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Cited by 142Sexual Differentiation and DisordersNeuroendocrine regulation and behaviorHypothalamic control of reproductive hormones

Brain Sex Differences and the Organisation of Juvenile Social Play Behaviour

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Auger, A. P., Olesen, K. M.·2009·Journal of Neuroendocrinology
DOI 10.1111/j.1365-2826.2009.01871.xPMC PMC2739448
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Abstract

Juvenile social play behaviour is one of the earliest forms of non‐mother directed social behaviour in rodents. Juvenile social play behaviour is sexually dimorphic, with males exhibiting higher levels compared to females, making it a useful model to study both social development and sexual differentiation of the brain. As with most sexually dimorphic behaviour, juvenile play behaviour is organised by neonatal steroid hormone exposure. The developmental organisation of juvenile play behaviour also appears to be influenced by the early maternal environment. This review will focus briefly on why and how rats play, some brain regions controlling play behaviour, and how neurotransmitters and the social environment converge within the developing brain to influence sexual differentiation of juvenile play behaviour.

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Crossref · 10.1111/j.1365-2826.2009.01871.x

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  • Manipulation of PRs may affect a variety of signaling molecules, such as arginine vasopressin, opioids, endocannabinoids, dopamine, norepinephrine, serotonin, and GABA, which are all involved in social play behavior.

    “Manipulation of PRs may affect a variety of signaling molecules, such as arginine vasopressin, opioids, endocannabinoids, dopamine, norepinephrine, serotonin, and GABA, which are all involved in social play behavior [31–33].”

    From Sex-specific effects of neonatal progestin receptor antagonism on juvenile social play behavior in rats (2021) · cites this paper as [31]

    The 'Neurotransmitters and play development' section links dopamine and the opioid system to juvenile social play, and 'Social play and activity level' reports an effect of cannabinoid receptor agonists. But the 'Possible convergence of neurotransmitters and steroid receptors' section describes dopamine activating progestin receptors, not PR manipulation affecting the listed molecules. Our copy does not establish a role in social play for every molecule named in the claim. (LLM, conf=0.87)

    Experimental — accuracy not yet measured

  • Androgen exposure during the early neonatal time period is responsible for later juvenile rough-and-tumble play behavior, and juvenile hormone levels are not involved in its regulation.

    “Therefore, it is believed that androgen exposure during the early neonatal time period is responsible for later juvenile rough-and-tumble play behavior, and that juvenile hormone levels are not involved in its regulation (18, 25).”

    From Puberty Blocker, Leuprolide, Reduces Sex Differences in Rough-and-Tumble Play and Anxiety-like Behavior in Juvenile Rats (2024) · cites this paper as [18]

    The 'Hormones and play development' section (page unavailable) says that perinatal testosterone exposure helps organize later juvenile social play, including through androgen receptors. It does not establish that hormone levels during the juvenile period are uninvolved in regulating play. (LLM, conf=0.86)

    Experimental — accuracy not yet measured

  • Control male rats engaged in higher levels of rough-and-tumble play behavior compared to female rats.

    “Consistent with previous studies, we found that control male rats engaged in higher levels of rough-and-tumble play behavior compared to female rats (18).”

    From Puberty Blocker, Leuprolide, Reduces Sex Differences in Rough-and-Tumble Play and Anxiety-like Behavior in Juvenile Rats (2024) · cites this paper as [18]

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Research works printed but not linked: 72

