Methamphetamine (MA), as a psychostimulant drug that crosses the placental barrier, may disrupt the development of social play. The present study aims to examine the effect of prenatal MA (5 mg/kg) exposure during the first (gestational day (GD) 1-11) or second (GD 12-22) halves of prenatal development of rats on social play behavior. To investigate an acute effect of MA on social play in adulthood, juvenile rats were exposed to a dose of 1 mg/kg MA or saline on the test day and tested for social play for 15 min. Prenatal exposure to MA during GD 1-11 increased social play behavior during 5-10 min interval of the test in males but not females. Prenatal MA during GD 12-22 did not influence social play in males nor females. However, social play occurred to a greater extent in GD 12-22 groups compared with GD 1-11. Acute exposure to MA eliminated playful behavior in all groups and decreased social exploration in GD 1-11. Our results suggest that manipulation of prenatal development during the first half of the gestational period has a greater impact on social play behavior than during the second half.

Department of Physiology 3rd Faculty of Medicine Charles University Prague Czech Republic

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ACUFF-SMITH KD, GEORGE M, LORENS SA, VORHEES CV. Preliminary evidence for methamphetamine-induced behavioral and ocular effects in rat offspring following exposure during early organogenesis. Psychopharmacology (Berl) 1992;109:255–263. doi: 10.1007/BF02245871. PubMed DOI

ACUFF-SMITH KD, SCHILLING MA, FISHER JE, VORHEES CV. Stage-specific effects of prenatal d-methamphetamine exposure on behavioral and eye development in rats. Neurotoxicol Teratol. 1996;18:199–215. doi: 10.1016/0892-0362(95)02015-2. PubMed DOI

ACHTERBERG EJ, TREZZA V, SIVIY SM, SCHRAMA L, SCHOFFELMEER AN, VANDERSCHUREN LJ. Amphetamine and cocaine suppress social play behavior in rats through distinct mechanisms. Psychopharmacology (Berl) 2014;231:1503–1515. doi: 10.1007/s00213-013-3272-9. PubMed DOI PMC

ACHTERBERG EJ, Van KERKHOF LW, DAMSTEEGT R, TREZZA V, VANDERSCHUREN LJ. Methylphenidate and atomoxetine inhibit social play behavior through prefrontal and subcortical limbic mechanisms in rats. J Neurosci. 2015;35:161–169. doi: 10.1523/JNEUROSCI.2945-14.2015. PubMed DOI PMC

BAYER SA, ALTMAN J, RUSSO RJ, ZHANG X. Timetables of neurogenesis in the human brain based on experimentally determined patterns in the rat. Neurotoxicology. 1993;14:83–144. PubMed

CALCAGNETTI DJ, SCHECHTER MD. Place conditioning reveals the rewarding aspect of social interaction in juvenile rats. Physiol Behav. 1992;51:667–672. doi: 10.1016/0031-9384(92)90101-7. PubMed DOI

DAVIDSON C, GOW AJ, LEE TH, ELLINWOOD EH. Methamphetamine neurotoxicity: necrotic and apoptotic mechanisms and relevance to human abuse and treatment. Brain Res Brain Res Rev. 2001;36:1–22. doi: 10.1016/S0165-0173(01)00054-6. PubMed DOI

DELLA GROTTA S, LAGASSE LL, ARRIA AM, DERAUF C, GRANT P, SMITH LM, SHAH R, HUESTIS M, LIU J, LESTER BM. Patterns of methamphetamine use during pregnancy: results from the Infant Development, Environment, and Lifestyle (IDEAL) Study. Matern Child Health J. 2010;14:519–527. doi: 10.1007/s10995-009-0491-0. PubMed DOI PMC

DOUGLAS LA, VARLINSKAYA EI, SPEAR LP. 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. 2004;45:153–162. doi: 10.1002/dev.20025. PubMed DOI

FILE SE, SETH P. A review of 25 years of the social interaction test. Eur J Pharmacol. 2003;463:35–53. doi: 10.1016/S0014-2999(03)01273-1. PubMed DOI

HERLENIUS E, LAGERCRANTZ H. Development of neurotransmitter systems during critical periods. Exp Neurol. 2004;190(Suppl 1):S8–21. doi: 10.1016/j.expneurol.2004.03.027. PubMed DOI

