Social interactions in mice are frequently analysed in genetically modified strains in order to get insight of disorders affecting social interactions such as autism spectrum disorders. Different types of social interactions have been described, mostly between females and pups, and between adult males and females. However, we recently showed that social interactions between adult males could also encompass cognitive and motivational features. During social interactions, rodents emit ultrasonic vocalizations (USVs), but it remains unknown if call types are differently used depending of the context and if they are correlated with motivational state. Here, we recorded the calls of adult C57BL/6J male mice in various behavioral conditions, such as social interaction, novelty exploration and restraint stress. We introduced a modulator for the motivational state by comparing males maintained in isolation and males maintained in groups before the experiments. Male mice uttered USVs in all social and non-social situations, and even in a stressful restraint context. They nevertheless emitted the most important number of calls with the largest diversity of call types in social interactions, particularly when showing a high motivation for social contact. For mice maintained in social isolation, the number of calls recorded was positively correlated with the duration of social contacts, and most calls were uttered during contacts between the two mice. This correlation was not observed in mice maintained in groups. These results open the way for a deeper understanding and characterization of acoustic signals associated with social interactions. They can also help evaluating the role of motivational states in the emission of acoustic signals.
References
[1]
Panksepp JB, Lahvis GP (2007) Social reward among juvenile mice. Genes, brain, and behavior Oct;6(7): 661–71.
[2]
Granon S, Faure P, Changeux J-P (2003) Executive and social behaviors under nicotinic receptor regulation. Proceedings of the National Academy of Sciences of the United States of America Aug;100(16): 9596–601.
[3]
Avale ME, Chabout J, Pons S, Serreau P, De Chaumont F, et al. (2011) Prefrontal nicotinic receptors control novel social interaction between mice. The FASEB journal: official publication of the Federation of American Societies for Experimental Biology Mar;(1): 1–11.
[4]
Trezza V, Damsteegt R, Achterberg EJM, Vanderschuren LJMJ (2011) Nucleus accumbens μ-opioid receptors mediate social reward. The Journal of neuroscience: the official journal of the Society for Neuroscience Apr 27;31(17): 6362–70.
[5]
Scattoni ML, Gandhy SU, Ricceri L, Crawley JN (2008) Unusual repertoire of vocalizations in the BTBR T+tf/J mouse model of autism. PloS one Jan;3(8): e3067.
[6]
Sadananda M, W？hr M, Schwarting RKW (2008) Playback of 22-kHz and 50-kHz ultrasonic vocalizations induces differential c-fos expression in rat brain. Neuroscience letters Apr 11;435(1): 17–23.
[7]
Bollen B, Bouslama M, Matrot B, D'Hooge R, Van den Bergh O, et al. (2007) Learned defense response to hypoxia in newborn mice. Neuroscience letters Jun 15;420(3): 268–72.
[8]
Branchi I, Santucci D, Vitale a, Alleva E (1998) Ultrasonic vocalizations by infant laboratory mice: a preliminary spectrographic characterization under different conditions. Developmental psychobiology Nov;33(3): 249–56.
[9]
Ahrens AM, Ma ST, Maier EY, Duvauchelle CL, Schallert T (2009) Repeated intravenous amphetamine exposure: rapid and persistent sensitization of 50-kHz ultrasonic trill calls in rats. Behavioural brain research Jan;197(1): 205–9.
[10]
Burgdorf J, Kroes Ra, Moskal JR, Pfaus JG, Brudzynski SM, et al. (2008) Ultrasonic vocalizations of rats (Rattus norvegicus) during mating, play, and aggression: Behavioral concomitants, relationship to reward, and self-administration of playback. Journal of comparative psychology Nov; 122(4): 357–67.
[11]
Portfors CV (2007) Types and functions of ultrasonic vocalizations in laboratory rats and mice. Journal of the American Association for Laboratory Animal Science: JAALAS Jan; 46(1): 28–34.
