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Social play behavior, ultrasonic vocalizations and their modulation by morphine and amphetamine in Wistar and Sprague-Dawley rats

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Abstract

Rationale

Social play behavior is the most characteristic social behavior in young mammals. It is highly rewarding and crucial for proper neurobehavioral development. Despite the importance of genetic factors in normal and pathological social behaviors, little information is available about strain influences on social play.

Objective and methods

The aim of this study was to investigate differences in social play behavior, 50-kHz ultrasonic vocalizations (USVs) and their modulation by acute morphine and amphetamine administration in two rat strains widely used in behavioral pharmacology studies, i.e., Wistar and Sprague–Dawley rats.

Results

Sprague–Dawley rats showed higher levels of social play than Wistar rats. In both strains, no correlation was found between the performance of social behaviors and the emission of 50-kHz USVs. In Wistar and Sprague–Dawley rats, morphine increased and amphetamine decreased social play. The effects of morphine, however, were more pronounced in Wistar than Sprague–Dawley animals. In both strains, morphine did not affect USV emission, while amphetamine increased it during cage exploration. In Sprague–Dawley rats only, amphetamine decreased USVs during social interaction.

Conclusions

Wistar and Sprague–Dawley rats differ in their absolute levels of social play behavior and 50-kHz USVs, and quantitative differences exist in their response to pharmacological manipulations of social play. The emission of 50-kHz USVs and the behavioral parameters thought to reflect rewarding social interactions in adolescent rats are dissociable.

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References

  • Alessandri SM (1992) Attention, play, and social behavior in ADHD preschoolers. J Abnorm Child Psychol 20:289–302

    Article  PubMed  CAS  Google Scholar 

  • Baarendse PJJ, Counotte DS, O'Donnell P, Vanderschuren LJMJ (2013) Early social experience is critical for the development of cognitive control and dopamine modulation of prefrontal cortex function. Neuropsychopharmacology 38(8):1485–1494

    Google Scholar 

  • Barker DJ, Root DH, Ma S, Jha S, Megehee L, Pawlak AP, West MO (2010) Dose-dependent differences in short ultrasonic vocalizations emitted by rats during cocaine self-administration. Psychopharmacology (Berl) 211:435–442

    Article  CAS  Google Scholar 

  • Beatty WW, Costello KB, Berry SL (1984) Suppression of play fighting by amphetamine: effects of catecholamine antagonists, agonists and synthesis inhibitors. Pharmacol, Biochem Behav 20:747–755

    Article  CAS  Google Scholar 

  • Beatty WW, Dodge AM, Dodge LJ, White K, Panksepp J (1982) Psychomotor stimulants, social deprivation and play in juvenile rats. Pharmacol, Biochem Behav 16:417–422

    Article  CAS  Google Scholar 

  • Bolanos CA, Glatt SJ, Jackson D (1998) Subsensitivity to dopaminergic drugs in periadolescent rats: a behavioral and neurochemical analysis. Brain Res Dev Brain Res 111:25–33

    Article  PubMed  CAS  Google Scholar 

  • Brand T, Spanagel R, Schneider M (2012) Decreased reward sensitivity in rats from the Fischer344 strain compared to Wistar rats is paralleled by differences in endocannabinoid signaling. PLoS One 7:e31169

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Browning JR, Browning DA, Maxwell AO, Dong Y, Jansen HT, Panksepp J, Sorg BA (2011) Positive affective vocalizations during cocaine and sucrose self-administration: a model for spontaneous drug desire in rats. Neuropharmacology 61:268–275

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Burgdorf J, Knutson B, Panksepp J (2000) Anticipation of rewarding electrical brain stimulation evokes ultrasonic vocalization in rats. Behav Neurosci 114:320–327

    Article  PubMed  CAS  Google Scholar 

  • Burgdorf J, Knutson B, Panksepp J, Ikemoto S (2001) Nucleus accumbens amphetamine microinjections unconditionally elicit 50-kHz ultrasonic vocalizations in rats. Behav Neurosci 115:940–944

    Article  PubMed  CAS  Google Scholar 

  • Burgdorf J, Panksepp J (2006) The neurobiology of positive emotions. Neurosci Biobehav Rev 30:173–187

