Hormonal programming of rat social play behavior: Standardized techniques will aid synthesis and translation to human health
Abstract
Early social behaviors like juvenile play are important for normal cognitive and social development. Deficits in these behaviors are associated with neurodevelopmental disorders, such as autism. Rat juvenile rough-and-tumble play is a useful behavioral biomarker of neurodevelopment, and is sensitive to chemical factors such as pre and neonatal hormones. Despite a rich body of literature characterizing hormonal programming of rodent juvenile play, the physiological mechanisms that regulate the organization of play behavior are not well characterized. Synthesizing results to understand the role of endocrine signaling in the development of play behavior remains difficult due to methodological inconsistency across studies. In this review, we synthesize what is known about hormonal mechanisms programming play, advocate standardized protocols for investigating rat play, and identify key areas where future research is needed. A synthetic understanding of the relationship between endocrine signaling and behavioral programming will improve our ability to understand the development and onset of neurodevelopmental disorders in humans and ultimately will help prevent these devastating conditions.
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Rat juvenile social play is sensitive to chemical factors such as prenatal and neonatal hormones and is a useful behavioral marker of neurodevelopment.
“Rat juvenile social play is sensitive to chemical factors such as prenatal and neonatal hormones and is a useful behavioral marker of neurodevelopment as severe deficits in this behavior are associated with neurodevelopmental disorders [7].”
From Developmental exposure to low levels of ethinylestradiol affects social play in juvenile male rats (2020) · cites this paper as [7]
Isolation is a strong stressor per se and represents an important confounding factor.
“Isolation is a strong stressor per se [53] and, although it may enhance the emergence of effects on play [7], it represents an important confounding factor.”
From Developmental exposure to low levels of ethinylestradiol affects social play in juvenile male rats (2020) · cites this paper as [7]
Cites
Hormones and endocrine-disrupting chemicals: low-dose effects and nonmonotonic dose responses
Vandenberg, L. N., Colborn, T., Hayes, T. B., Heindel, J. J., Jacobs, D. R., Lee, D.-H., Shioda, T., Soto, A. M., vom Saal, F. S., Welshons, W. V., et al. (2012) · Endocrine Reviews · doi:10.1210/er.2011-1050 · Cited by 3,209 · see citing works
The extreme male brain theory of autism
Baron-Cohen, S. (2002) · Trends in Cognitive Sciences · doi:10.1016/s1364-6613(02)01904-6 · Cited by 2,007 · see citing works
The Extreme Male-Brain Theory of Autism
Baron‐Cohen, S. (1999) · The MIT Press eBooks · doi:10.7551/mitpress/4945.003.0023 · Cited by 1,413 · see citing works
Understanding Other Minds Perspectives From Developmental Cognitive Neuroscience
Baron‐Cohen, S., Tager-Flusberg, H. B., & Cohen, D. J. (2000) · Cited by 1,187 · see citing works
Early behavioral intervention, brain plasticity, and the prevention of autism spectrum disorder
Dawson, G. (2008) · Development and Psychopathology · doi:10.1017/s0954579408000370 · Cited by 1,138 · see citing works
The Genesis of Animal Play: Testing the Limits
Burghardt, G. M. (2005) · doi:10.7551/mitpress/3229.001.0001 · Cited by 1,094 · see citing works
Behavioral Alterations in Rats Prenatally Exposed to Valproic Acid: Animal Model of Autism
Schneider, T., & Przewłocki, R. (2005) · Neuropsychopharmacology · doi:10.1038/sj.npp.1300518 · Cited by 959 · see citing works
Kasari, C., Freeman, S., & Paparella, T. (2006) · Journal of Child Psychology and Psychiatry · doi:10.1111/j.1469-7610.2005.01567.x · Cited by 951 · see citing works
Xenoestrogens Released from Lacquer Coatings in Food Cans
Brotons, J. A., Olea‐Serrano, F., Villalobos, M., Pedraza, V., & Olea, N. (1995) · Environmental Health Perspectives · doi:10.1289/ehp.95103608 · Cited by 942 · see citing works
Estradiol and the Developing Brain
McCARTHY, M. M. (2008) · Physiological Reviews · doi:10.1152/physrev.00010.2007 · Cited by 885 · see citing works
WEISZ, J., & WARD, I. L. (1980) · Endocrinology · doi:10.1210/endo-106-1-306 · Cited by 830 · see citing works
Organizational and activational effects of sex steroids on brain and behavior: A reanalysis
Arnold, A. P. (1985) · Hormones and Behavior · doi:10.1016/0018-506x(85)90042-x · Cited by 805 · see citing works
Why are autism spectrum conditions more prevalent in males?
