Are 50-kHz calls used as play signals in the playful interactions of rats? II. Evidence from the effects of devocalization

Behavioural Processes

Volumn 111, Issue , 2015, Pages 25-33

  Kisko, Theresa M ^a   Himmler, Brett T ^a   Himmler, Stephanie M ^a   Euston, David R ^a   Pellis, Sergio M ^a  

^a UNIVERSITY OF LETHBRIDGE   (Canada)

Author keywords

Communication; Devocalization; Emotion; Play behavior; Play signals; Ultrasonic vocalizations

Indexed keywords

COMMUNICATION BEHAVIOR; FREQUENCY-MAGNITUDE DISTRIBUTION; PLAY; RODENT; SIGNALING; ULTRASONICS; VOCALIZATION;

ANIMAL BEHAVIOR; ARTICLE; CONTROLLED STUDY; GROOMING; MALE; MOOD; NONHUMAN; PLAY; PREDICTION; RAT; SOCIAL INTERACTION; STARTLE REFLEX; VOCALIZATION; WRESTLING; AGGRESSION; ANIMAL; HUMAN RELATION; LONG EVANS RAT; PHYSIOLOGY; PSYCHOLOGY; RECREATION;

RATTUS;

AGGRESSION; ANIMALS; GROOMING; INTERPERSONAL RELATIONS; MALE; PLAY AND PLAYTHINGS; RATS; RATS, LONG-EVANS; VOCALIZATION, ANIMAL;

EID: 84912120669     PISSN: 03766357     EISSN: 18728308     Source Type: Journal    
DOI: 10.1016/j.beproc.2014.11.011     Document Type: Article

References (75)

