Development of Social Vocalizations in Mice

Adult mice are highly vocal animals, with both males and females vocalizing in same sex and cross sex social encounters. Mouse pups are also highly vocal, producing isolation vocalizations when they are cold or removed from the nest. This study examined patterns in the development of pup isolation vocalizations, and compared these to adult vocalizations. In three litters of CBA/CaJ mice, we recorded isolation vocalizations at ages postnatal day 5 (p5), p7, p9, p11, and p13. Adult vocalizations were obtained in a variety of social situations. Altogether, 28,384 discrete vocal signals were recorded using high-frequency-sensitive equipment and analyzed for syllable type, spectral and temporal features, and the temporal sequencing within bouts. We found that pups produced all but one of the 11 syllable types recorded from adults. The proportions of syllable types changed developmentally, but even the youngest pups produced complex syllables with frequency-time variations. When all syllable types were pooled together for analysis, changes in the peak frequency or the duration of syllables were small, although significant, from p5 through p13. However, individual syllable types showed different, large patterns of change over development, requiring analysis of each syllable type separately. Most adult syllables were substantially lower in frequency and shorter in duration. As pups aged, the complexity of vocal bouts increased, with a greater tendency to switch between syllable types. Vocal bouts from older animals, p13 and adult, had significantly more sequential structure than those from younger mice. Overall, these results demonstrate substantial changes in social vocalizations with age. Future studies are required to identify whether these changes result from developmental processes affecting the vocal tract or control of vocalization, or from vocal learning. To provide a tool for further research, we developed a MATLAB program that generates bouts of vocalizations that correspond to mice of different ages.

[1]  T. Holy,et al.  Ultrasonic Songs of Male Mice , 2005, PLoS biology.

[2]  D. Riskin,et al.  Ultrasonic sound as an indicator of acute pain in laboratory mice. , 2008, Journal of the American Association for Laboratory Animal Science : JAALAS.

[3]  Bijan Pesaran,et al.  The role of nonlinear dynamics of the syrinx in the vocalizations of a songbird , 1998, Nature.

[4]  C. Portfors,et al.  Types and functions of ultrasonic vocalizations in laboratory rats and mice. , 2007, Journal of the American Association for Laboratory Animal Science : JAALAS.

[5]  Thierry Aubin,et al.  Localisation of an acoustic signal in a noisy environment: the display call of the king penguin Aptenodytes patagonicus. , 2002, The Journal of experimental biology.

[6]  Robert C. Liu,et al.  Inhibitory Plasticity in a Lateral Band Improves Cortical Detection of Natural Vocalizations , 2009, Neuron.

[7]  K. Taniguchi,et al.  A comparative study of isolation-induced ultrasonic vocalization in rodent pups. , 2002, Experimental animals.

[8]  K. Johnson,et al.  Assessment of hearing in 80 inbred strains of mice by ABR threshold analyses , 1999, Hearing Research.

[9]  G. Ehret Development of absolute auditory thresholds in the house mouse (Mus musculus). , 1976, Journal of the American Audiology Society.

[10]  D. Rendall,et al.  Vocal recognition of individuals and kin in free-ranging rhesus monkeys , 1996, Animal Behaviour.

[11]  G. Ehret,et al.  Development of tonotopy in the inferior colliculus. I. Electrophysiological mapping in house mice. , 1990, Brain research. Developmental brain research.

[12]  G Whitney,et al.  Ultrasonic vocalizing by adult female mice (Mus musculus). , 1985, Journal of comparative psychology.

[13]  M. Barthélemy,et al.  Spectrographic analysis of the ultrasonic vocalisations of adult male and female BALB/c mice , 2004, Naturwissenschaften.

[14]  R. Zann The Zebra Finch: A Synthesis of Field and Laboratory Studies , 1996 .

[15]  L. Karkowski,et al.  Genetic and Developmental Influences on Infant Mouse Ultrasonic Calling. II. Developmental Patterns in the Calls of Mice 2–12 Days of Age , 1998, Behavior genetics.