    Article  PubMed  Google Scholar 

  • Burgdorf J, Panksepp J, Brudzynski SM, Kroes R, Moskal JR (2005) Breeding for 50-kHz positive affective vocalization in rats. Behav Genet 35:67–72

    Article  PubMed  Google Scholar 

  • Burgdorf J, Panksepp J, Moskal JR (2011) Frequency-modulated 50 kHz ultrasonic vocalizations: a tool for uncovering the molecular substrates of positive affect. Neurosci Biobehav Rev 35:1831–1836

    Article  PubMed  Google Scholar 

  • Calcagnetti DJ, Schechter MD (1992) Place conditioning reveals the rewarding aspect of social interaction in juvenile rats. Physiol Behav 51:667–672

    Article  PubMed  CAS  Google Scholar 

  • Clause BT (1993) The Wistar Rat as a right choice: establishing mammalian standards and the ideal of a standardized mammal. J Hist Biol 26:329–349

    Article  PubMed  CAS  Google Scholar 

  • Crowder WF, Hutto CW Jr (1992) Operant place conditioning measures examined using two nondrug reinforcers. Pharmacol, Biochem Behav 41:817–824

    Article  CAS  Google Scholar 

  • Douglas LA, Varlinskaya EI, Spear LP (2004) Rewarding properties of social interactions in adolescent and adult male and female rats: impact of social versus isolate housing of subjects and partners. Dev Psychobiol 45:153–162

    Article  PubMed  Google Scholar 

  • Ebstein RP, Israel S, Chew SH, Zhong S, Knafo A (2010) Genetics of human social behavior. Neuron 65:831–844

    Article  PubMed  CAS  Google Scholar 

  • Falk JL (1958) The grooming behavior of the chimpanzee as a reinforcer. J Exp Anal Behav 1:83–85

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Ferguson SA, Cada AM (2004) Spatial learning/memory and social and nonsocial behaviors in the spontaneously hypertensive, Wistar–Kyoto and Sprague–Dawley rat strains. Pharmacol, Biochem Behav 77:583–594

    Article  CAS  Google Scholar 

  • Field EF, Pellis SM (1994) Differential effects of amphetamine on the attack and defense components of play fighting in rats. Physiol Behav 56:325–330

    Article  PubMed  CAS  Google Scholar 

  • Fowler SC, Birkestrand B, Chen R, Vorontsova E, Zarcone T (2003) Behavioral sensitization to amphetamine in rats: changes in the rhythm of head movements during focused stereotypies. Psychopharmacology (Berl) 170:167–177

    Article  CAS  Google Scholar 

  • Hamed A, Taracha E, Szyndler J, Krzascik P, Lehner M, Maciejak P, Skorzewska A, Plaznik A (2012) The effects of morphine and morphine conditioned context on 50 kHz ultrasonic vocalisation in rats. Behav Brain Res 229:447–450

    Article  PubMed  CAS  Google Scholar 

  • Hedrich HJ (2006) Taxonomy and stocks and strains. In: Suckow MA, Weisbroth SH, Franklin CH (eds) The laboratory rat. Elsevier, Burlington

    Google Scholar 

  • Humphreys AP, Einon DF (1981) Play as a reinforcer for maze learning in juvenile rats. Anim Behav 29:259–270

    Article  Google Scholar 

  • Ikemoto S, Panksepp J (1992) The effects of early social isolation on the motivation for social play in juvenile rats. Dev Psychobiol 25:261–274

    Article  PubMed  CAS  Google Scholar 

  • Jordan R (2003) Social play and autistic spectrum disorders: a perspective on theory, implications and educational approaches. Autism 7:347–360

    Article  PubMed  Google Scholar 

  • Kinney GG, Wilkinson LO, Saywell KL, Tricklebank MD (1999) Rat strain differences in the ability to disrupt sensorimotor gating are limited to the dopaminergic system, specific to prepulse inhibition, and unrelated to changes in startle amplitude or nucleus accumbens dopamine receptor sensitivity. J Neurosci 19:5644–5653

