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Cited by 25Animal Vocal Communication and BehaviorGenetics and Neurodevelopmental DisordersNeuroendocrine regulation and behavior

Sex differences in the acoustic features of social play‐induced 50‐kHz ultrasonic vocalizations: A detailed spectrographic analysis in wild‐type Sprague–Dawley and Cacna1c haploinsufficient rats

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Kisko, Theresa M., Schwarting, Rainer K. W., Wöhr, Markus·2021·Developmental Psychobiology
DOI 10.1002/dev.21998
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Abstract

Sexual dimorphisms are widespread in the animal kingdom. At the behavioral level, there is evidence for sex differences in social play behavior. In rats, males typically engage more in rough‐and‐tumble play than females. One prominent component of the rough‐and‐tumble play repertoire in rats is the emission of 50‐kHz ultrasonic vocalizations (USV). Such 50‐kHz USV reflect the rewarding nature of play and serve as socioaffective signals. Here, we provide evidence for sexual dimorphisms within rough‐and‐tumble play‐induced 50‐kHz USV in juvenile rats. Specifically, females displayed reduced 50‐kHz USV emission during playful interactions. This reduction was associated with changes in 50‐kHz USV emission rates and subtype profiles during specific rough‐and‐tumble components, i.e., pinning, wrestling, and chasing, as well as differences in acoustic parameters. Interestingly, sex differences were modulated by Cacna1c, a gene strongly implicated in major neuropsychiatric disorders, often characterized by prominent sex biases, most notably autism. Specifically, Cacna1c haploinsufficiency affected the emission of 50‐kHz USV during rough‐and‐tumble play in female rats and we provide evidence supporting the notion that such effects of Cacna1c haploinsufficiency are driven by male‐typical features of 50‐kHz USV emission. This is in line with the hypermasculinized social play repertoire previously observed in juvenile Cacna1c haploinsufficient females.

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  • Juvenile male rats produce more USVs than females during social play including during pinning.

    “Juvenile male rats exhibit more playful initiation behaviour than females ( Meaney & Stewart, 1981; Pellis & Pellis, 1990; Thor & Holloway, 1984) and produce more USVs than females during social play including during pinning ( Kisko et al., 2021).”

    From Stage 2 Registered Report: Refinement of tickling protocols to improve positive animal welfare in laboratory rats (2025) · cites this paper as Kisko et al., 2021

    Section 4.1 reports that males produced more 50-kHz USVs during social play, but the sex difference was confined to wrestling among the individual play components. It explicitly states that USV emission rates during pinning did not differ between sexes. The copy does not provide a page number for this passage. (LLM, conf=0.92)