[16]  T. Holy,et al.  Loss of sex discrimination and male-male aggression in mice deficient for TRP2. , 2002, Nature Reviews Genetics.

[17]  C. Chatfield,et al.  Analysing sequences of behavioural events. , 1970, Journal of theoretical biology.

[18]  P. Marler Chapter 5 – Bird calls: a cornucopia for communication , 2004 .

[19]  G. Ehret,et al.  Low-frequency sound communication by mouse pups (Mus musculus): wriggling calls release maternal behaviour , 1986, Animal Behaviour.

[20]  Robert C. Liu,et al.  Auditory Cortical Detection and Discrimination Correlates with Communicative Significance , 2007, PLoS biology.

[21]  D. Santucci,et al.  Ultrasonic vocalizations by infant laboratory mice: a preliminary spectrographic characterization under different conditions. , 1998, Developmental psychobiology.

[22]  Marcus Müller,et al.  A physiological place–frequency map of the cochlea in the CBA/J mouse , 2005, Hearing Research.

[23]  Hanspeter Herzel,et al.  Calls out of chaos: the adaptive significance of nonlinear phenomena in mammalian vocal production , 2002, Animal Behaviour.

[24]  Jacqueline N. Crawley,et al.  Unusual Repertoire of Vocalizations in the BTBR T+tf/J Mouse Model of Autism , 2008, PloS one.

[25]  N. Simon,et al.  Spontaneous pup-killing by mice in response to large litters. , 1978, Developmental psychobiology.

[26]  G. Ehret,et al.  Categorical perception of mouse pup ultrasound by lactating females , 1981, Naturwissenschaften.

[27]  Robert C. Liu,et al.  Acoustic variability and distinguishability among mouse ultrasound vocalizations. , 2003, The Journal of the Acoustical Society of America.

[28]  R. Bell,et al.  Ultra-sounds in three inbred strains of young mice. , 1972, Behavioral biology.

[29]  K. Hammerschmidt,et al.  Female mice respond to male ultrasonic ‘songs’ with approach behaviour , 2009, Biology Letters.

[30]  G. Zipf The Psycho-Biology Of Language: AN INTRODUCTION TO DYNAMIC PHILOLOGY , 1999 .

[31]  A. Feng,et al.  Voices of the dead: complex nonlinear vocal signals from the larynx of an ultrasonic frog , 2006, Journal of Experimental Biology.

[32]  George Kingsley Zipf,et al.  Human behavior and the principle of least effort , 1949 .

[33]  W. Fitch,et al.  Vocal production in nonhuman primates: Acoustics, physiology, and functional constraints on “honest” advertisement , 1995, American journal of primatology.

[34]  Isao Tokuda,et al.  Nonlinear analysis of irregular animal vocalizations. , 2002, The Journal of the Acoustical Society of America.

[35]  G. Ehret,et al.  Sex and parental experience determine the onset of an instinctive behavior in mice , 2004, Naturwissenschaften.

[36]  P. Marler,et al.  Nature's Music: The Science of Birdsong , 2004 .

[37]  Günter Ehret,et al.  Sound communication between parents and offspring , 2009 .

[38]  G. Ehret,et al.  Categorical perception of mouse-pup ultrasounds in the temporal domain , 1992, Animal Behaviour.

[39]  Simon Johnston,et al.  Information theory, animal communication, and the search for extraterrestrial intelligence , 2011 .

[40]  J. C. Fentress,et al.  Individually distinct vocalizations in timber wolves, Canis lupus , 1990, Animal Behaviour.

[41]  W. Fitch Vocal tract length and formant frequency dispersion correlate with body size in rhesus macaques. , 1997, The Journal of the Acoustical Society of America.

[42]  Garet P. Lahvis,et al.  Affiliative Behavior, Ultrasonic Communication and Social Reward Are Influenced by Genetic Variation in Adolescent Mice , 2007, PloS one.