    PubMed  CAS  Google Scholar 

  • Knutson B, Burgdorf J, Panksepp J (1998) Anticipation of play elicits high-frequency ultrasonic vocalizations in young rats. J Comp Psychol 112:65–73

    Article  PubMed  CAS  Google Scholar 

  • Knutson B, Burgdorf J, Panksepp J (2002) Ultrasonic vocalizations as indices of affective states in rats. Psychol Bull 128:961–977

    Article  PubMed  Google Scholar 

  • Kuczenski R, Segal DS (1999) Sensitization of amphetamine-induced stereotyped behaviors during the acute response: role of D1 and D2 dopamine receptors. Brain Res 822:164–174

    Article  PubMed  CAS  Google Scholar 

  • Lahvis GP, Alleva E, Scattoni ML (2011) Translating mouse vocalizations: prosody and frequency modulation. Genes Brain Behav 10:4–16

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Magnus-Ellenbroek B, Havemann-Reinecke U (1993) Morphine-induced hyperactivity in rats—a rebound effect? Naunyn Schmiedebergs Arch Pharmacol 347:635–642

    Article  PubMed  CAS  Google Scholar 

  • Maier EY, Ma ST, Ahrens A, Schallert TJ, Duvauchelle CL (2010) Assessment of ultrasonic vocalizations during drug self-administration in rats. J Vis Exp pii: 2041.

  • Manning MM, Wainwright LD (2010) The role of high level play as a predictor social functioning in autism. J Autism Dev Disord 40(5):523–533

    Article  PubMed  Google Scholar 

  • Mas M, Sabater E, Olaso MJ, Horga JF, Faura CC (2000) Genetic variability in morphine sensitivity and tolerance between different strains of rats. Brain Res 866:109–115

    Article  PubMed  CAS  Google Scholar 

  • Mason WM, Saxon SV, Sharpe LG (1963) Preferential responses of young chimpanzees to food and social rewards. Psychol Rec 13:341–345

    Google Scholar 

  • McDermott C, Kelly JP (2008) Comparison of the behavioural pharmacology of the Lister-Hooded with 2 commonly utilised albino rat strains. Prog Neuropsychopharmacol Biol Psychiatry 32:1816–1823

    Article  PubMed  CAS  Google Scholar 

  • Meyer-Lindenberg A, Tost H (2012) Neural mechanisms of social risk for psychiatric disorders. Nat Neurosci 15:663–668

    Article  PubMed  CAS  Google Scholar 

  • Niesink RJ, Van Ree JM (1989) Involvement of opioid and dopaminergic systems in isolation-induced pinning and social grooming of young rats. Neuropharmacology 28:411–418

    Article  PubMed  CAS  Google Scholar 

  • Normansell L, Panksepp J (1990) Effects of morphine and naloxone on play-rewarded spatial discrimination in juvenile rats. Dev Psychobiol 23:75–83

    Article  PubMed  CAS  Google Scholar 

  • O'Connell LA, Hofmann HA (2010) Genes, hormones, and circuits: an integrative approach to study the evolution of social behavior. Front Neuroendocrinol 32:320–335

    Article  PubMed  CAS  Google Scholar 

  • Panksepp J, Beatty WW (1980) Social deprivation and play in rats. Behav Neural Biol 30:197–206

    Article  PubMed  CAS  Google Scholar 

  • Panksepp J, Jalowiec J, DeEskinazi FG, Bishop P (1985) Opiates and play dominance in juvenile rats. Behav Neurosci 99:441–453

    Article  PubMed  CAS  Google Scholar 

  • Panksepp J, Siviy S, Normansell L (1984) The psychobiology of play: theoretical and methodological perspectives. Neurosci Biobehav Rev 8:465–492

    Article  PubMed  CAS  Google Scholar 

  • Pellis SM, McKenna M (1992) Intrinsic and extrinsic influences on play fighting in rats: effects of dominance, partner's playfulness, temperament and neonatal exposure to testosterone propionate. Behav Brain Res 50:135–145

    Article  PubMed  CAS  Google Scholar 

  • Pellis SM, Pellis V (1987) Play-fighting differs from serious fighting in both target of attack and tactics of fighting in the laboratory rat Rattus norvegicus. Aggress Behav 13:227–242