Baron-Cohen, S., Lombardo, M. V., Auyeung, B., Ashwin, E., Chakrabarti, B., & Knickmeyer, R. (2011) · PLoS Biology · doi:10.1371/journal.pbio.1001081 · Cited by 754 · see citing works
Organophosphate Pesticide Exposure and Neurodevelopment in Young Mexican-American Children
Eskenazi, B., Marks, A. R., Bradman, A., Harley, K. G., Barr, D. B., Johnson, C. B., Morga, N., & Jewell, N. P. (2007) · Environmental Health Perspectives · doi:10.1289/ehp.9828 · Cited by 705 · see citing works
Prenatal Exposure to Organophosphate Pesticides and IQ in 7-Year-Old Children
Bouchard, M. F., Chevrier, J., Harley, K. G., Kogut, K. R., Vedar, M., Calderon, N., Trujillo, C., Johnson, C. B., Bradman, A., Barr, D. B., et al. (2011) · Environmental Health Perspectives · doi:10.1289/ehp.1003185 · Cited by 675 · see citing works
Parent bisphenol A accumulation in the human maternal-fetal-placental unit.
Schönfelder, G., Wittfoht, W., Hopp, H., Talsness, C. E., Paul, M., & Chahoud, I. (2002) · Environmental Health Perspectives · doi:10.1289/ehp.021100703 · Cited by 668 · see citing works
The Environmental Estrogen Bisphenol A Stimulates Prolactin Release in Vitro and in Vivo
Steinmetz, R. W., Brown, N. G., Allen, D. L., Bigsby, R. M., & Ben‐Jonathan, N. (1997) · Endocrinology · doi:10.1210/endo.138.5.5132 · Cited by 520 · see citing works
Fetal testosterone and autistic traits
Auyeung, B., Baron‐Cohen, S., Ashwin, E., Knickmeyer, R., Taylor, K., & Hackett, G. (2009) · British Journal of Psychology · doi:10.1348/000712608x311731 · Cited by 462 · see citing works
Roberts, E. M., English, P. B., Grether, J. K., Windham, G. C., Somberg, L., & Wolff, C. (2007) · Environmental Health Perspectives · doi:10.1289/ehp.10168 · Cited by 442 · see citing works
Windham, G. C., Zhang, L., Gunier, R., Croen, L. A., & Grether, J. K. (2006) · Environmental Health Perspectives · doi:10.1289/ehp.9120 · Cited by 424 · see citing works
Does play matter? Functional and evolutionary aspects of animal and human play
Smith, P. K. (1982) · Behavioral and Brain Sciences · doi:10.1017/s0140525x0001092x · Cited by 423 · see citing works
Endocrine disruptors and childhood social impairment
Miodovnik, A., Engel, S. M., Zhu, C., Ye, X., Soorya, L. V., Silva, M. J., Calafat, A. M., & Wolff, M. S. (2011) · NeuroToxicology · doi:10.1016/j.neuro.2010.12.009 · Cited by 423 · see citing works
Hertz‐Picciotto, I., Croen, L., Hansen, R. L., Jones, C. R., de Water, J. V., & Pessah, I. N. (2006) · Environmental Health Perspectives · doi:10.1289/ehp.8483 · Cited by 420 · see citing works
Social deprivation and play in rats
Panksepp, J., & Beatty, W. W. (1980) · Behavioral and Neural Biology · doi:10.1016/s0163-1047(80)91077-8 · Cited by 409 · see citing works
Theory of mind and autism: a fifteen year review
Baron‐Cohen, S. (1999) · doi:10.1093/oso/9780198524465.003.0001 · Cited by 390 · see citing works
Hayes, T. B., Anderson, L. L., Beasley, V. R., de Solla, S. R., Iguchi, T., Ingraham, H. A., Kestemont, P., Kniewald, J. R., Kniewald, Z. M., Langlois, V. S., et al. (2011) · The Journal of Steroid Biochemistry and Molecular Biology · doi:10.1016/j.jsbmb.2011.03.015 · Cited by 374 · see citing works
Self-citationSexual differentiation of human behavior: Effects of prenatal and pubertal organizational hormones