[12]
Scattoni ML, Ricceri L, Crawley JN (2010) Unusual repertoire of vocalizations in adult BTBR T+tf/J mice during three types of social encounters. Genes, brain, and behavior Jul: 1–13.
[13]
Timmer M, Sandi C (2010) A role for glucocorticoids in the long-term establishment of a social hierarchy. Psychoneuroendocrinology Nov; 35(10): 1543–52.
[14]
Bourgeron T, Jamain S, Granon S (2006) Animal models of autism: Focus on genetic models and behavioral test paradigms. In: Fisch GS, Flint J, editors. Transgenic and knockout models of neuropschiatric diseases. Contemporary clinic neuroscience, Humana Press Inc. pp. 151–174.
[15]
Jamain S, Radyushkin K, Hammerschmidt K, Granon S, Boretius S, et al. (2008) Reduced social interaction and ultrasonic communication in a mouse model of monogenic heritable autism. Proc of the Natl Acad Sci U S A Feb 5; 105(5): 1710–5.
[16]
Enard W, Gehre S, Hammerschmidt K, H？lter SM, Blass T, et al. (2009) A humanized version of Foxp2 affects cortico-basal ganglia circuits in mice. Cell May; 137(5): 961–71.
[17]
R Development Core Team (2011) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, URL http://www.R-project.org/.
[18]
Panksepp JB, Jochman Ka, Kim JU, Koy JJ, Wilson ED, et al. (2007) Affiliative behavior, ultrasonic communication and social reward are influenced by genetic variation in adolescent mice. PloS one Jan; 2(4): e351.
[19]
Holy TE, Guo Z (2005) Ultrasonic songs of male mice. PLoS biology Dec; 3(12): e386.
[20]
Hammerschmidt K, Radyushkin K, Ehrenreich H, Fischer J (2009) Female mice respond to male ultrasonic “songs” with approach behaviour. Biology letters Oct; 5(5): 589–92.
[21]
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, and behavior Jun: 1–11.
[22]
Hoffmann F, Musolf K, Penn DJ (2009) Freezing urine reduces its efficacy for eliciting ultrasonic vocalizations from male mice. Physiology & behavior Mar; 96(4–5): 602–5.
[23]
Brudzynski SM (2007) Ultrasonic calls of rats as indicator variables of negative or positive states: acetylcholine-dopamine interaction and acoustic coding. Behavioural brain research Sep; 182(2): 261–73.
[24]
Brudzynski SM, Ociepa D (1992) Ultrasonic vocalization of laboratory rats in response to handling and touch. Physiology & behavior Oct; 52(4): 655–60.
[25]
Brudzynski SM, Chiu EM (1995) Behavioural responses of laboratory rats to playback of 22 kHz ultrasonic calls. Physiology & behavior Jun; 57(6): 1039–44.
[26]
Borta A, W？hr M, Schwarting RKW (2006) Rat ultrasonic vocalization in aversively motivated situations and the role of individual differences in anxiety-related behavior. Behavioural brain research Jan 30; 166(2): 271–80.
[27]
Hegoburu C, Shionoya K, Garcia S, Messaoudi B, Thévenet M, et al. (2011) The RUB Cage: Respiration-Ultrasonic Vocalizations-Behavior Acquisition Setup for Assessing Emotional Memory in Rats. Frontiers in behavioral neuroscience Jan; 5: 25.
[28]
Litvin Y, Blanchard DC, Blanchard RJ (2007) Rat 22 kHz ultrasonic vocalizations as alarm cries. Behavioural brain research Sep 4; 182(2): 166–72.
[29]
McGregor PK, Dabelsteen T (1996) Communication networks. In: Kroodsma DE, Miller EH, editors. Ecology and Evolution of Acoustic Communication in Birds. Ithaca: Cornell University Press. pp. 409–425.