1. Beatty W., Costello K. Olfactory bulbectomy and play fighting in juvenile rats. Physiol. Behav. 1983, 30:525-528.
2. Bekoff M. Social play in coyotes, wolves, and dogs. Bioscience 1974, 24:225-230.
3. Bekoff M. The communication of play intention: are play signals functional?. Semiotica 1975, 15:231-239.
4. Bekoff M. Play signals as punctuation: the structure of social play in canids. Behaviour 1995, 132:419-429. 10.2307/4535273.
5. Biben M., Symmes D. Play vocalizations of squirrel monkeys (Saimiri sciureus). Folia Primatol. 1986, 46:173-182.
6. Braune P., Schmidt S.a., Zimmermann E. Spacing and group coordination in a nocturnal primate, the golden brown mouse lemur (Microcebus ravelobensis): the role of olfactory and acoustic signals. Behav. Ecol. Sociobiol. 2005, 58:587-596.
7. Brudzynski S. Communication of adult rats by ultrasonic vocalization: biological, sociobiological and neuroscience approaches. ILAR J 2009, 50:43-50.
8. Brudzynski S.M. Ultrasonic calls of rats as indicator variables of negative or positive states: acetylcholine-dopamine interaction and acoustic coding. Behav. Brain Res. 2007, 182:261-273. 10.1016/j.bbr.2007.03.004.
9. Burgdorf J., Kroes R., Moskal J., Pfaus J., Brudzynski S., Panksepp J. Ultrasonic vocalization of rats during mating, play and aggression: behavioral concomitants, relationship to reward, and self-administration of playback. J. Comp. Psychol. 2008, 122:357-367.
10. Burgdorf J., Panksepp J. Tickling induces reward in adolescent rats. Physiol. Behav. 2001, 72:167-173. 10.1016/s0031-9384(00)00411-x.
11. Burgdorf J., Panksepp J., Moskal J.R. Frequency-modulated 50kHz ultrasonic vocalizations: a tool for uncovering the molecular substrates of positive affect. Neurosci. Biobehav. Rev. 2011, 35:1831-1836. 10.1016/j.neubiorev.2010.11.011.
12. Cheney D. Interactions of immature male and female baboons with adult females. Anim. Behav. 1978, 26:389-408. 10.1016/0003-3472(78)90057-X.
13. Choong K., Shen R. Prenatal ethanol exposure alters the postnatal development of spontaneous electrical activity of dopamine neurons in the ventral tegmental area. Neuroscience 2004, 126:1083-1091.
14. Cloutier S., Panksepp J., Newberry R. Playful handling by caretakers reduces fear of human in the laboratory rat. Appl. Anim. Behav. Sci. 2012, 140:161-171.
15. Ewer R.F. The biology and behaviour of a free-living population of black rats (Rattus rattus). Anim. Behav. Monogr. 1971, 4:125-174.
16. Fagen R. Animal Play Behavior 1981, Oxford University Press, New York.
17. Himmler B.T., Kisko T., Euston D., Kolb B., Pellis S.M. Are 50-kHz calls used as play signals in the playful interactions of rats? I. Evidence from the timing and context of their use. Behav. Process. 2014, 106:60-66.
18. Himmler B.T., Pellis V.C., Pellis S.M. Peering into the dynamics of social interactions: measuring play fighting in rats. 2013, Retrieved from http://www.jove.com/video/4288.
19. Hohmann G.M., Herzog M.O. Vocal communication in lion-tailed macaques (Macaca silenu). Folia Primatol. 1985, 45:148-178.
20. Ikemoto S., Panksepp J. The effects of early social isolation on the motivation for social play in juvenile rats. Dev. Psychobiol. 1992, 25:261-274. 10.1002/dev.420250404.
21. Kahana A., Rozin A., Weller A. Social play with an unfamiliar group in weanling rats (Rattus norvegicus). Dev. Psychobiol. 1997, 30:165-176.
22. Kipper S., Todt D. The use of vocal signals in the social play of Barbary macaques. Primates 2002, 43:3-17.
23. Knutson B., Burgdorf J., Panksepp J. Anticipation of play elicits high frequency ultrasonic vocalizations in young rats. J. Comp. Psychol. 1998, 112:65-73.
24. Knutson B., Burgdorf J.a., Panksepp J. Ultrasonic vocalizations as indices of affective states in rats. Psychol. Bull. 2002, 128:961-977.
25. LeResche L.A. Dyadic play in Hamadryas baboons. Behaviour 1976, 57:290-305.
26. Lore R., Flannelly K.a., Farina P. Ultrasounds produced by rats accompany decreases in intraspecific fighting. Aggressive Behav. 1976, 2:175-181.
27. Masataka N., Kohda M. Primate play vocalizations and their functional significance. Folia Primatol. 1988, 50:152-156.