Berenbaum, S. A., & Beltz, A. M. (2011) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2011.03.001 · Cited by 340 · see citing works
Abnormal behaviours induced by chemical pollution: a review of the evidence and new challenges
Zala, S. M., & Penn, D. J. (2004) · Animal Behaviour · doi:10.1016/j.anbehav.2004.01.005 · Cited by 339 · see citing works
Wong, C.-I., KELCE, W. R., Sar, M., & Wilson, E. M. (1995) · Journal of Biological Chemistry · doi:10.1074/jbc.270.34.19998 · Cited by 337 · see citing works
Braun, J. M., Kalkbrenner, A. E., Just, A. C., Yolton, K., Calafat, A. M., Sjödin, A., Hauser, R., Webster, G. M., Chen, A., & Lanphear, B. P. (2014) · Environmental Health Perspectives · doi:10.1289/ehp.1307261 · Cited by 328 · see citing works
Winter, J. S. D., Faiman, C., Hobson, W. C., PRASAD, A. V., & Reyes, F. I. (1975) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem-40-4-545 · Cited by 326 · see citing works
The Impact of Endocrine Disruption: A Consensus Statement on the State of the Science
Bergman, Å., Heindel, J. J., Kasten, T., Kidd, K. A., Jobling, S., Neira, M., Zoeller, R. T., Becher, G., Bjerregaard, P., Bornman, R. M. S., et al. (2013) · Environmental Health Perspectives · doi:10.1289/ehp.1205448 · Cited by 324 · see citing works
Teaching symbolic play skills to children with autism using pivotal response training
Stahmer, A. C. (1995) · Journal of Autism and Developmental Disorders · doi:10.1007/bf02178500 · Cited by 307 · see citing works
Konkle, A., & McCarthy, M. (2011) · Endocrinology · doi:10.1210/en.2010-0607 · Cited by 307 · see citing works
Clemens, L. G. (1978) · Hormones and Behavior · doi:10.1016/0018-506x(78)90023-5 · Cited by 284 · see citing works
Foetal testosterone, social relationships, and restricted interests in children
Knickmeyer, R. C., Baron‐Cohen, S., Raggatt, P. R., & Taylor, K. (2004) · Journal of Child Psychology and Psychiatry · doi:10.1111/j.1469-7610.2004.00349.x · Cited by 279 · see citing works
Pellis, S. M., & Pellis, V. C. (1990) · Developmental Psychobiology · doi:10.1002/dev.420230303 · Cited by 255 · see citing works
Juntti, S. A., Tollkuhn, J., Wu, M. V., Fraser, E. J., Soderborg, T., Tan, S., Honda, S.-I., Harada, N., & Shah, N. M. (2010) · Neuron · doi:10.1016/j.neuron.2010.03.024 · Cited by 254 · see citing works
The genesis of animal play: testing the limits
(2005) · Choice Reviews Online · doi:10.5860/choice.43-0314 · Cited by 251 · see citing works
Wersinger, S. R., Sannen, K., Villalba, C., Lubahn, D. B., Rissman, E. F., & Vries, G. J. D. (1997) · Hormones and Behavior · doi:10.1006/hbeh.1997.1419 · Cited by 240 · see citing works
Zuloaga, D. G., Puts, D. A., Jordan, C. L., & Breedlove, S. M. (2008) · Hormones and Behavior · doi:10.1016/j.yhbeh.2008.01.013 · Cited by 236 · see citing works
PELLIS, S. M., FIELD, E. F., SMITH, L. K., & PELLIS, V. C. (1997) · Neuroscience & Biobehavioral Reviews · doi:10.1016/0149-7634(95)00060-7 · Cited by 234 · see citing works
Li, Y., Burns, K. A., Arao, Y., Luh, C. J., & Korach, K. S. (2012) · Environmental Health Perspectives · doi:10.1289/ehp.1104689 · Cited by 234 · see citing works
Hormonal determinants of the development of masculine and feminine behavior in male and female rats
