenile rats anticipating play. PLoS One. 2017;12:e0175841.

    PubMed  PubMed Central  Google Scholar 

  22. Keesom SM, Rendon NM, Demas GE, Hurley LM. Vocal behaviour during aggressive encounters between Siberian hamsters, Phodopus sungorus. Anim Behav. 2015;102:85–93.

    Google Scholar 

  23. Sales GD. Ultrasound and aggressive behaviour in rats and other small mammals. Anim Behav. 1972;20:88–100.

    CAS  PubMed  Google Scholar 

  24. Rieger NS, Marler CA. The function of ultrasonic vocalizations during territorial defence by pair-bonded male and female California mice. Anim Behav. 2018;135:97–108.

    Google Scholar 

  25. Seredynski AL, Balthazart J, Christophe VJ, Ball GF, Cornil CA. Neuroestrogens rapidly regulate sexual motivation but not performance. J Neurosci. 2013;33:164–74.

    CAS  PubMed  PubMed Central  Google Scholar 

  26. Lahvis GP, Alleva E, Scattoni ML. Translating mouse vocalizations: prosody and frequency modulation1. Genes Brain Behav. 2011;10:4–16.

    CAS  PubMed  PubMed Central  Google Scholar 

  27. Nyby J. Reflexive testosterone release: a model system for studying the nongenomic effects of testosterone upon male behavior. Front Neuroendocrinol. 2008;29:199–210.

    CAS  PubMed  Google Scholar 

  28. Hanson JL, Hurley LM. Female presence and estrous state influence mouse ultrasonic courtship vocalizations. PLoS One. 2012;7:e40782.

    CAS  PubMed  PubMed Central  Google Scholar 

  29. Nyby J. Ultrasonic vocalizations during sex behavior of male house mice (Mus musculus): a description. Behav Neural Biol. 1983;39:128–34.

    CAS  PubMed  Google Scholar 

  30. Sales GD. Ultrasound and mating behaviour in rodents with some observations on other behavioural situations. J Zool. 1972;168:149–64.

    Google Scholar 

  31. •• Fernández-Vargas M, Johnston RE. Ultrasonic vocalizations in golden hamsters (Mesocricetus auratus) reveal modest sex differences and nonlinear signals of sexual motivation. PLoS One. 2015;10:e0116789 This study described and analyzed the USV repertoire produced by golden hamsters after a sexual interaction. It also showed that motivation to vocalize depends on the sex of the stimulus, but the USV produced in response to the opposite sex were similar between sexes and across individuals.

    PubMed  PubMed Central  Google Scholar 

  32. Floody OR, Pfaff DW, Lewis CD. Communication among hamsters by high-frequency acoustic signals: II. Determinants of calling by females and males. J Comp Physiol Psychol. 1977;91:807–19.

    Google Scholar 

  33. Holman S. Sexually dimorphic, ultrasonic vocalizations of Mongolian gerbils. Behav Neural Biol. 1980;28:183–92.

    Google Scholar 

  34. Nyby J, Wysocki CJ, Whitney G, Dizinno G. Pheromonal regulation of male mouse ultrasonic courtship (Mus musculus). Anim Behav. 1977;25:333–41.

    CAS  PubMed  Google Scholar 

  35. Whitney G, Coble JR, Stockton MD, Tilson EF. Ultrasonic emissions: do they facilitate courtship of mice? J Comp Physiol Psychol. 1973;84:445–52.

    CAS  PubMed  Google Scholar 

  36. Cherry JA, Lepri JJ. Sexual dimorphism and gonadal control of ultrasonic vocalizations in adult pine voles, Microtus pinetorum. Horm Behav. 1986;20:34–48.

    CAS  PubMed  Google Scholar 

  37. Gourbal BEF, Barthelemy M, Petit G, Gabrion C. Spectrographic analysis of the ultrasonic vocalisations of adult male and female BALB/c mice. Naturwissenschaften. 2004;91:381–5.

    CAS  PubMed  Google Scholar 

  38. Pierce JD, Sawrey DK, Dewsbury DA. A comparative study of rodent ultrasonic vocalizations during copulation. Behav Neural Biol. 1989;51:211–21.

    PubMed  Google Scholar 

  39. Snoeren EMS, Ågmo A. Female ultrasonic vocalizations have no incentive value for male rats. Behav Neurosci. 2013;127:439–50.

