Specific 50-kHz vocalizations are tightly linked to particular types of behavior in juvenile rats anticipating play
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Rat ultrasonic vocalizations have been suggested to be either a byproduct of physical movement or, in the case of 50-kHz calls, a means to communicate positive affect. Yet there are up to 14 distinct types of 50-kHz calls, raising issues for both explanations. To discriminate between these theories and address the purpose for the numerous 50-kHz call types, we studied single juvenile rats that were waiting to play with a partner, a situation associated with a high number of 50-kHz calls. We used a Monte-Carlo shuffling procedure to identify vocalization-behavior correlations that were statistically different from chance. We found that certain call types ("split", "composite" and "multi-step") were strongly associated with running and jumping while other call types (those involving "trills") were more common during slower movements. Further, non-locomotor states such as resting and rearing were strongly predictive of a lack of vocalizations. We also found that the various sub-types of USVs can be clustered into 3-4 categories based on similarities in the way they are used. We did not find a one-to-one relationship between any movements and specific vocalizations, casting doubt on the motion byproduct theory. On the other hand, the use of specific calls during specific behaviors is problematic for the affect communication hypothesis. Based on our results, we suggest that ultrasonic calls may serve to coordinate moment-to-moment social interactions.
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Rats generally do not emit USVs when rearing.
“A comparison of USV data between groups with apparent differences in upright standing is complicated in that rats generally do not emit USVs when rearing.14”
From Ultrasonic Vocalization Analysis as a Novel Metric to Assess Cage Enrichment in Rats (2022) · cites this paper as [14]
The Results ('Specific correspondences between vocalizations and behaviors'; page not supplied) associate rearing with a marked reduction in the probability of calls, supporting the gist of the claim. But the study examined 50-kHz calls in juvenile rats anticipating play; it does not establish that rats generally do not emit USVs while rearing. (LLM, conf=0.84)
Experimental — accuracy not yet measuredExploration of distinct ultrasonic vocalizations has revealed a linkage between certain call types and behaviors.
“Exploration of distinct USVs has revealed a linkage between certain call types and behaviors.14”
From Ultrasonic Vocalization Analysis as a Novel Metric to Assess Cage Enrichment in Rats (2022) · cites this paper as [14]
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Burgdorf, J., Kroes, R. A., Moskal, J. R., Pfaus, J. G., Brudzynski, S. M., & Panksepp, J. (2008) · Journal of Comparative Psychology · doi:10.1037/a0012889 · Cited by 469 · see citing works
Himmler, B. T., Kisko, T. M., Euston, D. R., Kolb, B., & Pellis, S. M. (2014) · Behavioural Processes · doi:10.1016/j.beproc.2014.04.014 · Cited by 87 · see citing works
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Research works printed but not linked: 53
- [1]Brudzynski SM. Communication of adult rats by ultrasonic vocalization: biological, sociobiological, and neuroscience approaches. ILAR J. 2009; 50(1): 43– 50. Epub 2008/12/25. 19106451
- [2]Blumberg MS. Rodent ultrasonic short calls: locomotion, biomechanics, and communication. J Comp Psychol. 1992; 106(4): 360– 5. 1451418
- [3]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 (Berl). 2010; 211(1): 1– 13. Epub 2010/05/06. 20443111
- [4]Thiessen DD, Kittrell EMW, Graham JM. Biomechanics of Ultrasound Emissions in the Mongolian Gerbil, Meriones-Unguiculatus. Behavioral and Neural Biology. 1980; 29(4): 415– 29. 7447845