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  1. S Auger, A. P., & Olesen, K. M. (2009). Brain sex differences and the organi- sation of juvenile social play behaviour. Journal of Neuroendocrinology, 21, 519-525. https://doi.org/10.1111/j.1365-2826.2009.01871.x · DOI · Paper page
  2. Biben, M. (2010). Individual-and sex-related strategies of wrestling play in captive squirrel monkeys. Ethology, 71, 229-241. https://doi. org/10.1111/j.1439-0310.1986.tb005 86.x Blanchard, R. J., Agullana, R., McGee, L., Weiss, S., & Blanchard, D. C. (1992). Sex differences in the incidence and sonographic characteris- tics of antipredator ultrasonic cries in the laboratory rat (Rattus nor- vegicus). Journal of Comparative Psychology, 106, 270-277. https:// doi.org/10.1037/0735-7036.106.3.270 · DOI
  3. Burgdorf, J., Panksepp, J., Brudzynski, S. M., Beinfeld, M. C., Cromwell, H. C., Kroes, R. A., & Moskal, J. R. (2009). The effects of selective breeding for differential rates of 50-kHz ultrasonic vocalizations on emotional behavior in rats. Developmental Psychobiology: The Journal of the International Society for Developmental Psychobiology, 51, 34- 46. https://doi.org/10.1002/dev.20343 · DOI
  4. Burke, C. J., Kisko, T. M., Euston, D. R., & Pellis, S. M. (2018). Do juve- nile rats use specific ultrasonic calls to coordinate their social play? Animal Behaviour, 140, 81-92. https://doi.org/10.1016/j.anbeh av.2018.03.019 · DOI · Paper page
  5. Dao, D. T., Mahon, P. B., Cai, X., Kovacsics, C. E., Blackwell, R. A., Arad, M., … Gould, T. D. (2010). Mood disorder susceptibility gene CACNA1C modifies mood-related behaviors in mice and interacts with sex to influence behavior in mice and diagnosis in humans. Biological Psychiatry, 68, 801-810. https://doi.org/10.1016/j.biops ych.2010.06.019 · DOI
  6. Engelhardt, K. A., Fuchs, E., Schwarting, R. K. W., & Wöhr, M. (2017). Effects of amphetamine on pro-social ultrasonic communica- tion in juvenile rats: Implications for mania models. European Neuropsychopharmacology, 27, 261-273. https://doi.org/10.1016/j. euron euro.2017.01.003 · DOI
  7. Geurts, A. M., Cost, G. J., Freyvert, Y., Zeitler, B., Miller, J. C., Choi, V. M., Buelow, R. (2009). Knockout Rats via Embryo Microinjection of Zinc- Finger Nucleases. Science, 325(5939), 433.
  8. Green, E. K., Grozeva, D., Jones, I., Jones, L., Kirov, G., Caesar, S., … Craddock, N. (2010). The bipolar disorder risk allele at CACNA1C also confers risk of recurrent major depression and of schizophre- nia. Molecular Psychiatry, 15, 1016-1022. https://doi.org/10.1038/ mp.2009. · DOI · Paper page
  9. Homberg, J. R., Wöhr, M., & Alenina, N. (2017). Comeback of the rat in biomedical research. ACS Chemical Neuroscience, 8, 900-903. https://doi.org/10.1021/acsch emneu ro.6b00415 · DOI
  10. Inagaki, H., Takeuchi, Y., & Mori, Y. (2012). Close relationship between the frequency of 22-kHz calls and vocal tract length in male rats. Physiology & Behavior, 106, 224-228. https://doi.org/10.1016/j. physb eh.2012.01.018 · DOI
  11. Kennedy, D. P., & Adolphs, R. (2012). The social brain in psychiatric and neurological disorders. Trends in Cognitive Sciences, 16, 559-572. https://doi.org/10.1016/J.TICS.2012.09.006 · DOI
  12. Kisko, T. M., Braun, M. D., Michels, S., Witt, S. H., Rietschel, M., Culmsee, C., … Wöhr, M. (2018). Cacna1c haploinsufficiency leads to pro-social 50-kHz ultrasonic communication deficits in rats. Disease Models and Mechanisms, 11, dmm032116. https://doi. org/10.1242/dmm.034116 · DOI
  13. Kisko, T. M., Braun, M. D., Michels, S., Witt, S. H., Rietschel, M., Culmsee, C., … Wöhr, M. (2020). Sex-dependent effects of Cacna1c haploin- sufficiency on juvenile social play behavior and pro-social 50-kHz ultrasonic communication in rats. Genes, Brain and Behavior, 19, e12552. https://doi.org/10.1111/gbb.12552 · DOI
  14. Kisko, T. M., Euston, D. R., & Pellis, S. M. (2015). Are 50-khz calls used as play signals in the playful interactions of rats? III. The effects of devo- calization on play with unfamiliar partners as juveniles and as adults. Behavioural Processes, 113, 113-121. https://doi.org/10.1016/j. beproc.2015.01.016 · DOI
  15. Kisko, T. M., Himmler, B. T., Himmler, S. M., Euston, D. R., & Pellis, S. M. (2015). Are 50-kHz calls used as play signals in the playful in- teractions of rats? II. Evidence from the effects of devocaliza- tion. Behavioural Processes, 111, 25-33. https://doi.org/10.1016/j. beproc.2014.11.011 · DOI
  16. Kisko, T. M., Wöhr, M., Pellis, V. C., & Pellis, S. M. (2015). From Play to Aggression: High-Frequency 50-kHz Ultrasonic Vocalizations as Play and Appeasement Signals in Rats. In M. Wöhr, & S. Krach (Eds.), Current Topics in Behavioral Neurosciences, (Vol. 30, pp. 91-108). https://doi.org/10.1007/7854_2015_432 · DOI · Paper page
  17. Knutson, B., Burgdorf, J., & Panksepp, J. (1998). Anticipation of play elicits high-frequency ultrasonic vocalizations in young rats. Journal of Comparative Psychology, 112, 65-73. https://doi. org/10.1037/0735-7036.112.1.65 · DOI