  1. [1]Vanderschuren LJ Niesink RJ Van Ree JM The neurobiology of social play behavior in rats Neurosci Biobehav Rev 1997 21 309 326 9168267
  2. [3]Normansell L Panksepp J Effects of morphine and naloxone on play-rewarded spatial discrimination in juvenile rats Dev Psychobiol 1990 23 75 83 2160387
  3. [4]Calcagnetti DJ Schechter MD Place conditioning reveals the rewarding aspect of social interaction in juvenile rats Physiol Behav 1992 51 667 672 1594664
  4. [5]Knutson B Burgdorf J Panksepp J Anticipation of play elicits high-frequency ultrasonic vocalizations in young rats J Comp Psychol 1998 112 65 73 9528115
  5. [6]Knutson B Burgdorf J Panksepp J Ultrasonic vocalizations as indices of affective states in rats Psychol Bull 2002 128 961 977 12405139
  6. [7]Panksepp J Psychology. Beyond a joke: from animal laughter to human joy? Science 2005 308 62 63 15802592
  7. [8]Panksepp J Neuroevolutionary sources of laughter and social joy: modeling primal human laughter in laboratory rats Behav Brain Res 2007 182 231 244 17363075
  8. [12]Spear L Brake S Periadolescence: age-dependent behavior and psychopharacological responsivity in rats Dev Psychobiol 1983 16 83 109 6339302
  9. [14]Hol T Van den Berg CL Van Ree JM Spruijt BM Isolation during the play period in infancy decreases adult social interactions in rats Behav Brain Res 1999 100 91 97 10212056
  10. [15]Van den Berg CL Van Ree JM Spruijt BM Kitchen I Effects of juvenile isolation and morphine treatment on social interactions and opioid receptors in adult rats: behavioural and autoradiographic studies Eur J Neurosci 1999 11 3023 3032 10510167
  11. [16]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 10086231
  12. [17]Gerall H Ward IL Gerall AA Disruption of the male rat's sexual behaviour induced by social isolation Anim Behav 1967 15 54 58 6031110
  13. [18]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 23 215 231 2379760
  14. [20]Panksepp J The ontogeny of play in rats Dev Psychobiol 1981 14 327 332 7250521
  15. [21]Meaney MJ Stewart J Neonatal-androgens influence the social play of prepubescent rats Horm Behav 1981 15 197 213 7250910
  16. [23]Meaney MJ Dodge AM Beatty WW Sex-dependent effects of amygdaloid lesions on the social play of prepubertal rats Physiol Behav 1981 26 467 472 7195594
  17. [24]Meaney MJ McEwen BS Testosterone implants into the amygdala during the neonatal period masculinize the social play of juvenile female rats Brain Res 1986 398 324 328 3801906
  18. [25]Tonjes R Docke F Dorner G Effects of neonatal intracerebral implantation of sex steroids on sexual behaviour, social play behaviour and gonadotrophin secretion Exp Clin Endocrinol 1987 90 257 263 3450527
  19. [26]Freedman LJ Cassell MD Distribution of dopaminergic fibers in the central division of the extended amygdala of the rat Brain Res 1994 633 243 252 7511034
  20. [27]Chang HT Tian Q Vasoactive intestinal polypeptide (VIP) immunoreactive elements in the caudal ventral striatum of the rat: a light and electron microscopic study Brain Res Bull 1991 26 947 956 1933414
  21. [28]Scibilia RJ Lachowicz JE Kilts CD Topographic nonoverlapping distribution of D1 and D2 dopamine receptors in the amygdaloid nuclear complex of the rat brain Synapse 1992 11 146 154 1385664
  22. [29]Cassell MD Freedman LJ Shi C The intrinsic organization of the central extended amygdala Ann N Y Acad Sci 1999 877 217 241 10415652
  23. [30]Olesen KM Jessen HM Auger CJ Auger AP Dopaminergic activation of estrogen receptors in neonatal brain alters progestin receptor expression and juvenile social play behavior Endocrinology 2005 146 3705 3712 15919740
  24. [31]Pellis SM Pellis VC Locomotor-rotational movements in the ontogeny and play of the laboratory rat Rattus norvegicus Dev Psychobiol 1983 16 269 286 6884577
  25. [32]Moore CL Power KL Variation in maternal care and individual differences in play, exploration, and grooming of juvenile Norway rat offspring Dev Psychobiol 1992 25 165 182 1618369
  26. [33]Stevens R Goldstein R Effects of neonatal testosterone and estrogen on open-field behaviour in rats Physiol Behav 1981 26 551 553 7243970