HOLUBOVÁ A, ŠEVČÍKOVÁ M, MACÚCHOVÁ E, HREBÍČKOVÁ I, POMETLOVÁ M, ŠLAMBEROVÁ R. Effects of perinatal stress and drug abuse on maternal behavior and sensorimotor development of affected progeny. Physiol Res. 2017;66:S481–S491. doi: 10.33549/physiolres.933800. PubMed DOI

HOMBERG JR, SCHIEPERS OJ, SCHOFFELMEER AN, CUPPEN E, VANDERSCHUREN LJ. Acute and constitutive increases in central serotonin levels reduce social play behaviour in peri-adolescent rats. Psychopharmacology (Berl) 2007;195:175–182. doi: 10.1007/s00213-007-0895-8. PubMed DOI PMC

HREBÍČKOVÁ I, MALINOVÁ-ŠEVČÍKOVÁ M, MACÚCHOVA E, NOHEJLOVÁ K, ŠLAMBEROVÁ R. Exposure to methamphetamine during first and second half of prenatal period and its consequences on cognition after long-term application in adulthood. Physiol Res. 2014;63(Suppl 4):S535–545. PubMed

HREBÍČKOVÁ I, ŠEVČÍKOVÁ M, MACÚCHOVÁ E, ŠLAMBEROVÁ R. How methamphetamine exposure during different neurodevelopmental stages affects social behavior of adult rats? Physiol Behav. 2017;179:391–400. doi: 10.1016/j.physbeh.2017.07.009. PubMed DOI

HREBÍČKOVÁ I, ŠEVČÍKOVÁ M, NOHEJLOVÁ K, ŠLAMBEROVÁ R. Does effect from developmental methamphetamine exposure on spatial learning and memory depend on stage of neuroontogeny? Physiol Res. 2016;65(Suppl 5):S577–S589. doi: 10.33549/physiolres.933534. PubMed DOI

JORDAN R. Social play and autistic spectrum disorders: a perspective on theory, implications and educational approaches. Autism. 2003;7:347–360. doi: 10.1177/1362361303007004002. PubMed DOI

KOLB B, MYCHASIUK R, MUHAMMAD A, LI Y, FROST DO, GIBB R. Experience and the developing prefrontal cortex. Proc Natl Acad Sci U S A 109 Suppl. 2012;2:17186–17193. doi: 10.1073/pnas.1121251109. PubMed DOI PMC

MACÚCHOVÁ E, NOHEJLOVÁ K, ŠEVČÍKOVÁ M, HREBÍČKOVÁ I, ŠLAMBEROVÁ R. Sex differences in the strategies of spatial learning in prenatally-exposed rats treated with various drugs in adulthood. Behav Brain Res. 2017;327:83–93. doi: 10.1016/j.bbr.2017.03.041. PubMed DOI

MACÚCHOVÁ E, ŠEVČÍKOVÁ M, HREBÍČKOVÁ I, NOHEJLOVÁ K, ŠLAMBEROVÁ R. How various drugs affect anxiety-related behavior in male and female rats prenatally exposed to methamphetamine. Int J Dev Neurosci. 2016;51:1–11. doi: 10.1016/j.ijdevneu.2016.04.001. PubMed DOI

MACÚCHOVÁ E, ŠLAMBEROVÁ R. Does prenatal methamphetamine exposure induce sensitization to drugs in adulthood? Physiol Res. 2017;66:S457–S467. doi: 10.33549/physiolres.933803. PubMed DOI

MAGALHAES A, SUMMAVIELLE T, MELO P, ROSA R, TAVARES MA, De SOUSA L. Prenatal exposure to cocaine and enriched environment: effects on social interactions. Ann N Y Acad Sci. 2006;1074:620–631. doi: 10.1196/annals.1369.060. PubMed DOI

MALINOVÁ-ŠEVČÍKOVÁ M, HREBÍČKOVÁ I, MACÚCHOVÁ E, NOVÁ E, POMETLOVÁ M, ŠLAMBEROVÁ R. Differences in maternal behavior and development of their pups depend on the time of methamphetamine exposure during gestation period. Physiol Res. 2014;63(Suppl 4):S559–572. PubMed