    Article  Google Scholar 

  • Pellis SM, Pellis V (2009) The playful brain: venturing to the limits of neuroscience. Oneworld Publications, Oxford, UK

    Google Scholar 

  • Pellis SM, Pellis VC, Dewsbury DA (1989) Different levels of complexity in the play fighting of muroid rodents appear to result from different levels of intensity of attack and defense. Aggress Behav 15:297–310

    Article  Google Scholar 

  • Poole TB, Fish J (1975) An investigation of playful behavior in Rattus norvegicus and Mus musculus (Mammalia). J Zool 175:61–71

    Article  Google Scholar 

  • Reinhart CJ, McIntyre DC, Metz GA, Pellis SM (2006) Play fighting between kindling-prone (FAST) and kindling-resistant (SLOW) rats. J Comp Psychol 120:19–30

    Article  PubMed  Google Scholar 

  • Rex A, Voigt JP, Gustedt C, Beckett S, Fink H (2004) Anxiolytic-like profile in Wistar, but not Sprague–Dawley rats in the social interaction test. Psychopharmacology (Berl) 177:23–34

    Article  CAS  Google Scholar 

  • Sadananda M, Natusch C, Karrenbauer B, Schwarting RK (2012) 50-kHz calls in rats: effects of MDMA and the 5-HT(1A) receptor agonist 8-OH-DPAT. Pharmacol, Biochem Behav 101:258–264

    Article  CAS  Google Scholar 

  • Scattoni ML, Crawley J, Ricceri L (2009) Ultrasonic vocalizations: a tool for behavioural phenotyping of mouse models of neurodevelopmental disorders. Neurosci Biobehav Rev 33:508–515

    Article  PubMed Central  PubMed  Google Scholar 

  • Shoaib M, Spanagel R, Stohr T, Shippenberg TS (1995) Strain differences in the rewarding and dopamine-releasing effects of morphine in rats. Psychopharmacology (Berl) 117:240–247

    Article  CAS  Google Scholar 

  • Simola N, Fenu S, Costa G, Pinna A, Plumitallo A, Morelli M (2012) Pharmacological characterization of 50-kHz ultrasonic vocalizations in rats: comparison of the effects of different psychoactive drugs and relevance in drug-induced reward. Neuropharmacology 63:224–234

    Article  PubMed  CAS  Google Scholar 

  • Siviy SM, Crawford CA, Akopian G, Walsh JP (2011) Dysfunctional play and dopamine physiology in the Fischer 344 rat. Behav Brain Res 220:294–304

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Siviy SM, Love NJ, DeCicco BM, Giordano SB, Seifert TL (2003) The relative playfulness of juvenile Lewis and Fischer-344 rats. Physiol Behav 80:385–394

    Article  PubMed  CAS  Google Scholar 

  • Siviy SM, Panksepp J (1987) Juvenile play in the rat: thalamic and brain stem involvement. Physiol Behav 41:103–114

    Article  PubMed  CAS  Google Scholar 

  • Siviy SM, Panksepp J (2011) In search of the neurobiological substrates for social playfulness in mammalian brains. Neurosci Biobehav Rev 35:1821–1830

    Article  PubMed  Google Scholar 

  • Spinka M, Newberry RC, Bekoff M (2001) Mammalian play: training for the unexpected. Q Rev Biol 76:141–168

    Article  PubMed  CAS  Google Scholar 

  • Staples LG, McGregor IS (2006) Defensive responses of Wistar and Sprague–Dawley rats to cat odour and TMT. Behav Brain Res 172:351–354

    Article  PubMed  CAS  Google Scholar 

  • Sutton ME, Raskin LA (1986) A behavioral analysis of the effects of amphetamine on play and locomotor activity in the post-weaning rat. Pharmacol, Biochem Behav 24:455–461

    Article  CAS  Google Scholar 

  • Takahashi N, Kashino M, Hironaka N (2010) Structure of rat ultrasonic vocalizations and its relevance to behavior. PLoS One 5:e14115

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Thiel KJ, Okun AC, Neisewander JL (2008) Social reward-conditioned place preference: a model revealing an interaction between cocaine and social context rewards in rats. Drug Alcohol Depend 96:202–212