  27. [35]Panksepp J Siviy S Normansell L The psychobiology of play: theoretical and methodological perspectives Neurosci Biobehav Rev 1984 8 465 492 6392950
  28. [36]Schneider M Koch M Deficient social and play behavior in juvenile and adult rats after neonatal cortical lesion: effects of chronic pubertal cannabinoid treatment Neuropsychopharm 2005 30 944 957 15592349
  29. [37]Trezza V Vanderschuren LJ Bidirectional cannabinoid modulation of social behavior in adolescent rats Psychopharmacology (Berl) 2008 197 217 227 18058088
  30. [44]Olioff M Stewart J Sex differences in the play behavior of prepubescent rats Physiol Behav 1978 20 113 115 662934
  31. [45]Meaney MJ Stewart J Poulin P McEwen BS Sexual differentiation of social play in rat pups is mediated by the neonatal androgen-receptor system Neuroendocrin 1983 37 85 90 6888663
  32. [46]Pellis SM Field EF Smith LK Pellis VC Multiple differences in the play fighting of male and female rats. Implications for the causes and functions of play Neurosci Biobehav Rev 1997 21 105 120 8994213
  33. [47]Meaney MJ Stewart J Neonatal-androgens influence the social play of prepubescent rats Horm Behav 1981 15 197 213 7250910
  34. [49]Panksepp J The ontogeny of play in rats Dev Psychobiol 1981 14 327 332 7250521
  35. [50]Panksepp J Beatty WW Social deprivation and play in rats Behav Neurol Biol 1980 30 197 206 7447871
  36. [51]Pellis SM McKenna MM 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 1992 50 135 145 1449641
  37. [52]Pellis SM Pellis VC McKenna MM Feminine dimension in the play fighting of rats (Rattus norvegicus) and its defeminization neonatally by androgens J Comp Psychol 1994 108 68 73 8174346
  38. [54]Casto JM Ward OB Bartke A Play, copulation, anatomy, and testosterone in gonadally intact male rats prenatally exposed to flutamide Physiol Behav 2003 79 633 641 12954404
  39. [55]Hotchkiss AK Ostby JS Vandenburgh JG Gray LE Jr An environmental antiandrogen, vinclozolin, alters the organization of play behavior Physiol Behav 2003 79 151 156 12834785
  40. [56]Amateau SK Alt JJ Stamps CL McCarthy MM Brain estradiol content in newborn rats: sex differences, regional heterogeneity, and possible de novo synthesis by the female telencephalon Endocrinology 2004 145 2906 2917 14988386
  41. [59]Thor DH Holloway WR Jr Social play in juvenile rats: a decade of methodological and experimental research Neurosci Biobehav Rev 1984 8 455 464 6514252
  42. [60]Wallen K Hormonal influences on sexually differentiated behavior in nonhuman primates Front Neuroendocrinol 2005 26 7 26 15862182
  43. [61]McAbee MD Doncarlos LL Estrogen, but not androgens, regulates androgen receptor messenger ribonucleic acid expression in the developing male rat forebrain Endocrinology 1999 140 3674 3681 10433226
  44. [62]Hull EM Nishita JK Bitran D Dalterio S Perinatal dopamine-related drugs demasculinize rats Science 1984 224 1011 1013 6719125
  45. [63]Gonzales FG Ortega JG Salazar M Effect of neonatal administration of an antidopaminergic drug (metoclopramide) on sexual behavior of male rats Arch Androl 2000 45 137 142 11111861
  46. [64]Gotz F Tonjes R Maywald J Dorner G Short- and long-term effects of a dopamine agonist (lisuride) on sex- specific behavioural patterns in rats Exp Clin Endocrinol 1991 98 111 121 1778225
  47. [65]Tonjes R Gotz F Maywald J Dorner G Influence of a dopamine agonist (lisuride) on sex-specific behavioural patterns in rats. II. Long-term effects Exp Clin Endocrinol 1989 94 48 54 2599021
  48. [66]Simerly RB Hormonal control of the development and regulation of tyrosine hydroxylase expression within a sexually dimorphic population of dopaminergic cells in the hypothalamus Molecular Brain Research 1989 5 297 310 2574404
  49. [67]Balan IS Ugrumov MV Calas A Mailly P Krieger M Thibault J Tyrosine hydroxylase-expressing and/or aromatic L-amino acid decarboxylase-expressing neurons in the mediobasal hypothalamus of perinatal rats: differentiation and sexual dimorphism J Comp Neurol 2000 425 167 176 10954837
  50. [68]Lesage J Bernet F Montel V Dupouy JP Hypothalamic metabolism of neurotransmitters (Serotonin, norepinephrine, dopamine) and NPY, and gonadal and adrenal activities, during the early postnatal period in the rat Neurochem Res 1996 21 87 96 8833228