    PubMed  Google Scholar 

  40. Warburton VL, Sales GD, Milligan SR. The emission and elicitation of mouse ultrasonic vocalizations: the effects of age, sex and gonadal status. Physiol Behav. 1989;45:41–7.

    CAS  PubMed  Google Scholar 

  41. Wright JM, Gourdon JC, Clarke PB. Identification of multiple call categories within the rich repertoire of adult rat 50-kHz ultrasonic vocalizations: effects of amphetamine and social context. Psychopharmacology. 2010;211:1–13.

    CAS  PubMed  Google Scholar 

  42. Maggio JC, Whitney G. Ultrasonic vocalizing by adult female mice (Mus musculus). J Comp Psychol. 1985;99:420–36.

    CAS  PubMed  Google Scholar 

  43. White NR, Prasad M, Barfield RJ, Nyby JG. 40- and 70-kHz vocalizations of mice (Mus musculus) during copulation. Physiol Behav. 1998;63:467–73.

    CAS  PubMed  Google Scholar 

  44. •• Neunuebel JP, Taylor AL, Arthur BJ, Egnor SER. Female mice ultrasonically interact with males during courtship displays. Elife. 2015;4. Authors implemented a microphone-array-based system to identify the source of vocal signals produced by an interacting male-female pair. It rejects the prevalent assumption that females are mostly quiet in the presence of a male and offers evidence of an interactive exchange of vocalizations during courtship.

  45. Holy TE, Guo Z. Ultrasonic songs of male mice. PLoS Biol 2005;3:e386.

    PubMed  PubMed Central  Google Scholar 

  46. Roullet FI, Wöhr M, Crawley JN. Female urine-induced male mice ultrasonic vocalizations, but not scent-marking, is modulated by social experience. Behav Brain Res. 2011;216:19–28.

    PubMed  Google Scholar 

  47. • Burke K, Screven LA, Dent ML. CBA/CaJ mouse ultrasonic vocalizations depend on prior social experience. PLoS One. 2018;13:e0197774 This study demonstrated that male and female mice can produce vocalizations after social interactions and both sexes produced as many USV after being exposed to a same-sex or an opposite-sex individual.

    PubMed  PubMed Central  Google Scholar 

  48. Floody OR, Comerci JT, Lisk RD. Hormonal control of sex differences in ultrasound production by hamsters. Horm Behav. 1987;21:17–35.

    CAS  PubMed  Google Scholar 

  49. McGinnis MY, Vakulenko M. Characterization of 50-kHz ultrasonic vocalizations in male and female rats. Physiol Behav. 2003;80:81–8.

    CAS  PubMed  Google Scholar 

  50. Cherry JA. Ultrasonic vocalizations by male hamsters: parameters of calling and effects of playbacks on female behaviour. Anim Behav. 1989;38:138–53.

    Google Scholar 

  51. Gahr M. Sexual differentiation of the vocal control system of birds. Adv Genet. 2007;59:67–105.

    CAS  PubMed  Google Scholar 

  52. Briggs JR, Kalcounis-Rueppell MC. Similar acoustic structure and behavioural context of vocalizations produced by male and female California mice in the wild. Anim Behav. 2011;82:1263–73.

    Google Scholar 

  53. Hammerschmidt K, Radyushkin K, Ehrenreich H, Fischer J. The structure and usage of female and male mouse ultrasonic vocalizations reveal only minor differences. PLoS One. 2012;7:e41133.

    CAS  PubMed  PubMed Central  Google Scholar 

  54. von Merten S, Hoier S, Pfeifle C, Tautz D. A role for ultrasonic vocalisation in social communication and divergence of natural populations of the house mouse (Mus musculus domesticus). PLoS One. 2014;9:e97244.

    Google Scholar 

  55. • Zala SM, Reitschmidt D, Noll A, Balazs P, Penn DJ. Sex-dependent modulation of ultrasonic vocalizations in house mice (Mus musculus musculus). PLoS One. 2017;12:e0188647 This study recorded USV produced by male and female F1 of wild-caught mice during an opposite-sex or same-sex interaction across a divider with holes. Males and females produced similar number of USV, but an opposite-sex interaction elicited higher rates and call frequency than a same-sex interaction.