Whalen, R. E., & Edwards, D. A. (1967) · The Anatomical Record · doi:10.1002/ar.1091570208 · Cited by 220 · see citing works
Hines, M., & KAUFMAN, F. R. (1994) · Child Development · doi:10.1111/j.1467-8624.1994.tb00801.x · Cited by 216 · see citing works
Lambright, C. S. (2000) · Toxicological Sciences · doi:10.1093/toxsci/56.2.389 · Cited by 214 · see citing works
Play fighting of rats in comparative perspective: a schema for neurobehavioral analyses
Pellis, S. M., & Pellis, V. C. (1998) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(97)00071-7 · Cited by 210 · see citing works
Strain, P. S., Kerr, M. M., & Ragland, E. U. (1979) · Journal of Autism and Developmental Disorders · doi:10.1007/bf01531291 · Cited by 209 · see citing works
Foetal testosterone and autistic traits in 18 to 24-month-old children
Auyeung, B., Taylor, K., Hackett, G., & Baron-Cohen, S. (2010) · Molecular Autism · doi:10.1186/2040-2392-1-11 · Cited by 208 · see citing works
Kemppainen, J., Langley, E., Wong, C.-I., Bobseine, K., KELCE, W. R., & Wilson, E. M. (1999) · Molecular Endocrinology · doi:10.1210/mend.13.3.0255 · Cited by 207 · see citing works
Effects of sociodramatic play training on children with autism
Thorp, D. M., Stahmer, A. C., & Schreibman, L. (1995) · Journal of Autism and Developmental Disorders · doi:10.1007/bf02179288 · Cited by 202 · see citing works
Prenatal PCB exposure and neonatal behavioral assessment scale (NBAS) performance
Stewart, P., Reihman, J., Lonky, E., Darvill, T., & Pagano, J. J. (2000) · Neurotoxicology and Teratology · doi:10.1016/s0892-0362(99)00056-2 · Cited by 200 · see citing works
Yarbrough, W. G., Quarmby, V. E., Simental, J. A., Joseph, D. R., Sar, M., Lubahn, D. B., Olsen, K. L., French, F. S., & Wilson, E. M. (1990) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)38972-0 · Cited by 199 · see citing works
Play as a reinforcer for maze-learning in juvenile rats
Humphreys, A. P., & Einon, D. F. (1981) · Animal Behaviour · doi:10.1016/s0003-3472(81)80173-x · Cited by 199 · see citing works
de Cock, M., Maas, Y. G. H., & van de Bor, M. (2012) · Acta Paediatrica · doi:10.1111/j.1651-2227.2012.02693.x · Cited by 198 · see citing works
Neonatal-androgens influence the social play of prepubescent rats
MEANEY, M. (1981) · Hormones and Behavior · doi:10.1016/0018-506x(81)90028-3 · Cited by 192 · see citing works
Androgens and autistic traits: A study of individuals with congenital adrenal hyperplasia
Knickmeyer, R. C., Baron‐Cohen, S., Fane, B. A., Wheelwright, S. J., Mathews, G. A., Conway, G. S., Brook, C. G. D., & Hines, M. (2006) · Hormones and Behavior · doi:10.1016/j.yhbeh.2006.02.006 · Cited by 189 · see citing works
Effects of perinatal exposure to PCBs and dioxins on play behavior in Dutch children at school age
Vreugdenhil, H. J. I., Slijper, F. M. E., Mulder, P. G. H., & Weisglas-Kuperus, N. (2002) · Environmental Health Perspectives · doi:10.1289/ehp.021100593 · Cited by 188 · see citing works
Play, Cognitive Development, and the Social World: Piaget, Vygotsky, and Beyond
Nicolopoulou, A. (2010) · Human Development · doi:10.1159/000277285 · Cited by 184 · see citing works
Understanding other minds: Perspectives from developmental cognitive neuroscience, 2nd ed.