- [5]Roberts LH. The rodent ultrasound production mechanism. Ultrasonics. 1975; 13(2): 83– 8. 1167711
- [6]Sirotin YB, Costa ME, Laplagne DA. Rodent ultrasonic vocalizations are bound to active sniffing behavior. Front Behav Neurosci. 2014; 8: 399 Epub 2014/12/06. doi: 10.3389/fnbeh.2014.00399 25477796 PMC4235378 · DOI
- [7]Bramble DM, Carrier DR. Running and breathing in mammals. Science. 1983; 219(4582): 251– 6. 6849136
- [8]Alves JA, Boerner BC, Laplagne DA. Flexible Coupling of Respiration and Vocalizations with Locomotion and Head Movements in the Freely Behaving Rat. Neural Plast. 2016; 2016: 4065073 PubMed Central PMCID: PMCPMC4976156. doi: 10.1155/2016/4065073 27525126 PMC4976156 · DOI
- [9]Riede T. Stereotypic laryngeal and respiratory motor patterns generate different call types in rat ultrasound vocalization. J Exp Zool A Ecol Genet Physiol. 2013; 319(4): 213– 24. PubMed Central PMCID: PMCPMC3926509. doi: 10.1002/jez.1785 23423862 PMC3926509 · DOI
- [10]Riede T. Subglottal pressure, tracheal airflow, and intrinsic laryngeal muscle activity during rat ultrasound vocalization. J Neurophysiol. 2011; 106(5): 2580– 92. PubMed Central PMCID: PMCPMC3214115. doi: 10.1152/jn.00478.2011 21832032 PMC3214115 · DOI
- [11]Kisko TM, Himmler BT, Himmler SM, Euston DR, Pellis SM. Are 50-kHz calls used as play signals in the playful interactions of rats? II. Evidence from the effects of devocalization. Behav Processes. 2015; 111: 25– 33. doi: 10.1016/j.beproc.2014.11.011 25447515 · DOI
- [12]Kisko TM, Euston DR, Pellis SM. Are 50-khz calls used as play signals in the playful interactions of rats? III. The effects of devocalization on play with unfamiliar partners as juveniles and as adults. Behav Processes. 2015; 113: 113– 21. doi: 10.1016/j.beproc.2015.01.016 25643949 · DOI
- [13]Laplagne DA, Elias Costa M. Rats Synchronize Locomotion with Ultrasonic Vocalizations at the Subsecond Time Scale. Front Behav Neurosci. 2016; 10: 184 PubMed Central PMCID: PMCPMC5040720. doi: 10.3389/fnbeh.2016.00184 27746726 PMC5040720 · DOI
- [14]Knutson B, Burgdorf J, Panksepp J. Ultrasonic vocalizations as indices of affective states in rats. Psychol Bull. 2002; 128(6): 961– 77. 12405139
- [15]Blanchard RJ, Blanchard DC, Agullana R, Weiss SM. Twenty-two kHz alarm cries to presentation of a predator, by laboratory rats living in visible burrow systems. Physiol Behav. 1991; 50(5): 967– 72. Epub 1991/11/01. 1805287
- [16]Tonoue T, Ashida Y, Makino H, Hata H. Inhibition of shock-elicited ultrasonic vocalization by opioid peptides in the rat: a psychotropic effect. Psychoneuroendocrinology. 1986; 11(2): 177– 84. 2428074
- [17]Antoniadis EA, McDonald RJ. Discriminative fear conditioning to context expressed by multiple measures of fear in the rat. Behav Brain Res. 1999; 101(1): 1– 13. 10342394
- [18]Kikusui T, Nishizawa D, Takeuchi Y, Mori Y. Conditioned fear-related ultrasonic vocalizations are emitted as an emotional response. J Vet Med Sci. 2003; 65(12): 1299– 305. 14709817
- [19]Wohr M, Schwarting RKW. Ultrasonic calling during fear conditioning in the rat: no evidence for an audience effect. Animal Behaviour. 2008; 76: 749– 60.
- [20]Sales GD. Ultrasound and aggressive behaviour in rats and other small mammals. Anim Behav. 1972; 20(1): 88– 100. 4677167
- [21]Panksepp J, Burgdorf J, Beinfeld MC, Kroes RA, Moskal JR. Regional brain cholecystokinin changes as a function of friendly and aggressive social interactions in rats. Brain Res. 2004; 1025(1–2): 75– 84. doi: 10.1016/j.brainres.2004.07.076 15464747 · DOI · Paper page
- [22]Thomas DA, Takahashi LK, Barfield RJ. Analysis of ultrasonic vocalizations emitted by intruders during aggressive encounters among rats (Rattus norvegicus). J Comp Psychol. 1983; 97(3): 201– 6. 6684525