    PubMed  PubMed Central  Google Scholar 

  56. Börner A, Hjemdahl R, Götz T, Brown GR. Ultrasonic vocalizations of female Norway rats (Rattus norvegicus) in response to social partners. J Comp Psychol. 2016;130:76–80.

    PubMed  Google Scholar 

  57. Floody OR, Pfaff DW. Communication among hamsters by high-frequency acoustic signals: I. Physical characteristics of hamster calls. J Comp Physiol Psychol. 1977;91:794–806.

    Google Scholar 

  58. Bachorowski J-A. Vocal expression and perception of emotion. Curr Dir Psychol Sci. 1999;8:53–7.

    Google Scholar 

  59. Brudzynski SM. Handbook of mammalian vocalization: an integrative neuroscience approach. Academic Press; 2010.

  60. Brudzynski SM. Ethotransmission: communication of emotional states through ultrasonic vocalization in rats. Curr Opin Neurobiol. 2013;23:310–7.

    CAS  PubMed  Google Scholar 

  61. Panksepp J. Emotional causes and consequences of social-affective vocalization. In: Brudzynski SM, editor Handbook of Mammalian Vocalization: An Integrative Neuroscience Approach Academic Press; 2010. p. 201–208.

  62. • Stewart AM, Lewis GF, Yee JR, Kenkel WM, Davila MI, Sue Carter C, et al. Acoustic features of prairie vole (Microtus ochrogaster) ultrasonic vocalizations covary with heart rate. Physiol Behav. 2015;138:94–100 Telemetric transmitters were implanted in prairie voles to measure heart rate during a female-female separation-in-proximity test. Although the study is based on a small sample size, data suggested that acoustic parameters such as call frequency and duration were positively correlated with heart rate.

    CAS  PubMed  Google Scholar 

  63. Fitch WT, Neubauer J, Herzel H. Calls out of chaos: the adaptive significance of nonlinear phenomena in mammalian vocal production. Anim Behav. 2002;63:407–18.

    Google Scholar 

  64. Scheumann M, Roser A-E, Konerding W, Bleich E, Hedrich H-J, Zimmermann E. Vocal correlates of sender-identity and arousal in the isolation calls of domestic kitten (Felis silvestris catus). Front Zool. 2012;9:36.

    PubMed  PubMed Central  Google Scholar 

  65. Rendall D. Acoustic correlates of caller identity and affect intensity in the vowel-like grunt vocalizations of baboons. J Acoust Soc Am. 2003;113:3390–402.

    PubMed  Google Scholar 

  66. •• Finton CJ, Keesom SM, Hood KE, Hurley LM. What’s in a squeak? Female vocal signals predict the sexual behaviour of male house mice during courtship. Anim Behav. 2017;126:163–75 This study analyzed the acoustics and behavioral context of a female call produced during a male-female interaction. This particular audible call is characterized by nonlinear acoustic phenomena whose duration that is associated with receptivity and varied among individuals.

    Google Scholar 

  67. •• Fernández-Vargas M. Presence of a potential competitor and its individual identity modulate ultrasonic vocalizations in male hamsters. Anim Behav. 2018;145:11–27 This study found that a competitive context and memory for specific individuals can modulate call duration and energy over time in a male after interacting with a female.

    Google Scholar 

  68. •• Bialy M, Bogacki-Rychlik W, Kasarello K, Nikolaev E, Sajdel-Sulkowska EM. Modulation of 22-khz postejaculatory vocalizations by conditioning to new place: evidence for expression of a positive emotional state. Behav Neurosci. 2016;130:415–21 This study showed that the production of postejaculatory 22 kHz USV in rats required cues associated with ejaculation and a relaxation state. The duration of these calls can be modulated by the presence of odor cues from an unfamiliar vs. familiar males.

    CAS  PubMed  Google Scholar 

  69. Matochik JA, Barfield RJ, Nyby J. Regulation of sociosexual communication in female Long-Evans rats by ovarian hormones. Horm Behav. 1992;26:545–55.

    CAS  PubMed  Google Scholar 

  70. Johnston RE. Vomeronasal and/or olfactory mediation of ultrasonic calling and scent marking by female golden hamsters. Physiol Behav. 1992;51:437–48.