Baron‐Cohen, S., Tager-Flusberg, H. B., & Cohen, D. J. (2000) · Cited by 182 · see citing works
Social play in juvenile rats: A decade of methodological and experimental research
Thor, D. H., & Holloway, W. R. (1984) · Neuroscience & Biobehavioral Reviews · doi:10.1016/0149-7634(84)90004-6 · Cited by 176 · see citing works
Implications of Prenatal Steroid Perturbations for Neurodevelopment, Behavior, and Autism
Gore, A. C., Martien, K. M., Gagnidze, K., & Pfaff, D. W. (2014) · Endocrine Reviews · doi:10.1210/er.2013-1122 · Cited by 159 · see citing works
Hines, M., & KAUFMAN, F. R. (1994) · Child Development · doi:10.2307/1131303 · Cited by 153 · see citing works
Effects of Perinatal Exposure to Bisphenol A on Play Behavior of Female and Male Juvenile Rats
Dessì-Fulgheri, F., Porrini, S., & Farabollini, F. (2002) · Environmental Health Perspectives · doi:10.1289/ehp.02110s3403 · Cited by 146 · see citing works
Sex differences in the play behavior of prepubescent rats
Olioff, M., & Stewart, J. (1978) · Physiology & Behavior · doi:10.1016/0031-9384(78)90060-4 · Cited by 145 · see citing works
Meaney, M. J., Stewart, J., Poulin, P., & McEwen, B. S. (2008) · Neuroendocrinology · doi:10.1159/000123524 · Cited by 144 · see citing works
Habert, R., & Picon, R. (1984) · Journal of Steroid Biochemistry · doi:10.1016/0022-4731(84)90383-2 · Cited by 138 · see citing works
The sexual differentiation of social play
Meaney, M. J. (1988) · Trends in Neurosciences · doi:10.1016/0166-2236(88)90164-6 · Cited by 136 · see citing works
Pellis, S. M. (2002) · Archives of Sexual Behavior · doi:10.1023/a:1014070916047 · Cited by 124 · see citing works
Meaney, M. J., & McEwen, B. S. (1986) · Brain Research · doi:10.1016/0006-8993(86)91492-7 · Cited by 122 · see citing works
Von Frijtag, J. C., Schot, M., van den Bos, R., & Spruijt, B. M. (2002) · Developmental Psychobiology · doi:10.1002/dev.10057 · Cited by 116 · see citing works
Early exposure to a low dose of bisphenol A affects socio-sexual behavior of juvenile female rats
Porrini, S., Belloni, V., Seta, D. D., Farabollini, F., Giannelli, G., & Dessì-Fulgheri, F. (2005) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2004.11.014 · Cited by 114 · see citing works
Bentel, J. M., Birrell, S. N., Pickering, M. A., Holds, D. J., Horsfall, D. J., & Tilley, W. D. (1999) · Molecular and Cellular Endocrinology · doi:10.1016/s0303-7207(99)00109-4 · Cited by 110 · see citing works
Effects of genistein exposure on sexually dimorphic behaviors in rats.
Flynn, K. M. (2000) · Toxicological Sciences · doi:10.1093/toxsci/55.2.311 · Cited by 92 · see citing works
Atrazine‐induced changes in aromatase activity in estrogen sensitive target tissues
Holloway, A. C., Anger, D. A., Crankshaw, D., Wu, M., & Foster, W. G. (2007) · Journal of Applied Toxicology · doi:10.1002/jat.1275 · Cited by 90 · see citing works
Olesen, K. M., Jessen, H. M., Auger, C. J., & Auger, A. P. (2005) · Endocrinology · doi:10.1210/en.2005-0498 · Cited by 89 · see citing works
The intersection of neurotoxicology and endocrine disruption
Weiss, B. (2012) · NeuroToxicology · doi:10.1016/j.neuro.2012.05.014 · Cited by 86 · see citing works
Cellular mechanisms of estradiol-mediated masculinization of the brain
Schwarz, J. M., & McCarthy, M. M. (2008) · The Journal of Steroid Biochemistry and Molecular Biology · doi:10.1016/j.jsbmb.2008.03.012 · Cited by 85 · see citing works
Peering into the Dynamics of Social Interactions: Measuring Play Fighting in Rats
Himmler, B. T., Pellis, V. C., & Pellis, S. M. (2013) · Journal of Visualized Experiments · doi:10.3791/4288 · Cited by 81 · see citing works
Two decades of biomonitoring polar bear health in Greenland: a review
Sonne, C., Letcher, R. J., Bechshøft, T., et al. (2012) · Acta veterinaria Scandinavica · doi:10.1186/1751-0147-54-s1-s15 · Cited by 81 · see citing works
An environmental antiandrogen, vinclozolin, alters the organization of play behavior
Hotchkiss, A. K., Ostby, J. S., Vandenbergh, J. G., & Gray, L. E. (2003) · Physiology & Behavior · doi:10.1016/s0031-9384(03)00093-3 · Cited by 77 · see citing works
Molecular Autism: accelerating and integrating research into neurodevelopmental conditions
Buxbaum, J. D., & Baron‐Cohen, S. (2010) · Molecular Autism · doi:10.1186/2040-2392-1-1 · Cited by 77 · see citing works
Pellis, S. M., Pellis, V. C., & McKenna, M. M. (1994) · Journal of Comparative Psychology · doi:10.1037/0735-7036.108.1.68 · Cited by 76 · see citing works
HELLMAN, L., Bradlow, H. L., Freed, S. Z., LEVIN, J., Rosenfeld, R. S., Whitmore, W. F., & Zumoff, B. (1977) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem-45-6-1224 · Cited by 76 · see citing works
Temporal boundary of the sensitive period for hormonal organization of social play in juvenile rats.