28. Meaney M.J., Stewart J. Neonatal androgens influence the social play of prepubescent rats. Horm. Behav. 1981, 15:197-213.
29. Palagi E. Sharing the motivation to play: the use of signals in adult bonobos. Anim. Behav. 2008, 75:887-896.
30. Palagi E., Mancini G. Playing with the face: playful facial "chattering" and signal modulation in a monkey species (Theropithecus gelada). J. Comp. Psychol. 2011, 125:11.
31. Panksepp J. The ontogeny of play in rats. Dev. Psychobiol. 1981, 14:327-332.
32. Panksepp J., Beatty W. Social deprivation and play in rats. Behav. Neural. Biol. 1980, 30:197-206.
33. 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, 115:25-38.
34. Pellis S.M., McKenna M.M., Field E.F., Pellis V.C., Prusky G.T., Whishaw I.Q. Uses of vision by rats in play fighting and other close-quarter social interactions. Physiol. Behav. 1996, 59:905-913.
35. Pellis S.M., Pellis V.C. Play-fighting differs from serious fighting in both target of attack and tactics of fighting in the laboratory rat Rattus norvegicus. Aggressive Behav. 1987, 13:227-242.
36. Pellis S.M., Pellis V.C. Differential rates of attack, defense, and counterattack during the developmental decrease in play fighting by male and female rats. Dev. Psychobiol. 1990, 23:215-231.
37. Pellis S.M., Pellis V.C. Attack and defense during play fighting appear to be motivationally independent behaviors in muroid rodents. Psychol. Rec. 1991, 41:175-184.
38. Pellis S.M., Pellis V.C. Juvenilized play fighting in subordinate male rats. Aggressive Behav. 1992, 18:449-457.
39. Pellis S.M., Pellis V.C. Targets, tactics, and the open mouth face during play fighting in three species of primates. Aggressive Behav. 1997, 23:41-57.
40. Pellis S.M., Pellis V.C. To whom the play signal is directed: a study of headshaking in black-handed spider monkeys (Ateles geoffroyi). J. Comp. Psychol. 2011, 125:1-10.
41. Pellis S.M., Pellis V.C., Whishaw I.Q. The role of the cortex in play fighting by rats: developmental and evolutionary implications. Brain Behav. Evol. 1992, 39:270-284.
42. Pellis S.M., Pellis V.C., Foroud A. Play fighting: aggression, affiliation and the development of nuanced social skills. Developmental Origins of Aggression 2005, 47-62. Guilford Press, New York. R. Tremblay, W.W. Hartup, J. Archer (Eds.).
43. Pellis S.M., Pellis V.C., Reinhart C.J. The evolution of social play. Formative Experiences: The Interaction of Caregiving, Culture, and Developmental Psychobiology 2010, 404-431. Cambridge University Press, Cambridge, UK. C. Worthman, P. Plotsky, D. Schechter, C. Cummings (Eds.).
44. Pellis S.M., Pellis V.C., McKenna M.M. Feminine dimension in the play fighting of rats (Rattus norvegicus) and its defeminization neonatally by androgens. J. Comp. Psychol. 1994, 108:68-73.
45. Pellis S.M., Field E.F., Smith L.K., Pellis V.C. Multiple differences in the play fighting of male and female rats. Implications for the causes and functions of play. Neurosci. Biobehav. R 1997, 21:105-120.
46. Pellis S.M., Pellis V.C., Reinhart C.J., Thierry B. The use of the bared-teeth display during play fighting in Tonkean macaques (Macaca tonkeana): sometimes it is all about oneself. J. Comp. Psychol. 2011, 125:393-403.
47. Pellis S.M., Pellis V.C., Barrett L., Henzi S.P. One good turn deserves another: combat versus other functions of acrobatic maneuvers in the play fighting of vervet monkeys (Chlorocebus aethiops). Anim. Behav. Cog. 2014, 1:128-143.
48. Poole T.B., Fish J. An investigation of individual, age and sexual differences in the play of rats Rattus norvegicus (Mammalia: Rodentia). J. Zool. 1976, 179:249-260.
49. Portavella M., Depaulis A.a., Vergnes M. 22-28kHz ultrasonic vocalizations associated with defensive reactions in male rats do not result from fear or aversion. Psychopharmacology 1993, 111:190-194.
50. Rasa O. A motivational analysis of object play in juvenile dwarf mongooses (Helogale undulata rufula). Anim. Behav. 1984, 32:579-589.
51. Reinhart C.J., McIntyre D.C., Pellis S.M. The development of play fighting in kindling-prone (FAST) and kindling-resistant (SLOW) rats: how does the retention of phenotypic juvenility affect the complexity of play?. Dev. Psychobiol. 2004, 45:83-92.