    CAS  PubMed  Google Scholar 

  71. Ågmo A, Snoeren EMS. Silent or vocalizing rats copulate in a similar manner. PLoS One. 2015;10:e0144164.

    PubMed  PubMed Central  Google Scholar 

  72. Snoeren EMS, Ågmo A. The incentive value of males’ 50-kHz ultrasonic vocalizations for female rats (Rattus norvegicus). J Comp Psychol. 2014;128:40–55.

    PubMed  Google Scholar 

  73. Willadsen M, Seffer D, Schwarting RKW, Wöhr M. Rodent ultrasonic communication: male prosocial 50-kHz ultrasonic vocalizations elicit social approach behavior in female rats (Rattus norvegicus). J Comp Psychol. 2014;128:56–64.

    PubMed  Google Scholar 

  74. Chabout J, Sarkar A, Dunson DB, Jarvis ED. Male mice song syntax depends on social contexts and influences female preferences. Front Behav Neurosci. 2015;9:76.

  75. Musolf K, Meindl S, Larsen AL, Kalcounis-Rueppell MC, Penn DJ. Ultrasonic vocalizations of male mice differ among species and females show assortative preferences for male calls. PLoS One 2015;10:e0134123.

    PubMed  PubMed Central  Google Scholar 

  76. Brudzynski SM, Fletcher NH. Rat ultrasonic vocalization: short-range communication. In: Brudzynski SM, editor. Handbook of Mammalian Vocalization: An Integrative Neuroscience Approach. Academic Press; 2010. p. 69–76.

  77. Floody OR, Bauer GB. Selectivity in the responses of hamsters to conspecific vocalizations. Horm Behav. 1987;21:522–7.

    CAS  PubMed  Google Scholar 

  78. • Asaba A, Osakada T, Touhara K, Kato M, Mogi K, Kikusui T. Male mice ultrasonic vocalizations enhance female sexual approach and hypothalamic kisspeptin neuron activity. Horm Behav. 2017;94:53–60 This study showed that USV produced by male mice increased activation of kisspeptin neurons in the arcuate nucleus of diestrous females. Because these neurons regulate the pulse of GnRH and are involved in follicular maturation, it is possible that male USV could be involved in female reproduction.

    CAS  PubMed  Google Scholar 

  79. Holman SD, Seale WTC, Hutchison JB. Ultrasonic vocalizations in immature gerbils: emission rate and structural changes after neonatal exposure to androgen. Physiol Behav. 1995;57:451–60.

    CAS  PubMed  Google Scholar 

  80. Holman SD. Neonatal androgenic influences on masculine ultrasonic vocalizations of mongolian gerbils. Physiol Behav. 1981;26:583–6.

    CAS  PubMed  Google Scholar 

  81. Adkins-Regan E. Hormones and animal social behavior: Princeton University Press; 2005.

  82. Floody OR, Walsh C, Flanagan MT. Testosterone stimulates ultrasound production by male hamsters. Horm Behav. 1979;12:164–71.

    CAS  PubMed  Google Scholar 

  83. Matochik JA, Barfield RJ. Hormonal control of precopulatory sebaceous scent marking and ultrasonic mating vocalizations in male rats. Horm Behav. 1991;25:445–60.

    CAS  PubMed  Google Scholar 

  84. Nyby J, Dizinno G, Whitney G. Sexual dimorphism in ultrasonic vocalizations of mice (Mus musculus): gonadal hormone regulation. J Comp Physiol Psychol. 1977;91:1424–31.

    CAS  PubMed  Google Scholar 

  85. Nunez AA, Nyby J, Whitney G. The effects of testosterone, estradiol, and dihydrotestosterone on male mouse (Mus musculus) ultrasonic vocalizations. Horm Behav. 1978;11:264–72.

    CAS  PubMed  Google Scholar 

  86. Bean NJ, Nyby J, Kerchner M, Dahinden Z. Hormonal regulation of chemosignal-stimulated precopulatory behaviors in male housemice (Mus musculus). Horm Behav. 1986;20:390–404.

    CAS  PubMed  Google Scholar 

  87. Pomerantz SM, Fox E, Clemens LG. Gonadal hormone activation of male courtship ultrasonic vocalizations and male copulatory behavior in castrated male deer mice (Peromyscus maniculatus bairdi). Behav Neurosci. 1983;97:462–9.