  51. [69]Connell S Karikari C Hohmann CF Sex-specific development of cortical monoamine levels in mouse Brain Res Dev Brain Res 2004 151 187 191 %19 15246704
  52. [70]Melnikova V Orosco M Calas A Sapronova A Gainetdinov R Delhaye-Bouchaud N Nicolaidis S Rayevsky K Ugrumov M Dopamine turnover in the mediobasal hypothalamus in rat fetuses Neuroscience 1999 89 235 241 10051232
  53. [71]Hol T Niesink M Van Ree JM Spruijt BM Prenatal exposure to morphine affects juvenile play behavior and adult social behavior in rats Pharmacol Biochem Behav 1996 55 615 618 8981592
  54. [72]Niesink RJ van Buren-van DL Van Ree JM Social behavior of juvenile rats after in utero exposure to morphine: dose-time-effect relationship Neuropharmacology 1999 38 1207 1223 10462133
  55. [73]Niesink RJ Vanderschuren LJ Van Ree JM Social play in juvenile rats after in utero exposure to morphine Neurotoxicology 1996 17 905 912 9198792
  56. [74]Mani SK Allen JMC Clark JH Blaustein JD O'Malley BW Convergent pathways for steroid hormone- and neurotransmitter- induced rat sexual behavior Science 1994 265 1246 1249 7915049
  57. [75]Beyer C Gonzalez-Flores O Gonzalez-mariscal G Progesterone receptor participates in the stimulatory effect of LHRH, prostaglandin E2, and cyclic AMP on lordosis and proceptive behaviors in rats J Neuroendocrinology 1997 9 609 614 9283049
  58. [76]Chu HP Morales JC Etgen AM Cyclic GMP may potentiate lordosis behaviour by progesterone receptor activation J Neuroendocrinol 1999 11 107 113 10048465
  59. [77]Mani SK Allen JMC Rettori V Mccann SM O'Malley BW Clark JH Nitric oxide mediates sexual behavior in female rats Proc Natl Acad Sci USA 1994 91 6468 6472 7517551 PMC44223
  60. [78]Schreihofer DA Resnick EM Lin VY Shupnik MA Ligand-independent activation of pituitary er: dependence on pka-stimulated pathways Endocrinology 2001 142 3361 3368 11459779
  61. [79]Aronica SM Katzenellenbogen BS Stimulation of estrogen receptor-mediated transcription and alteration in the phosphorylation state of the rat uterine estrogen Mol Endocrinol 1993 7 743 752 7689695
  62. [80]Apostolakis EM Garai J Lohmann JE Clark JH O'Malley BW Epidermal growth factor activates reproductive behavior independent of ovarian steroids in female rodents Mol Endocrinol 2000 14 1086 1098 10894157
  63. [82]Chamove AS Rosenblum LA Harlow HF Monkeys (Macaca mulatta) raised only with peers A pilot study Anim Behav 1973 21 316 325 4198504
  64. [84]Moore CL Maternal behavior of rats is affected by hormonal condition of pups J Comp Physiol Psychol 1982 96 123 129 7056895
  65. [85]Moore CL Power KL Variation in maternal care and individual differences in play, exploration, and grooming of juvenile Norway rat offspring Dev Psychobiol 1992 25 165 182 1618369
  66. [86]Birke LI Sadler D Differences in maternal behavior of rats and the sociosexual development of the offspring Dev Psychobiol 1987 20 85 99 3556787
  67. [87]Parent CI Meaney MJ The influence of natural variations in maternal care on play fighting in the rat Dev Psychobiol 2008 18846499
  68. [88]De Vries GJ Minireview: Sex differences in adult and developing brains: compensation, compensation, compensation Endocrinology 2004 145 1063 1068 14670982
  69. [89]Champagne FA Weaver IC Diorio J Dymov S Szyf M Meaney MJ Maternal care associated with methylation of the estrogen receptor-alpha1b promoter and estrogen receptor-alpha expression in the medial preoptic area of female offspring Endocrinology 2006 147 2909 2915 16513834
  70. [90]Kurian JR Forbes-Lorman RM Auger AP Sex difference in mecp2 expression during a critical period of rat brain development Epigenetics 2007 2 173 178 17965589
  71. [91]Nan X Ng HH Johnson CA Laherty CD Turner BM Eisenman RN Bird A Transcriptional repression by the methyl-CpG-binding protein MeCP2 involves a histone deacetylase complex Nature 1998 393 386 389 9620804
  72. [92]Weaver IC Cervoni N Champagne FA D'Alessio AC Sharma S Seckl JR Dymov S Szyf M Meaney MJ Epigenetic programming by maternal behavior Nat Neurosci 2004 7 847 854 15220929