MARWICK C. NIDA seeking data on effect of fetal exposure to methamphetamine. JAMA. 2000;283:2225–2226. doi: 10.1001/jama.283.17.2225-JMN0503-2-1. PubMed DOI

NEUGEBAUER NM, CUNNINGHAM ST, ZHU J, BRYANT RI, MIDDLETON LS, DWOSKIN LP. Effects of environmental enrichment on behavior and dopamine transporter function in medial prefrontal cortex in adult rats prenatally treated with cocaine. Brain Res Dev Brain Res. 2004;153:213–223. doi: 10.1016/j.devbrainres.2004.09.001. PubMed DOI

NIJHOF SL, VINKERS CH, van GEELEN SM, DUIJFF SN, ACHTERBERG EJM, van der NET J, VELTKAMP RC, GROOTENHUIS MA, van de PUTTE EM, HILLEGERS MHJ, van der BRUG AW, WIERENGA CJ, BENDERS M, ENGELS R, van der ENT CK, VANDERSCHUREN L, LESSCHER HMB. Healthy play, better coping: The importance of play for the development of children in health and disease. Neurosci Biobehav Rev. 2018;95:421–429. doi: 10.1016/j.neubiorev.2018.09.024. PubMed DOI

PANKSEPP J, SIVIY S, NORMANSELL L. The psychobiology of play: theoretical and methodological perspectives. Neurosci Biobehav Rev. 1984;8:465–492. doi: 10.1016/0149-7634(84)90005-8. PubMed DOI

PELLIS SM, PELLIS VC. Play fighting of rats in comparative perspective: a schema for neurobehavioral analyses. Neurosci Biobehav Rev. 1998;23:87–101. doi: 10.1016/S0149-7634(97)00071-7. PubMed DOI

RAMBOUSEK L, KAČER P, SYSLOVÁ K, BUMBA J, BUBENÍKOVÁ-VALEŠOVÁ V, ŠLAMBEROVÁ R. Sex differences in methamphetamine pharmacokinetics in adult rats and its transferal to pups via placental membrane and breast milk. Drug and Alcohol Dependence. 2014;139:138–144. doi: 10.1016/j.drugalcdep.2014.03.023. PubMed DOI

RICE D, BARONE S., jr Critical periods of vulnerability for the developing nervous system: evidence from humans and animal models. Environ Health Perspect 108 Suppl. 2000;3:511–533. doi: 10.1289/ehp.00108s3511. PubMed DOI PMC

ROTHMAN RB, BAUMANN MH. Monoamine transporters and psychostimulant drugs. Eur J Pharmacol. 2003;479:23–40. doi: 10.1016/j.ejphar.2003.08.054. PubMed DOI

ROTHMAN RB, BAUMANN MH, DERSCH CM, ROMERO DV, RICE KC, CARROLL FI, PARTILLA JS. Amphetamine-type central nervous system stimulants release norepinephrine more potently than they release dopamine and serotonin. Synapse. 2001;39:32–41. doi: 10.1002/1098-2396(20010101)39:1<32::AID-SYN5>3.0.CO,2-3. PubMed DOI

RUBIN KH, WATSON KS, JAMBOR TW. Free-play behaviors in preschool and kindergarten children. Child Development. 1978;49:534–536. doi: 10.2307/1128725. DOI

RYAN AM, BERMAN RF, BAUMAN MD. Bridging the species gap in translational research for neurodevelopmental disorders. Neurobiol Learn Mem. 2018 doi: 10.1016/j.nlm.2018.10.006. PubMed DOI PMC

SCHMIDT RR, JOHNSON EM. Principles of teratology. In: HOOD RD, editor. Handbook of Developmental Toxicology. CRC Press; Boca Raton, FL: 1997. pp. 3–12..