  18. Lai, M.-C., Lombardo, M. V., & Baron-Cohen, S. (2014). Autism. The Lancet, 383, 896-910. https://doi.org/10.1016/S0140 -6736(13)61539 -1 · DOI · Paper page
  19. Lenell, C., & Johnson, A. M. (2017). Sexual dimorphism in laryngeal muscle fibers and ultrasonic vocalizations in the adult rat. The Laryngoscope, 127, E270-E276. https://doi.org/10.1002/lary.26561 · DOI
  20. Lukas, M., & Wöhr, M. (2015). Endogenous vasopressin, in- nate anxiety, and the emission of pro-social 50-kHz ultra- sonic vocalizations during social play behavior in juvenile rats. Psychoneuroendocrinology, 56, 35-44. https://doi.org/10.1016/j. psyne uen.2015.03.005 · DOI
  21. Meaney, M. J., Stewart, J., Poulin, P., & McEwen, B. S. (1983). Sexual dif- ferentiation of social play in rat pups is mediated by the neonatal androgen-receptor system. Neuroendocrinology, 37, 85-90. https:// doi.org/10.1159/00012 3524 · DOI · Paper page
  22. Meyer-Lindenberg, A., & Tost, H. (2012). Neural mechanisms of social risk for psychiatric disorders. Nature Neuroscience, 15, 663-668. https://doi.org/10.1038/nn.3083 · DOI
  23. Olioff, M., & Stewart, J. (1978). Sex differences in the play behavior of prepubescent rats. Physiology & Behavior, 20, 113-115. https://doi. org/10.1016/0031-9384(78)90060 -4 · DOI · Paper page
  24. Olivier, B., & Mos, J. (1992). Rodent models of aggressive behavior and serotonergic drugs. Progress in Neuro-Psychopharmacology and Biological Psychiatry, 16, 847-870. https://doi.org/10.1016/0278- 5846(92)90104 -M Owens, N. W. (1975). Social play behaviour in free-living baboons, Papio anubis. Animal Behaviour, 23, 387-408. https://doi. org/10.1016/0003-3472(75)90087 -1 · DOI
  25. Panksepp, J., & Burgdorf, J. (2003). "Laughing" rats and the evolution- ary antecedents of human joy? Physiology and Behavior, 79, 533-547. https://doi.org/10.1016/S0031 -9384(03)00159 -8 · DOI
  26. Pellis, S. M., & McKenna, M. M. (1992). Intrinsic and extrinsic influences on play fighting in rats: Effects of dominance, partner's playfulness, temperament and neonatal exposure to testosterone propionate. Behavioural Brain Research, 50, 135-145. https://doi.org/10.1016/ S0166 -4328(05)80295 -5 · DOI · Paper page
  27. Pellis, S. M., & McKenna, M. M. (1995). What do rats find rewarding in play fight- ing?-an analysis using drug-induced non-playful partners. Behavioural Brain Research, 68, 65-73. https://doi.org/10.1016/0166-4328(94)00161 -8 · DOI
  28. Pellis, S. M., & Pellis, V. C. (1990). Differential rates of attack, defense, and counterattack during the developmental decrease in play fight- ing by male and female rats. Developmental Psychobiology, 23, 215- 231. https://doi.org/10.1002/dev.42023 0303 · DOI · Paper page
  29. Pellis, S. M., Pellis, V. C., & Dewsbury, D. A. (1989). Different levels of complexity in the play-fighting by muroid rodents appear to result from different levels of intensity of attack and defense. Aggressive Behavior, 15, 297-310. https://doi.org/10.1002/ab.24801 50405 · DOI · Paper page
  30. Pellis, S. M., Pellis, V. C., & McKenna, M. M. (1994). Feminine dimension in the play fighting of rats (Rattus norvegicus) and its defeminization neonatally by androgens. Journal of Comparative Psychology, 108, 68. https://doi.org/10.1037/0735-7036.108.1.68 · DOI · Paper page
  31. Pereira, M., Andreatini, R., Schwarting, R. K. W., & Brenes, J. C. (2014). Amphetamine-induced appetitive 50-kHz calls in rats: A marker of affect in mania? Psychopharmacology (Berl), 231, 2567-2577. https:// doi.org/10.1007/s0021 3-013-3413-1 · DOI
  32. Potasiewicz, A., Holuj, M., Piotrowska, D., Zajda, K., Wojcik, M., Popik, P., & Nikiforuk, A. (2019). Evaluation of ultrasonic vocalizations in a neu- rodevelopmental model of schizophrenia during the early life stages of rats. Neuropharmacology, 146, 28-38. https://doi.org/10.1016/J. NEURO PHARM.2018.11.023 · DOI
  33. Prum, R. O. (2010). Phylogenetic analysis of the evolution of display behavior in the neotropical manakins (Aves: Pipridae). Ethology, 84, 202-231. https://doi.org/10.1111/j.1439-0310.1990.tb007 98.x Redecker, T. M., Kisko, T. M., Schwarting, R. K. W., & Wöhr, M. (2019). Effects of Cacna1c haploinsufficiency on social interaction behavior and 50-kHz ultrasonic vocalizations in adult female rats. Behavioural Brain Research, 367, 35-52. https://doi.org/10.1016/J.BBR.2019.03.032 · DOI
  34. Symons, D. (1978). Play and aggression: A study of rhesus monkeys. New York: Columbia University Press.
  35. Taylor, G. T., Frechmann, T., & Royalty, J. (1986). Social behaviour and testicular activity of juvenile rats. Journal of Endocrinology, 110, 533- 537. https://doi.org/10.1677/joe.0.1100533 · DOI
  36. Williams, T. M., & Carroll, S. B. (2009). Genetic and molecular insights into the development and evolution of sexual dimorphism. Nature Reviews Genetics, 10, 797-804. https://doi.org/10.1038/nrg2687 · DOI
  37. Wöhr, M., Rippberger, H., Schwarting, R. K. W., & Van Gaalen, M. M. (2015). Critical involvement of 5-HT2C receptor function in am- phetamine-induced 50-kHz ultrasonic vocalizations in rats. Psychopharmacology (Berl), 232, 1817-1829. https://doi.org/10.1007/ s0021 3-014-3814-9 · DOI