[30]
Fendt M, Schwienbacher I, Schnitzler H-U (2006) Carbachol injections into the nucleus accumbens induce 50 kHz calls in rats. Neuroscience letters Jun 19; 401(1–2): 10–5.
[31]
Brudzynski SM, Pniak A (2002) Social contacts and production of 50-kHz short ultrasonic calls in adult rats. Journal of Comparative Psychology 116(1): 73–82.
[32]
Elie JE, Soula HA, Mathevon N, Vignal C (2011) Dynamics of communal vocalizations in a social songbird, the zebra finch (Taeniopygia guttata). The Journal of the Acoustical Society of America Jun; 129(6): 4037.
[33]
Scherer KR, Zei B (1988) Vocal indicators of affective disorders. Psychotherapy and psychosomatics Jan; 49(3–4): 179–86.
[34]
Schehka S, Esser K-H, Zimmermann E (2007) Acoustical expression of arousal in conflict situations in tree shrews (Tupaia belangeri). Journal of comparative physiology. A, Neuroethology, sensory, neural, and behavioral physiology Aug; 193(8): 845–52.
[35]
Rendall D (2011) Acoustic correlates of caller identity and affect intensity in the vowel-like grunt vocalizations of baboons. The Journal of the Acoustical Society of America Jun; 113(6): 3390–402.
[36]
Meise K (2008) Information content of female chacma baboon grunts - The signallers potential to utter functionnally referential grunts. Diploma thesis. University of Bielefeld, Germany.
[37]
Moles A, Costantini F, Garbugino L, Zanettini C, D'Amato FR (2007) Ultrasonic vocalizations emitted during dyadic interactions in female mice: a possible index of sociability? Behavioural brain research Sep; 182(2): 223–30.
[38]
W？hr M, Schwarting RKW (2009) Ultrasonic communication in rats: Effects of morphine and naloxone on vocal and behavioral responses to playback of 50-kHz vocalizations. Pharmacology, biochemistry, and behavior Dec; 94(2): 285–95.
[39]
Menuet C, Cazals Y, Gestreau C, Borghgraef P, Gielis L, et al. (2011) Age-Related Impairment of Ultrasonic Vocalization in Tau.P301L Mice: Possible Implication for Progressive Language Disorders. PloS ONE Jan; 6(10): e25770.
[40]
Grimsley JMS, Monaghan JJM, Wenstrup JJ (2011) Development of Social Vocalizations in Mice. PLoS ONE Mar; 6(3): e17460.
[41]
Takahashi N, Kashino M, Hironaka N (2010) Structure of rat ultrasonic vocalizations and its relevance to behavior. PloS ONE Jan; 5(11): e14115.
[42]
Hamilton SM, Spencer CM, Harrison WR, Yuva-Paylor La, Graham DF, et al. (2011) Multiple autism-like behaviors in a novel transgenic mouse model. Behavioural brain research Mar 17; 218(1): 29–41.
[43]
Hoffmann F, Musolf K, Penn DJ (2011) Spectrographic analyses reveal signals of individuality and kinship in the ultrasonic courtship vocalizations of wild house mice. Physiology & behavior Oct; 105(3): 766–771.
[44]
Arriaga G, Jarvis ED (2011) Of Mice, Birds, and Men. Diploma thesis. Duke university, USA.
[45]
Moy SS, Nadler JJ, Magnuson TR, Crawley JN (2006) Mouse Models of Autism Spectrum Disorders: The Challenge for Behavioral Genetics. Autism 51(7146): 40–51.
[46]
Ey E, Leblond CS, Bourgeron T (2011) Behavioral profiles of mouse models for autism spectrum disorders. Autism research: official journal of the International Society for Autism Research Feb; 4(1): 5–16.
[47]
W？hr M, Schwarting RKW (2007) Ultrasonic communication in rats: can playback of 50-kHz calls induce approach behavior? PloS ONE Jan; 2(12): e1365.