- [23]Kaltwasser MT. Startle-inducing acoustic stimuli evoke ultrasonic vocalization in the rat. Physiol Behav. 1990; 48(1): 13– 7. 2236259
- [24]Blanchard RJ, Flannelly KJ, Blanchard DC. Defensive behavior of laboratory and wild Rattus norvegicus. J Comp Psychol. 1986; 100(2): 101– 7. 3720282
- [25]Brudzynski SM, Ociepa D. Ultrasonic vocalization of laboratory rats in response to handling and touch. Physiol Behav. 1992; 52(4): 655– 60. 1409936
- [26]Knutson B, Burgdorf J, Panksepp J. High-frequency ultrasonic vocalizations index conditioned pharmacological reward in rats. Physiol Behav. 1999; 66(4): 639– 43. Epub 1999/07/01. 10386908
- [27]Bialy M, Rydz M, Kaczmarek L. Precontact 50-kHz vocalizations in male rats during acquisition of sexual experience. Behav Neurosci. 2000; 114(5): 983– 90. 11085613
- [28]Burgdorf J, Knutson B, Panksepp J. Anticipation of rewarding electrical brain stimulation evokes ultrasonic vocalization in rats. Behav Neurosci. 2000; 114(2): 320– 7. Epub 2000/06/01. 10832793
- [30]Panksepp J, Burgdorf J. 50-kHz chirping (laughter?) in response to conditioned and unconditioned tickle-induced reward in rats: effects of social housing and genetic variables. Behav Brain Res. 2000; 115(1): 25– 38. Epub 2000/09/21. 10996405
- [31]Wohr M, Houx B, Schwarting RK, Spruijt B. Effects of experience and context on 50-kHz vocalizations in rats. Physiol Behav. 2008; 93(4–5): 766– 76. doi: 10.1016/j.physbeh.2007.11.031 18191963 · DOI
- [32]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(2): 328– 36. Epub 2009/04/01. doi: 10.1037/a0014593 19331456 PMC2737695 · DOI
- [33]Takahashi N, Kashino M, Hironaka N. Structure of rat ultrasonic vocalizations and its relevance to behavior. PloS one. 2010; 5(11): e14115–e. doi: 10.1371/journal.pone.0014115 21124767 PMC2993931 · DOI
- [34]Grimsley JMS, Monaghan JJM, Wenstrup JJ. Development of Social Vocalizations in Mice. PLoS ONE. 2011; 6(3): e17460 doi: 10.1371/journal.pone.0017460 21408007 PMC3052362 · DOI
- [35]Hanson JL, Hurley LM. Female presence and estrous state influence mouse ultrasonic courtship vocalizations. PLoS One. 2012; 7(7): e40782 PubMed Central PMCID: PMCPMC3399843. doi: 10.1371/journal.pone.0040782 22815817 PMC3399843 · DOI
- [36]Brudzynski SM. Ethotransmission: communication of emotional states through ultrasonic vocalization in rats. Curr Opin Neurobiol. 2013; 23(3): 310– 7. Epub 2013/02/05. doi: 10.1016/j.conb.2013.01.014 23375168 · DOI · Paper page
- [37]Knutson B, Burgdorf J, Panksepp J. Anticipation of play elicits high-frequency ultrasonic vocalizations in young rats. J Comp Psychol. 1998; 112(1): 65– 73. Epub 1998/04/07. 9528115
- [38]Pellis SM, Pellis VC. The prejuvenile onset of play fighting in laboratory rats (Rattus norvegicus). Dev Psychobiol. 1997; 31(3): 193– 205. Epub 1997/12/05. 9386921
- [39]Himmler BT, Pellis SM, Kolb B. Juvenile play experience primes neurons in the medial prefrontal cortex to be more responsive to later experiences. Neurosci Lett. 2013; 556: 42– 5. doi: 10.1016/j.neulet.2013.09.061 24103373 · DOI
- [40]Niesink RJ, Van Ree JM. Involvement of opioid and dopaminergic systems in isolation-induced pinning and social grooming of young rats. Neuropharmacology. 1989; 28(4): 411– 8. 2546087
- [41]Panksepp J, Beatty WW. Social deprivation and play in rats. Behav Neural Biol. 1980; 30(2): 197– 206. 7447871
- [42]Pellis SM, Pellis VC. Differential rates of attack, defense, and counterattack during the developmental decrease in play fighting by male and female rats. Dev Psychobiol. 1990; 23(3): 215– 31. doi: 10.1002/dev.420230303 2379760 · DOI · Paper page
- [43]Muir G. Locomotion In: Whishaw IQ, Kolb B, editors. The behavior of the laboratory rat: a handbook with tests. Oxford;New York;: Oxford University Press; 2005 p. 150– 61.