SCHUTOVÁ B, HRUBÁ L, POMETLOVÁ M, ROKYTA R, ŠLAMBEROVÁ R. Responsiveness to methamphetamine in adulthood is altered by prenatal exposure in rats. Physiol Behav. 2010;99:381–387. doi: 10.1016/j.physbeh.2009.12.004. PubMed DOI

SIVIY SM, PANKSEPP J. In search of the neurobiological substrates for social playfulness in mammalian brains. Neurosci Biobehav Rev. 2011;35:1821–1830. doi: 10.1016/j.neubiorev.2011.03.006. PubMed DOI

SOBRIAN SK, HOLSON RR. Social behavior of offspring following prenatal cocaine exposure in rodents: a comparison with prenatal alcohol. Front Psychiatry. 2011;2:66. doi: 10.3389/fpsyt.2011.00066. PubMed DOI PMC

SULZER D, CHEN TK, LAU YY, KRISTENSEN H, RAYPORT S, EWING A. Amphetamine redistributes dopamine from synaptic vesicles to the cytosol and promotes reverse transport. J Neurosci. 1995;15:4102–4108. doi: 10.1523/JNEUROSCI.15-05-04102.1995. PubMed DOI PMC

SUNDSTROM E, KOLARE S, SOUVERBIE F, SAMUELSSON EB, PSCHERA H, LUNELL NO, SEIGER A. Neurochemical differentiation of human bulbospinal monoaminergic neurons during the first trimester. Brain Res Dev Brain Res. 1993;75:1–12. doi: 10.1016/0165-3806(93)90059-J. PubMed DOI

SYME LA, SYME GJ. Group instability and the social response to methamphetamine. Pharmacol Biochem Behav. 1974;2:851–854. doi: 10.1016/0091-3057(74)90122-1. PubMed DOI

ŠEVČÍKOVÁ M, HREBÍČKOVÁ I, MACÚCHOVÁ E, ŠLAMBEROVÁ R. The influence of methamphetamine on maternal behavior and development of the pups during the neonatal period. Int J Dev Neurosci. 2017;59:37–46. doi: 10.1016/j.ijdevneu.2017.03.005. PubMed DOI

ŠLAMBEROVÁ R, MIKULECKÁ A, MACÚCHOVÁ E, HREBÍČKOVÁ I, ŠEVČÍKOVÁ M, NOHEJLOVÁ K, POMETLOVÁ M. Effects of psychostimulants on social interaction in adult male rats. Behav Pharmacol. 2015a;26:776–785. doi: 10.1097/FBP.0000000000000148. PubMed DOI

ŠLAMBEROVÁ R, MIKULECKÁ A, POMETLOVÁ M, SCHUTOVÁ B, HRUBÁ L, DEYKUN K. The effect of methamphetamine on social interaction of adult male rats. Behav Brain Res. 2010;214:423–427. doi: 10.1016/j.bbr.2010.06.019. PubMed DOI

ŠLAMBEROVÁ R, POMETLOVÁ M, CHAROUSOVÁ P. Postnatal development of rat pups is altered by prenatal methamphetamine exposure. Prog Neuropsychopharmacol Biol Psychiatry. 2006;30:82–88. doi: 10.1016/j.pnpbp.2005.06.006. PubMed DOI

ŠLAMBEROVÁ R, POMETLOVÁ M, MACÚCHOVÁ E, NOHEJLOVÁ K, STUCHLÍK A, VALEŠ K. Do the effects of prenatal exposure and acute treatment of methamphetamine on anxiety vary depending on the animal model used? Behav Brain Res. 2015b;292:361–369. doi: 10.1016/j.bbr.2015.07.001. PubMed DOI

ŠLAMBEROVÁ R, POMETLOVÁ M, ROKYTA R. Effect of methamphetamine exposure during prenatal and preweaning periods lasts for generations in rats. Dev Psychobiol. 2007;49:312–322. doi: 10.1002/dev.20203. PubMed DOI

ŠLAMBEROVÁ R, VRAJOVÁ M, SCHUTOVÁ B, MERTLOVÁ M, MACÚCHOVÁ E, NOHEJLOVÁ K, HRUBÁ L, PUSKARČÍKOVÁ J, BUBENÍKOVÁ-VALEŠOVÁ V, YAMAMOTOVÁ A. Prenatal methamphetamine exposure induces long-lasting alterations in memory and development of NMDA receptors in the hippocampus. Physiol Res. 2014;63(Suppl 4):S547–558. PubMed