Beatty, W. W., Dodge, A. M., Traylor, K. L., & Meaney, M. J. (1981) · Physiology & Behavior · doi:10.1016/0031-9384(81)90017-2 · Cited by 70 · see citing works
Casto, J., Ward, O., & Bartke, A. (2003) · Physiology and Behavior · doi:10.1016/s0031-9384(03)00120-3 · Cited by 64 · see citing works
Progesterone receptors and the sexual differentiation of the medial preoptic nucleus
Quadros, P. S., López, V., Vries, G. J. D., Chung, W. C. J., & Wagner, C. K. (2002) · Journal of Neurobiology · doi:10.1002/neu.10040 · Cited by 63 · see citing works
Nguyen, T. V., Yao, M., & Pike, C. J. (2007) · Endocrinology · doi:10.1210/en.2006-1469 · Cited by 62 · see citing works
Colbert, N. K. W., Pelletier, N. C., Cote, J. M., Concannon, J. B., Jurdak, N. A., Minott, S. B., & Markowski, V. P. (2005) · Environmental Health Perspectives · doi:10.1289/ehp.7509 · Cited by 60 · see citing works
Pazol, K., Wilson, M. E., & Wallen, K. (2004) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2003-032086 · Cited by 50 · see citing works
Progestins can mimic, inhibit and potentiate the actions of androgens
Bardin, C. W., Brown, T. R., ISOMAA, V. V., & Jänne, O. A. (1983) · Pharmacology & Therapeutics · doi:10.1016/0163-7258(83)90023-2 · Cited by 47 · see citing works
Rodent models for autism: A critical review
Belzung, C., Leman, S., Vourc’h, P., & Andres, C. R. (2005) · Drug Discovery Today Disease Models · doi:10.1016/j.ddmod.2005.05.004 · Cited by 43 · see citing works
Progestin-induced changes in play behaviour of the prepubertal rat
Birke, L. I. A., & Sadler, D. (1983) · Physiology & Behavior · doi:10.1016/0031-9384(83)90136-1 · Cited by 36 · see citing works
Behavioral responses of rats exposed to long-term dietary vinclozolin
Flynn, K. M., Delclos, K. B., Newbold, R. R., & Ferguson, S. A. (2001) · Journal of Agricultural and Food Chemistry · doi:10.1021/jf0008893 · Cited by 33 · see citing works
Field, E. F., Whishaw, I. Q., Pellis, S. M., & Watson, N. V. (2006) · Developmental Psychobiology · doi:10.1002/dev.20121 · Cited by 30 · see citing works
Tönjes, R., Döcke, F., & Dörner, G. (2009) · Experimental and Clinical Endocrinology & Diabetes · doi:10.1055/s-0029-1210699 · Cited by 21 · see citing works
Effect of the Antiandrogen Flutamide on Pituitary LH Content and Release
Sardañons, M. L., Heras, M. A. D. L., Calandra, R. S., Solano, A. R., & Podesta, E. J. (2008) · Neuroendocrinology · doi:10.1159/000125224 · Cited by 18 · see citing works
BIRKE, L., & SADLER, D. (1984) · Physiology & Behavior · doi:10.1016/0031-9384(84)90102-1 · Cited by 16 · see citing works
Endocrine disrupting compounds, gonadal hormones, and autism
Braun, J. M. (2012) · Developmental Medicine & Child Neurology · doi:10.1111/j.1469-8749.2012.04372.x · Cited by 15 · see citing works
Baldwin, E. L., & Groos, K. (1899) · The Philosophical Review · doi:10.2307/2176969 · Cited by 15 · see citing works
Flynn, K. M., Delclos, K. B., Newbold, R. R., & Ferguson, S. A. (2005) · Food and Chemical Toxicology · doi:10.1016/j.fct.2005.03.009 · Cited by 14 · see citing works
Götz, F., Tönjes, R., Maywald, J., & Dörner, G. (2009) · Experimental and Clinical Endocrinology & Diabetes · doi:10.1055/s-0029-1211107 · Cited by 12 · see citing works
Birke, L. I. A., & Sadler, D. (1988) · Hormones and Behavior · doi:10.1016/0018-506x(88)90062-1 · Cited by 10 · see citing works
Clues to Autistic Behaviors: Exploring the Role of Endocrine Disruptors
Betts, K. S. (2014) · Environmental Health Perspectives · doi:10.1289/ehp.122-a137 · Cited by 9 · see citing works
Tönjes, R., Götz, F., Maywald, J., et al. (2009) · Experimental and Clinical Endocrinology & Diabetes · doi:10.1055/s-0029-1210879 · Cited by 8 · see citing works