Cited by

Sorted by citations

Authors
Kisko, T. M., Schwarting, R. K. W., & Wöhr, M.
Affiliations
Philipps University of Marburg (DE)
Corresponding author
Wöhr, Markus
ORCID
Venue
Developmental Psychobiology
Publisher
Wiley
Published
2020-06-07
Volume
63
Issue
2
Pages
262-276
ISSN
  • 0012-1630 (ISSN-L)
  • 1098-2302
DOI
10.1002/dev.21998
OpenAlex
W3034040458
Cited by
25
References
6
Citations by year
2026: 5 · 2025: 3 · 2024: 1 · 2023: 6 · 2022: 3 · 2021: 7
FWCI
3.72
Type
journal article
Language
en
Open access
Licence
Locations
  • Developmental Psychobiology (publishedVersion, cc-by-nc-nd)
  • PubMed (publishedVersion)
  • Lirias (KU Leuven) (submittedVersion, cc-by-nc-nd)
  • University of Southern Denmark Research Portal (University of Southern Denmark) (submittedVersion, cc-by-nc-nd)
Funders
Deutsche Forschungsgemeinschaft (DFG 559/14‐1, DFG 559/14‐2, DFG WO 1732/4‐1, DFG WO 1732/4‐2)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Developmental Biology › Animal Vocal Communication and Behavior
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetics and Neurodevelopmental Disorders
  • Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
Keywords
sex differences, 50-kHz ultrasonic vocalizations, social play, rough-and-tumble play, CACNA1C, haploinsufficiency, autism spectrum disorder, acoustic features, young rats, social communication, pinning, wrestling, pursuit
MeSH terms
Acoustics, Animals, Female, Male, Sex Characteristics, Social Behavior, Vocalization, Animal, Rats, Sprague-Dawley, Calcium Channels, L-Type, Rats, Haploinsufficiency

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