    CAS  PubMed  Google Scholar 

  88. Floody OR, Petropoulos AC. Aromatase inhibition depresses ultrasound production and copulation in male hamsters. Horm Behav. 1987;21:100–4.

    CAS  PubMed  Google Scholar 

  89. Floody OR, Merkle DA, Cahill TJ, Shopp GM. Gonadal hormones stimulate ultrasound production by female hamsters. Horm Behav. 1979;12:172–84.

    CAS  PubMed  Google Scholar 

  90. •• Balthazart J, Choleris E, Remage-Healey L. Steroids and the brain: 50years of research, conceptual shifts and the ascent of non-classical and membrane-initiated actions. Horm Behav. 2018;99:1–8 This recent review summarized of the history of steroid endocrinology and emphasized on the latest research advances on the rapid, non-classical mechanisms of steroids.

    CAS  PubMed  Google Scholar 

  91. Charlier TD, Cornil CA, Patte-Mensah C, Meyer L, Mensah-Nyagan AG, Balthazart J. Local modulation of steroid action: rapid control of enzymatic activity. Front Neurosci. 2015;9:83.

    PubMed  PubMed Central  Google Scholar 

  92. Cornil CA, Charlier TD. Rapid behavioural effects of oestrogens and fast regulation of their local synthesis by brain aromatase. J Neuroendocrinol. 2010;22:664–73.

    CAS  PubMed  PubMed Central  Google Scholar 

  93. Cornil CA, Ball GF, Balthazart J. Rapid control of male typical behaviors by brain-derived estrogens. Front Neuroendocrinol. 2012;33:425–46.

    CAS  PubMed  PubMed Central  Google Scholar 

  94. Balthazart J, Ball G. Brain aromatase, estrogens, and behavior. OUP USA; 2013.

  95. Cornil CA. On the role of brain aromatase in females: why are estrogens produced locally when they are available systemically? J Comp Physiol A. 2018;204:31–49.

    CAS  Google Scholar 

  96. Gleason ED, Fuxjager MJ, Oyegbile TO, Marler CA. Testosterone release and social context: when it occurs and why. Front Neuroendocrinol 2009;30:460–469.

    CAS  PubMed  Google Scholar 

  97. Harding CF. Social modulation of circulating hormone levels in the male. Amer Zool. 1981;21:223–31.

    CAS  Google Scholar 

  98. Amstislavskaya TG, Popova NK. Female-induced sexual arousal in male mice and rats: behavioral and testosterone response. Horm Behav. 2004;46:544–50.

    CAS  PubMed  Google Scholar 

  99. Cornil CA, Ball GF, Balthazart J. Functional significance of the rapid regulation of brain estrogens: where do the estrogens come from? Brain Res. 2006;1126:2–26.

    CAS  PubMed  PubMed Central  Google Scholar 

  100. Hayden-Hixson DM, Ferris CF. Steroid-specific regulation of agonistic responding in the anterior hypothalamus of male hamsters. Physiol Behav. 1991;50:793–9.

    CAS  PubMed  Google Scholar 

  101. Taziaux M, Keller M, Bakker J, Balthazart J. Sexual behavior activity tracks rapid changes in brain estrogen concentrations. J Neurosci. 2007;27:6563–72.

    CAS  PubMed  Google Scholar 

  102. • Fernández-Vargas M. Rapid effects of estrogens and androgens on temporal and spectral features in ultrasonic vocalizations. Horm Behav. 2017;94:69–83 This study showed how a single subcutaneous injection of testosterone or 17-β estradiol can rapidly (30–15 min respectively) change call duration and frequency over a short period of time compared to a vehicle injection in gonadally-intact males.

    PubMed  Google Scholar 

  103. Fuxjager MJ, Knaebe B, Marler CA. A single testosterone pulse rapidly reduces urinary marking behaviour in subordinate, but not dominant, white-footed mice. Anim Behav. 2015;100:8–14.

    Google Scholar 

  104. • Pultorak JD, Fuxjager MJ, Kalcounis-Rueppell MC, Marler CA. Male fidelity expressed through rapid testosterone suppression of ultrasonic vocalizations to novel females in the monogamous California mouse. Horm Behav. 2015;70:47–56 This study found that a single intraperitoneal injection of testosterone can change the number of USV produced by paired-males, but not unpaired males, during male-female interactions.