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Thiel KJ, Sanabria F, Neisewander JL (2009) Synergistic interaction between nicotine and social rewards in adolescent male rats. Psychopharmacology (Berl) 204:391–402

    Article  CAS  Google Scholar 

  • Thompson B, Leonard KC, Brudzynski SM (2006) Amphetamine-induced 50 kHz calls from rat nucleus accumbens: a quantitative mapping study and acoustic analysis. Behav Brain Res 168:64–73

    Article  PubMed  CAS  Google Scholar 

  • Thor DH, Holloway WR Jr (1983) Play soliciting in juvenile male rats: effects of caffeine, amphetamine and methylphenidate. Pharmacol, Biochem Behav 19:725–727

    Article  CAS  Google Scholar 

  • Trezza V, Baarendse PJJ, Vanderschuren LJMJ (2009) Prosocial effects of nicotine and ethanol in adolescent rats through partially dissociable neurobehavioral mechanisms. Neuropsychopharmacology 34:2560–2573

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Trezza V, Baarendse PJJ, Vanderschuren LJMJ (2010) The pleasures of play: pharmacological insights into social reward mechanisms. Trends Pharmacol Sci 31:463–469

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Trezza V, Campolongo P, Cassano T, Macheda T, Dipasquale P, Carratu MR, Gaetani S, Cuomo V (2008) Effects of perinatal exposure to delta-9-tetrahydrocannabinol on the emotional reactivity of the offspring: a longitudinal behavioral study in Wistar rats. Psychopharmacology (Berl) 198:529–537

    Article  CAS  Google Scholar 

  • Trezza V, Campolongo P, Vanderschuren LJMJ (2011a) Evaluating the rewarding nature of social interactions in laboratory animals. Dev Cogn Neurosci 1:444–458

    Article  PubMed  Google Scholar 

  • Trezza V, Damsteegt R, Achterberg EJM, Vanderschuren LJMJ (2011b) Nucleus accumbens mu-opioid receptors mediate social reward. J Neurosci 31:6362–6370

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Trezza V, Vanderschuren LJMJ (2008a) Bidirectional cannabinoid modulation of social behavior in adolescent rats. Psychopharmacology (Berl) 197:217–227

    Article  CAS  Google Scholar 

  • Trezza V, Vanderschuren LJMJ (2008b) Cannabinoid and opioid modulation of social play behavior in adolescent rats: differential behavioral mechanisms. Eur Neuropsychopharmacol 18:519–530

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Van den Berg CL, Pijlman FT, Koning HA, Diergaarde L, Van Ree JM, Spruijt BM (1999) Isolation changes the incentive value of sucrose and social behaviour in juvenile and adult rats. Behav Brain Res 106:133–142

    Article  PubMed  Google Scholar 

  • Vanderschuren LJMJ, Niesink RJM, Spruijt BM, Van Ree JM (1995a) Effects of morphine on different aspects of social play in juvenile rats. Psychopharmacology (Berl) 117:225–231

    Article  CAS  Google Scholar 

  • Vanderschuren LJMJ, Niesink RJM, Spruijt BM, Van Ree JM (1995b) Influence of environmental factors on social play behavior of juvenile rats. Physiol Behav 58:119–123

    Article  PubMed  CAS  Google Scholar 

  • Vanderschuren LJMJ, Spruijt BM, Hol T, Niesink RJM, Van Ree JM (1995c) Sequential analysis of social play behavior in juvenile rats: effects of morphine. Behav Brain Res 72:89–95

    Article  PubMed  CAS  Google Scholar 

  • Vanderschuren LJMJ (2010) How the brain makes play fun. Am J Play 2:315–337

    Google Scholar 

  • Vanderschuren LJMJ, Niesink RJ, Van Ree JM (1997) The neurobiology of social play behavior in rats. Neurosci Biobehav Rev 21:309–326

    Article  PubMed  CAS  Google Scholar 

  • Vanderschuren LJMJ, Trezza V, Griffioen-Roose S, Schiepers OJG, Van Leeuwen N, De Vries TJ, Schoffelmeer ANM (2008) Methylphenidate disrupts social play behavior in adolescent rats. Neuropsychopharmacology 33:2946–2956