52. Riters L.V. Pleasure seeking and birdsong. Neurosci. Biobehav. Rev. 2011, 35:1837-1845.
53. Sadananda M., Wöhr M.a., Schwarting R.K.W. Playback of 22-kHz and 50-kHz ultrasonic vocalizations induces differential c-fos expression in rat brain. Neurosci. Lett. 2008, 435:17-23. 10.1016/j.neulet.2008.02.002.
54. Sales G. Ultrasound and aggressive behaviour in rats and other small mammals. Anim. Behav. 1972, 20:88-100.
55. Siviy S., Panksepp J. Sensory modulation of juvenile play in rats. Dev. Psychobiol. 1987, 20:39-55.
56. Smith L., Fantella S.-L., Pellis S.M. Playful defensive responses in adult male rats depend on the status of the unfamiliar opponent. Aggressive Behav. 1999, 25:141-152.
57. Snoeren E., Amgo A. Female ultrasonic vocalizations have no incentive value for male rats. Behav. Neurosci. 2013, 127:439-450.
58. Stevenson M., Poole T. Playful interactions in family groups of the common marmoset (Callithrix jacchus jacchus). Anim. Behav. 1982, 30:886-900. 10.1016/S0003-3472(82)80163-2.
59. Takahashi L., Lore R. Play fighting and the development of agonistic behavior in male and female rats. Aggressive Behav. 1983, 9:217-227.
60. Thor D.H., Holloway W.R. Play-solicitation behavior in juvenile male and female rats. Anim. Learn. Behav. 1983, 11:173-178.
61. Thor D.H., Holloway W.R. Play soliciting in prepubertal and postpubertal rats. Anim. Learn. Behav. 1985, 13:327-330.
62. Thor D.H., Holloway W.R. Anosmia and play fighting behavior in prepubescent male and female rats. Physiol. Behav. 1982, 29:281-285. 10.1016/0031-9384(82)90016-6.
63. Thor D.H., Holloway W.R. Developmental analyses of social play behavior in juvenile rats. Bull. Psychonomic Soc. 1984, 22:587-590.
64. Van Hooff J. The Facial Displays of the Catarrhine Monkeys and Apes 1967, Weidenfield & Nicolson, London. D. Morris (Ed.).
65. Van Leeuwen E., Zimmermann E.A., Ross M. Responding to inequities: gorillas try to maintain their competitive advantage during play fights. Biol. Lett. 2011, 7:39-42.
66. Varlinskaya E., Spear L.a., Spear N. Social behavior and social motivation in adolescent rats: role of housing conditions and partner's activity. Physiol. Behav. 1999, 67:475-482. 10.1016/S0031-9384(98)00285-6.
67. Waller B., Dunbar R. Differential behavioural effects of silent bared teeth display and relaxed open mouth display in chimpanzees (Pan troglodytes). Ethology 2005, 111:129-142.
68. Willadsen M., Seffer D., Schwarting R.K.W., Wöhr M. Rodent ultrasonic communication: male prosocial 50-kHz ultrasonic vocalizations elicit social approach behavior on female rats. J. Comp. Psychol. 2014, 128:56-64.
69. Willey A., Spear L. Effects of ethanol on social approach and 50 kHz ultrasonic vocalization production in adolescent male Sprague-Dawley rats. Pharmacol. Biochem. Behav. 2013, 70:317-323.
70. Wöhr M., Houx B., Schwarting R.a., Spruijt B. Effects of experience and context on 50kHz vocalizations in rats. Physiol. Behav. 2008, 93:766-776.
71. Wöhr M., Schwarting R. Ultrasonic communication in rats: effects of morphine and naloxone on vocal and behavioral responses to playback of 50-kHz vocalizations. Pharmacol. Biochem. Behav. 2009, 94:285-295. 10.1016/j.pbb.2009.09.008.
72. Wöhr M., Schwarting R. Testing social acoustic memory in rats: effects of stimulus configuration and long-term memory on the induction of social approach behavior by appetitive 50-kHz ultrasonic vocalizations. Neurobiol. Learn. Mem. 2012, 98:154-164. 10.1016/j.nlm.2012.05.004.
73. Wöhr M., Kehl M., Borta A., Schänzer A., Schwarting R.K.W., Höglinger G.U. New insights into the relationship of neurogenesis and affect: tickling induces hippocampal cell proliferation in rats emitting appetitive 50-kHz ultrasonic vocalizations. Neuroscience 2009, 163:1024-1030.
74. Wright J., Gourdon J.a., Clarke P. Identification of multiple call categories within the rich repertoire of adult rat 50-kHz ultrasonic vocalizations: effects of amphetamine on social context. Psychopharmacology 2010, 211:1-13.
75. Zimmermann E. Acoustic Communication in Nocturnal Prosimians 1995, Plenum Press Div Plenum Publishing Corp, New York.