    CAS  PubMed  Google Scholar 

  105. Newman SW. The medial extended amygdala in male reproductive behavior a node in the mammalian social behavior network. Ann N Y Acad Sci. 1999;877:242–57.

    CAS  PubMed  Google Scholar 

  106. O’Connell LA, Hofmann HA. Evolution of a vertebrate social decision-making network. Science. 2012;336:1154–7.

    PubMed  Google Scholar 

  107. Harding SM, McGinnis MY. Androgen receptor blockade in the MPOA or VMN: effects on male sociosexual behaviors. Physiol Behav. 2004;81:671–80.

    CAS  PubMed  Google Scholar 

  108. Matochik JA, Sipos ML, Nyby JG, Barfield RJ. Intracranial androgenic activation of male-typical behaviors in house mice: motivation versus performance. Behav Brain Res. 1994;60:141–9.

    CAS  PubMed  Google Scholar 

  109. Nyby J, Matochik JA, Barfield RJ. Intracranial androgenic and estrogenic stimulation of male-typical behaviors in house mice (Mus domesticus). Horm Behav. 1992;26:24–45.

    CAS  PubMed  Google Scholar 

  110. Sipos ML, Nyby JH. Intracranial androgenic activation of male-typical behaviours in house mice: concurrent stimulation of the medial preoptic area and medial nucleus of the amygdala. J Neuroendocrinol. 1998;10:557–86.

    Google Scholar 

  111. Harding SM, McGinnis MY. Effects of testosterone in the VMN on copulation, partner preference, and vocalizations in male rats. Horm Behav. 2003;43:327–35.

    CAS  PubMed  Google Scholar 

  112. Harding SM, McGinnis MY. Microlesions of the ventromedial nucleus of the hypothalamus: effects on sociosexual behaviors in male rats. Behav Neurosci. 2005;119:1227–34.

    PubMed  Google Scholar 

  113. Sipos ML, Nyby JG. Concurrent androgenic stimulation of the ventral tegmental area and medial preoptic area: synergistic effects on male-typical reproductive behaviors in house mice. Brain Res. 1996;729:29–44.

    CAS  PubMed  Google Scholar 

  114. Floody OR. Dissociation of hypothalamic effects on ultrasound production and copulation. Physiol Behav. 1989;46:299–307.

    CAS  PubMed  Google Scholar 

  115. Floody OR. Cuts between the septum and preoptic area increase ultrasound production, lordosis, and body weight in female hamsters. Physiol Behav. 1993;54:383–92.

    CAS  PubMed  Google Scholar 

  116. Floody OR, Cooper TT, Albers HE. Injection of oxytocin into the medial preoptic–anterior hypothalamus increases ultrasound production by female hamsters. Peptides. 1998;19:833–9.

    CAS  PubMed  Google Scholar 

  117. Floody OR, O’Donohue TL. Lesions of the mesencephalic central gray depress ultrasound production and lordosis by female hamsters. Physiol Behav. 1980;24:79–85.

    CAS  PubMed  Google Scholar 

  118. Kirn J, Floody OR. Differential effects of lesions in three limbic areas on ultrasound production and lordosis by female hamsters. Behav Neurosci. 1985;99:1142–52.

    CAS  PubMed  Google Scholar 

  119. Floody OR. Time course of VMN lesion effects on lordosis and proceptive behavior in female hamsters. Horm Behav. 2002;41:366–76.

    PubMed  Google Scholar 

  120. Floody OR, DeBold JF. Effects of midbrain lesions on lordosis and ultrasound production. Physiol Behav. 2004;82:791–804.

    CAS  PubMed  Google Scholar 

  121. Gibson BM, Floody OR. Time course of VMN lesion effects on lordosis and ultrasound production in hamsters. Behav Neurosci. 1998;112:1236–46.

    CAS  PubMed  Google Scholar 

  122. Jürgens U. The neural control of vocalization in mammals: a review. J Voice. 2009;23:1–10.

    PubMed  Google Scholar 

  123. Newman JD. Chapter 2.2 - evolution of the communication brain in control of mammalian vocalization. In: Brudzynski SM, editor. Handbook of mammalian vocalization: an integrative neuroscience approach. Academic press; 2010. p. 23–28.