- [44]Pellis SM, Pellis VC. Locomotor-rotational movements in the ontogeny and play of the laboratory rat RATTUS norvegicus. Developmental Psychobiology. 1983; 16(4): 269– 86. doi: 10.1002/dev.420160403 6884577 · DOI · Paper page
- [45]Gorzalka BB, Hanson LA. Sexual behavior and wet dog shakes in the male rat: regulation by corticosterone. Behav Brain Res. 1998; 97(1–2): 143– 51. 9867239
- [46]Aldridge JW. Grooming In: Whishaw IQ, Kolb B, editors. The behavior of the laboratory rat: a handbook with tests. Oxford;New York;: Oxford University Press; 2005 p. 141– 9.
- [47]Cai JJ, Smith DK, Xia X, Yuen KY. MBEToolbox: a MATLAB toolbox for sequence data analysis in molecular biology and evolution. BMC Bioinformatics. 2005; 6: 64 PubMed Central PMCID: PMCPMC1274259. doi: 10.1186/1471-2105-6-64 15780146 PMC1274259 · DOI
- [49]Wohr M, Schwarting RK. Ultrasonic communication in rats: can playback of 50-kHz calls induce approach behavior? PLoS One. 2007; 2(12): e1365 Epub 2007/12/27. PubMed Central PMCID: PMC2137933. doi: 10.1371/journal.pone.0001365 18159248 PMC2137933 · DOI
- [50]Brudzynski SM, Gibson B, Silkstone M, Burgdorf J, Kroes RA, Moskal JR, et al Motor and locomotor responses to systemic amphetamine in three lines of selectively bred Long-Evans rats. Pharmacol Biochem Behav. 2011; 100(1): 119– 24. doi: 10.1016/j.pbb.2011.08.006 21867727 · DOI
- [51]Mu P, Fuchs T, Saal DB, Sorg BA, Dong Y, Panksepp J. Repeated cocaine exposure induces sensitization of ultrasonic vocalization in rats. Neurosci Lett. 2009; 453(1): 31– 5. PubMed Central PMCID: PMCPMC2680749. doi: 10.1016/j.neulet.2009.02.007 19429010 PMC2680749 · DOI
- [52]Maier EY, Ma ST, Ahrens A, Schallert TJ, Duvauchelle CL. Assessment of ultrasonic vocalizations during drug self-administration in rats. J Vis Exp. 2010;(41). PubMed Central PMCID: PMCPMC3156074. PMC3156074 20689507
- [53]Thiessen DD, Davenport R, Graham M. Ultrasonic Signaling in Gerbil (Meriones-Unguiculatus)—Social-Interaction and Olfaction. Journal of Comparative and Physiological Psychology. 1978; 92(6): 1041– 9.
- [54]Brenes JC, Lackinger M, Hoglinger GU, Schratt G, Schwarting RK, Wohr M. Differential effects of social and physical environmental enrichment on brain plasticity, cognition, and ultrasonic communication in rats. J Comp Neurol. 2016; 524(8): 1586– 607. doi: 10.1002/cne.23842 26132842 · DOI · Paper page
- [55]Liberman AM, Cooper FS, Shankweiler DP, Studdert-Kennedy M. Perception of the speech code. Psychol Rev. 1967; 74(6): 431– 61. 4170865
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- Authors
- Burke, C. J., Kisko, T. M., Swiftwolfe, H., Pellis, S. M., & Euston, D. R.
- Affiliations
- University of Lethbridge (CA)
- Philipps University of Marburg (DE)
- Corresponding author
- Euston, David R.
- Venue
- PLOS ONE
- Publisher
- Public Library of Science (PLoS)
- Published
- 2017-05-03
- Volume
- 12
- Issue
- 5
- Pages
- e0175841
- ISSN
- 1932-6203 (ISSN-L)
- PMC
- PMC5414981
- OpenAlex
- W2611786193
- Cited by
- 78
- References
- 2
- Citations by year
- 2026: 10 · 2025: 10 · 2024: 7 · 2023: 10 · 2022: 6 · 2021: 11 · 2020: 7 · 2019: 9 · 2018: 7 · 2017: 1
- FWCI
- 6.10
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- PLoS ONE (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- Natural Sciences and Engineering Research Council of Canada (40058, 372305)
- Alberta Innovates - Health Solutions
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Developmental Biology › Animal Vocal Communication and Behavior
- Social Sciences › Psychology › Social Psychology › Primate Behavior and Ecology
- Physical Sciences › Environmental Science › Ecology › Marine animal studies overview
- Keywords
- ultrasonic vocalizations, 50-kHz calls, young rats, anticipatory behavior, play behavior, locomotion
- MeSH terms
- Animals, Behavior, Animal, Male, Social Behavior, Vocalization, Animal, Rats, Long-Evans, Rats
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