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Research works printed but not linked: 4
- Dessì-Fulgheri, 2002, Effects of perinatal exposure to bisphenol A on play behavior of female and male juvenile rats, Environ. Health Perspect., 110, 403, 10.1289/ehp.02110s3403 · DOI · Paper page
- Meaney, 1981, Neonatal-androgens influence the social play of prepubescent rats, Horm. Behav., 15, 197, 10.1016/0018-506X(81)90028-3 · DOI · Paper page
- Meaney, 1983, Sexual differentiation of social play in rat pups is mediated by the neonatal androgen-receptor system, Neuroendocrinology, 37, 85, 10.1159/000123524 · DOI · Paper page
- Pellis, 1993, Sex and the evolution of play fighting: a review and a model based on the behavior of muroid rodents, J. Play Theory Res., 1, 56
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Developmental origins of sex differences in the neural circuitry of play
VanRyzin, J. W., Marquardt, A. E., & McCarthy, M. M. (2020) · International Journal of Play · doi:10.1080/21594937.2020.1723370 · Cited by 34 · see citing works
“The consensus is that play is essential to the development of adult social behavior, as well as cognition and reproductive success (Blake & McCoy, 2015; Pellis, Pellis, Pelletier, & Leca, 2019; see also Stark & Pellis 2020), but why this is so remains a mystery.”
BackgroundAchterberg, E. J. M., Burke, C. J., & Pellis, S. M. (2023) · Behavioural Processes · doi:10.1016/j.beproc.2023.104933 · Cited by 20 · see citing works
Pinning in the Play Fighting of Rats: A Comparative Perspective With Methodological Recommendations
Himmler, S. M., Himmler, B. T., Stryjek, R., Modlińska, K., Pisula, W., & Pellis, S. M. (2016) · International Journal of Comparative Psychology · doi:10.46867/ijcp.2016.29.00.06 · Cited by 19 · see citing works
Developmental exposure to low levels of ethinylestradiol affects social play in juvenile male rats
Zaccaroni, M., Massolo, A., Beani, L., Seta, D. D., Farabollini, F., Giannelli, G., Fusani, L., & Dessì-Fulgheri, F. (2020) · Toxicological Research · doi:10.1007/s43188-019-00035-z · Cited by 5 · see citing works
Evaluating the play fighting of rats: A sociological perspective
Ham, J. R., Pellis, S. M., Pellis, V. C., & Achterberg, E. J. M. (2026) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2026.110836
- Authors
- Blake, B. E., & McCoy, K. A.
- Affiliations
- East Carolina University (US)
- Corresponding author
- McCoy, Krista A.
- Venue
- Neuroscience & Biobehavioral Reviews
- Publisher
- Elsevier BV
- Published
- 2015-08
- Volume
- 55
- Pages
- 184-197
- ISSN
- 0149-7634 (ISSN-L)
- OpenAlex
- W2275765103
- Semantic Scholar
- ff640bcf921e8df0b553f25308a5d886b50f43aa
- Cited by
- 20
- References
- 106
- Citations by year
- 2026: 1 · 2025: 1 · 2023: 2 · 2022: 2 · 2021: 2 · 2020: 3 · 2018: 3 · 2017: 4 · 2016: 2
- FWCI
- 4.70
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Neuroscience & Biobehavioral Reviews (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Sexual Differentiation and Disorders
- Life Sciences › Neuroscience › Cognitive Neuroscience › Autism Spectrum Disorder Research
- Keywords
- social play, hormone signaling, brain development, autism spectrum disorder, behavioral biomarkers, rat model, social development (developmental psychology)
- MeSH terms
- Animals, Animals, Newborn, Hormones, Humans, Social Behavior, Signal Transduction, Rats, Translational Research, Biomedical, Neurodevelopmental Disorders
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Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
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