  124. Nyby J. Adult house mouse (Mus musculus) ultrasonic calls: hormonal and pheromonal regulation. In: Brudzynski SM, editor. Handbook of mammalian vocalization: an integrative neuroscience approach. Academic press; 2010. p. 303–310.

  125. • Grimsley JMS, Sheth S, Vallabh N, Grimsley CA, Bhattal J, Latsko M, et al. Contextual modulation of vocal behavior in mouse: newly identified 12 kHz “mid-frequency” vocalization emitted during restraint. Front Behav Neurosci. 2016;10:38 This study compared mice vocalizations produced during mating, isolation or restrain and identified an audible vocalization produced under restrain stress. Overall, vocalizations were significantly longer when produced during mating than during isolation or restrain.

    PubMed  PubMed Central  Google Scholar 

  126. Charif RA, Waack AM, Strickman LM. Raven Pro 1.4 user’s manual. Ithaca, NY: Cornell Lab of Ornithology; 2010.

  127. Kikusui T, Nakanishi K, Nakagawa R, Nagasawa M, Mogi K, Okanoya K. Cross fostering experiments suggest that mice songs are innate. PLoS One. 2011;6:e17721.

    CAS  PubMed  PubMed Central  Google Scholar 

  128. •• Zala SM, Reitschmidt D, Noll A, Balazs P, Penn DJ. Automatic mouse ultrasound detector (A-MUD): a new tool for processing rodent vocalizations. PLoS One. 2017;12:e0181200 This study developed an algorithm that automatically detects mouse USV and evaluates its performance in comparison with other commercially available software. The detector is free for scientific use.

    PubMed  PubMed Central  Google Scholar 

  129. Nakagawa S, Schielzeth H. A general and simple method for obtaining R2 from generalized linear mixed-effects models. Methods Ecol Evol. 2013;4:133–42.

    Google Scholar 

  130. Dingemanse NJ, Dochtermann NA. Quantifying individual variation in behaviour: mixed-effect modelling approaches. J Anim Ecol. 2013;82:39–54.

    PubMed  Google Scholar 

  131. Bolker BM, Brooks ME, Clark CJ, Geange SW, Poulsen JR, Stevens MHH, et al. Generalized linear mixed models: a practical guide for ecology and evolution. Trends Ecol Evol. 2009;24:127–35.

    PubMed  Google Scholar 

  132. Huck UW, Lisk RD, Allison JC, Van Dongen CG. Determinants of mating success in the golden hamster (Mesocricetus auratus): social dominance and mating tactics under seminatural conditions. Anim Behav. 1986;34:971–89.

    Google Scholar 

  133. Lisk RD, Ciaccio LA, Catanzaro C. Mating behaviour of the golden hamster under seminatural conditions. Anim Behav. 1983;31:659–66.

    Google Scholar 

  134. •• Gore AC, Holley AM, Crews D. Mate choice, sexual selection, and endocrine-disrupting chemicals. Horm Behav. 2018;101:3–12 This review provides evidence that endocrine-disrupting chemicals can affect all levels of reproduction including development, activation, neurobiology and behavior.

    CAS  PubMed  Google Scholar 

Download references

Acknowledgments

I would like to thank Robert E. Johnston, Elizabeth Adkins-Regan, and Andrew Bass for guidance and support in the writing of an earlier version of this manuscript. I thank Gregory J. Peters and Luke Remage-Healey for helpful comments on how to improve this manuscript. Finally, I would like to thank Fay Guarraci and Lesley Marson for constructive editorial and reviewer comments and for the invitation to contribute with this article.

Author information

Authors and Affiliations

  1. Psychological and Brain Sciences, University of Massachusetts, Amherst, Amherst, MA, 01003, USA

    Marcela Fernández-Vargas

Authors
  1. Marcela Fernández-Vargas
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Marcela Fernández-Vargas.

Ethics declarations

Conflict of Interest

The author declares no conflicts of interest.

Human and Animal Rights and Informed Consent

This article does contain studies with animal subjects performed by the author.

Additional information

This article is part of the Topical Collection on Preclinical and Psychophysiology

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Fernández-Vargas, M. Vocal Signals of Sexual Motivation in Male and Female Rodents. Curr Sex Health Rep 10, 315–328 (2018). https://doi.org/10.1007/s11930-018-0179-9

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11930-018-0179-9

Keywords

Search

Navigation