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Varlinskaya EI, Spear LP (2002) Acute effects of ethanol on social behavior of adolescent and adult rats: role of familiarity of the test situation. Alcohol Clin Exp Res 26:1502–1511

    Article  PubMed  Google Scholar 

  • Varlinskaya EI, Spear LP (2008) Social interactions in adolescent and adult Sprague–Dawley rats: impact of social deprivation and test context familiarity. Behav Brain Res 188:398–405

    Article  PubMed Central  PubMed  Google Scholar 

  • Vezina P, Queen AL (2000) Induction of locomotor sensitization by amphetamine requires the activation of NMDA receptors in the rat ventral tegmental area. Psychopharmacology (Berl) 151:184–191

    Article  CAS  Google Scholar 

  • Von Frijtag JC, Schot M, van den Bos R, Spruijt BM (2002) Individual housing during the play period results in changed responses to and consequences of a psychosocial stress situation in rats. Dev Psychobiol 41(1):58–69

    Article  Google Scholar 

  • Walker FR, Naicker S, Hinwood M, Dunn N, Day TA (2009) Strain differences in coping behaviour, novelty seeking behaviour, and susceptibility to socially conditioned fear: a comparison between Wistar and Sprague Dawley rats. Stress 12:507–516

    Article  PubMed  Google Scholar 

  • Willey AR, Spear LP (2012) Development of anticipatory 50 kHz USV production to a social stimuli in adolescent and adult male Sprague-Dawley rats. Behav Brain Res 226:613–618

    Article  PubMed Central  PubMed  Google Scholar 

  • Willey AR, Spear LP (2013) The effects of pre-test social deprivation on a natural reward incentive test and concomitant 50kHz ultrasonic vocalization production in adolescent and adult male Sprague–Dawley rats. Behav Brain Res 245:107–112

    Article  PubMed  Google Scholar 

  • Willey AR, Varlinskaya EI, Spear LP (2009) Social interactions and 50-kHz ultrasonic vocalizations in adolescent and adult rats. Behav Brain Res 202:122–129

    Article  PubMed Central  PubMed  Google Scholar 

  • Wintink AJ, Brudzynski SM (2001) The related roles of dopamine and glutamate in the initiation of 50-kHz ultrasonic calls in adult rats. Pharmacol, Biochem Behav 70:317–323

    Article  CAS  Google Scholar 

  • Wohr M, Schwarting RK (2013) Affective communication in rodents: ultrasonic vocalizations as a tool for research on emotion and motivation. Cell Tissue Res

  • Wright JM, Deng L, Clarke PB (2012) Failure of rewarding and locomotor stimulant doses of morphine to promote adult rat 50-kHz ultrasonic vocalizations. Psychopharmacology (Berl) 224:477–487

    Article  CAS  Google Scholar 

  • Yilmazer-Hanke DM (2008) Morphological correlates of emotional and cognitive behaviour: insights from studies on inbred and outbred rodent strains and their crosses. Behav Pharmacol 19:403–434

    Article  PubMed  Google Scholar 

  • Zmarowski A, Beekhuijzen M, Lensen J, Emmen H (2012) Differential performance of Wistar Han and Sprague Dawley rats in behavioral tests: differences in baseline behavior and reactivity to positive control agents. Reprod Toxicol 34:192–203

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

This study was supported by Veni grant 91611052 (Nederlandse Organisatie voor Wetenschappelijk Onderzoek, V.T.), Marie Curie Career Reintegration Grant PCIG09-GA-2011-293589 (Seventh Framework Programme People, V.T.), and Futuro in Ricerca 2010 (Italian Ministry for University and Scientific Research, V.T., P.C.). We thank Andrea Peloso, Lidia Montebello, and Alessandro Pasquale (Master students, Department of Physiology and Pharmacology, Sapienza, University of Rome) for their technical help.

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Manduca, A., Campolongo, P., Palmery, M. et al. Social play behavior, ultrasonic vocalizations and their modulation by morphine and amphetamine in Wistar and Sprague-Dawley rats. Psychopharmacology 231, 1661–1673 (2014). https://doi.org/10.1007/s00213-013-3337-9

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