ŠPINKA M, NEWBERRY RC, BEKOFF M. Mammalian play: training for the unexpected. Q Rev Biol. 2001;76:141–168. doi: 10.1086/393866. PubMed DOI

TREZZA V, BAARENDSE PJ, VANDERSCHUREN LJ. Prosocial effects of nicotine and ethanol in adolescent rats through partially dissociable neurobehavioral mechanisms. Neuropsychopharmacology. 2009a;34:2560–2573. doi: 10.1038/npp.2009.85. PubMed DOI PMC

TREZZA V, BAARENDSE PJ, VANDERSCHUREN LJ. The pleasures of play: pharmacological insights into social reward mechanisms. Trends Pharmacol Sci. 2010;31:463–469. doi: 10.1016/j.tips.2010.06.008. PubMed DOI PMC

TREZZA V, DAMSTEEGT R, VANDERSCHUREN LJ. Conditioned place preference induced by social play behavior: parametrics, extinction, reinstatement and disruption by methylphenidate. Eur Neuropsychopharmacol. 2009b;19:659–669. doi: 10.1016/j.euroneuro.2009.03.006. PubMed DOI PMC

van den BERG CL, HOL T, Van REE JM, SPRUIJT BM, EVERTS H, KOOLHAAS JM. Play is indispensable for an adequate development of coping with social challenges in the rat. Dev Psychobiol. 1999;34:129–138. doi: 10.1002/(SICI)1098-2302(199903)34:2<129::AID-DEV6>3.0.CO,2-L. PubMed DOI

VANDERSCHUREN LJ, ACHTERBERG EJ, TREZZA V. The neurobiology of social play and its rewarding value in rats. Neurosci Biobehav Rev. 2016;70:86–105. doi: 10.1016/j.neubiorev.2016.07.025. PubMed DOI PMC

VANDERSCHUREN LJ, NIESINK RJ, Van REE JM. The neurobiology of social play behavior in rats. Neurosci Biobehav Rev. 1997;21:309–326. doi: 10.1016/S0149-7634(96)00020-6. PubMed DOI

VANDERSCHUREN LJ, STEIN EA, WIEGANT VM, Van REE JM. Social isolation and social interaction alter regional brain opioid receptor binding in rats. Eur Neuropsychopharmacol. 1995a;5:119–127. doi: 10.1016/0924-977X(95)00010-M. PubMed DOI

VANDERSCHUREN LJ, STEIN EA, WIEGANT VM, Van REE JM. Social play alters regional brain opioid receptor binding in juvenile rats. Brain Res. 1995b;680:148–156. doi: 10.1016/0006-8993(95)00256-P. PubMed DOI

VANDERSCHUREN LJ, TREZZA V. What the laboratory rat has taught us about social play behavior: role in behavioral development and neural mechanisms. Curr Top Behav Neurosci. 2014;16:189–212. doi: 10.1007/978-3-662-45758-0_268. PubMed DOI

VANDERSCHUREN LJ, TREZZA V, GRIFFIOEN-ROOSE S, SCHIEPERS OJ, Van LEEUWEN N, De VRIES TJ, SCHOFFELMEER AN. Methylphenidate disrupts social play behavior in adolescent rats. Neuropsychopharmacology. 2008;33:2946–2956. doi: 10.1038/npp.2008.10. PubMed DOI PMC

WOOD RD, BANNOURA MD, JOHANSON IB. Prenatal cocaine exposure: effects on play behavior in the juvenile rat. Neurotoxicol Teratol. 1994;16:139–144. doi: 10.1016/0892-0362(94)90110-4. PubMed DOI

WOOD RD, MOLINA VA, WAGNER JM, SPEAR LP. Play behavior and stress responsivity in periadolescent offspring exposed prenatally to cocaine. Pharmacol Biochem Behav. 1995;52:367–374. doi: 10.1016/0091-3057(95)00120-L. PubMed DOI

YAMAMOTOVÁ A, HRUBÁ L, SCHUTOVÁ B, ROKYTA R, ŠLAMBEROVÁ R. Perinatal effect of methamphetamine on nociception in adult Wistar rats. Int J Dev Neurosci. 2011;29:85–92. doi: 10.1016/j.ijdevneu.2010.08.004. PubMed DOI

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