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Authors
Auger, A. P., & Olesen, K. M.
Affiliations
  • University of Wisconsin–Madison (US)
  • University of Massachusetts Amherst (US)
Corresponding author
Auger, A. P.
ORCID
Auger, A. P.
Venue
Journal of Neuroendocrinology
Publisher
Wiley
Published
2009-05-15
Volume
21
Issue
6
Pages
519-525
ISSN
  • 0953-8194 (ISSN-L)
  • 1365-2826
DOI
10.1111/j.1365-2826.2009.01871.x
PMC
PMC2739448
OpenAlex
W1544936282
Cited by
142
References
9
Citations by year
2026: 6 · 2025: 5 · 2024: 13 · 2023: 11 · 2022: 7 · 2021: 10 · 2020: 6 · 2019: 12 · 2018: 12 · 2017: 7 · 2016: 9 · 2015: 11 · 2014: 8 · 2013: 5 · 2012: 2
FWCI
0.51
Type
journal article
Language
en
Open access
Licence
onlinelibrary.wiley.com/termsAndConditions#vor (vor)
Locations
  • Journal of Neuroendocrinology (publishedVersion)
  • PubMed (publishedVersion)
  • PubMed Central (acceptedVersion)
Funders
  • National Institutes of Health
  • National Institute of Mental Health (R01MH072956)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Sexual Differentiation and Disorders
  • Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
  • Health Sciences › Medicine › Reproductive Medicine › Hypothalamic control of reproductive hormones
Keywords
sexual dimorphism, sexual differentiation of the brain, maternal environment, social development (developmental psychology), neurotransmitters, rats
MeSH terms
Animals, Behavior, Animal, Brain, Humans, Play and Playthings, Receptors, Steroid, Sex Characteristics, Gonadal Steroid Hormones, Social Behavior, Neurotransmitter Agents, Epigenesis, Genetic, Rats

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