The DOI matches its Crossref record; 33 of the 33 references it cites were found in a registry or an index.
Prenatal stress feminizes juvenile play patterns in male rats
Abstract
Sexually dimorphic rough-and-tumble play patterns were compared in male and female rats derived from control mothers and mothers stressed from days 14-21 of pregnancy. Animals were weaned into groups of 8 consisting of 2 males and 2 females from each treatment. Play in the home cage was recorded at 25, 28, 31, 34, 37 and 45 days of age and was most intense on day 31. The overall level of play was significantly higher in control males than in females or stressed males. Control males showed higher levels of the pinning component of rough-and-tumble play than females or stressed males. No play partner preferences were detected in any group. In adulthood, a higher percentage of stressed than control males displayed the female lordotic pattern. No deficits in ejaculatory behavior occurred in the stressed males. Since maternal stress alters patterns of plasma testosterone in male fetuses, the data suggest that the sexual differentiation of social play begins during prenatal ontogeny in the rat. The present results show that sexually dimorphic behaviors displayed before puberty are incompletely masculinized in prenatally stressed males, a finding similar to that reported for a number of adult behaviors.
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“the available evidence suggests that the critical period for the differentiation of play begins late in gestation and continues through PND10 (Meaney et al. 1983; Ward and Stehm 1991).”
From Perinatal Exposure to Low Levels of the Environmental Antiandrogen Vinclozolin Alters Sex-Differentiated Social Play and Sexual Behaviors in the Rat (2005) · cites this paper as Ward and Stehm 1991
In the citing paper
“In rats, the ontogeny of play is characterized by an inverted U-shaped function that peaks between PND32 and PND40 (Panskeep 1980; Spear and Brake 1983; Ward and Stehm 1991).”
From Perinatal Exposure to Low Levels of the Environmental Antiandrogen Vinclozolin Alters Sex-Differentiated Social Play and Sexual Behaviors in the Rat (2005) · cites this paper as Ward and Stehm 1991
Citations
Cites
WEISZ, J., & WARD, I. L. (1980) · Endocrinology · doi:10.1210/endo-106-1-306 · Cited by 830
Self-citationPrenatal Stress Feminizes and Demasculinizes the Behavior of Males
Ward, I. L. (1972) · Science · doi:10.1126/science.175.4017.82 · Cited by 545
Self-citationPanksepp, J. (1981) · Developmental Psychobiology · doi:10.1002/dev.420140405 · Cited by 537
The psychobiology of play: Theoretical and methodological perspectives
Panksepp, J., Siviy, S., & Normansell, L. (1984) · Neuroscience & Biobehavioral Reviews · doi:10.1016/0149-7634(84)90005-8 · Cited by 468
WARD, I. L., & WEISZ, J. (1984) · Endocrinology · doi:10.1210/endo-114-5-1635 · Cited by 447
Self-citationA descriptive study of social development in the rat (Rattus norvegicus)
Meaney, M. J., & Stewart, J. (1981) · Animal Behaviour · doi:10.1016/s0003-3472(81)80149-2 · Cited by 403
Maternal Stress Alters Plasma Testosterone in Fetal Males
Ward, I. L., & Weisz, J. (1980) · Science · doi:10.1126/science.7188648 · Cited by 370
Self-citationNeonatal-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
Poole, T. B., & Fish, J. (1976) · Journal of Zoology · doi:10.1111/j.1469-7998.1976.tb02294.x · Cited by 149
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
Meaney, M. J., Stewart, J., Poulin, P., & McEwen, B. S. (2008) · Neuroendocrinology · doi:10.1159/000123524 · Cited by 144
The prenatal stress syndrome: Current status
Ward, I. L. (1984) · Psychoneuroendocrinology · doi:10.1016/0306-4530(84)90016-7 · Cited by 136
Self-citationRhees, R. W., & Fleming, D. E. (1981) · Physiology & Behavior · doi:10.1016/0031-9384(81)90057-3 · Cited by 131
Maternal Stress Decreases Steroid Aromatase Activity in Brains of Male and Female Rat Fetuses
Weisz, J., Brown, B., & Ward, I. L. (2008) · Neuroendocrinology · doi:10.1159/000123410 · Cited by 129
Self-citationInfluence of maternal stress on offspring sexual behaviour
Dahlöf, L., Hȧrd, E., & Larsson, K. (1977) · Animal Behaviour · doi:10.1016/0003-3472(77)90047-1 · Cited by 111
Exogenous androgen activates female behavior in noncopulating, prenatally stressed male rats.
Ward, I. L. (1977) · Journal of Comparative and Physiological Psychology · doi:10.1037/h0077342 · Cited by 77
Self-citationVOMSAAL, F. (1983) · Physiology & Behavior · doi:10.1016/0031-9384(83)90162-2 · Cited by 74
Thor, D. H., & Holloway, W. R. (1986) · Behavioral Neuroscience · doi:10.1037/0735-7044.100.2.275 · Cited by 73
Kinsley, C. H. (1988) · Hormones and Behavior · doi:10.1016/0018-506x(88)90032-3 · Cited by 72
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
Ward, I. L., & Reed, J. (1985) · Behavioral Neuroscience · doi:10.1037//0735-7044.99.2.301 · Cited by 67
Self-citationSexual Behavior Differentiation
Ward, I. L., & Ward, O. B. (1985) · Handbook of behavioral neurobiology · doi:10.1007/978-1-4684-4832-0_4 · Cited by 64
Self-citationCrump, C. J., & Chevins, P. F. D. (1989) · Hormones and Behavior · doi:10.1016/0018-506x(89)90047-0 · Cited by 61
Prenatal stress interacts with prepuberal social isolation to reduce male copulatory behavior
Dunlap, J. L., Zadina, J. E., & Gougis, G. (1978) · Physiology & Behavior · doi:10.1016/0031-9384(78)90158-0 · Cited by 58
Orth, J. M., Weisz, J., Ward, O. B., & Ward, I. L. (1983) · Biology of Reproduction · doi:10.1095/biolreprod28.3.625 · Cited by 46
Self-citationCrowding pregnant mice affects attack and threat behavior of male offspring
Harvey, P. W., & Chevins, P. F. D. (1985) · Hormones and Behavior · doi:10.1016/0018-506x(85)90009-1 · Cited by 42
Salisbury, R. L., Reed, J., Ward, I. L., & Weisz, J. (1989) · Biology of Reproduction · doi:10.1095/biolreprod40.1.111 · Cited by 17
Self-citationMcLeod, P. J., & Brown, R. E. (1988) · Psychobiology · doi:10.3758/bf03327334 · Cited by 15
Ohkawa, T. (1987) · Folia Endocrinologica Japonica · doi:10.1507/endocrine1927.63.7_823 · Cited by 15
Ward, I. L., Ward, O., Hayden, O. B., Weisz, J., & Orth, J. (1990) · Endocrinology · doi:10.1210/endo-127-1-88 · Cited by 12
Self-citationNaloxone induces copulation in control but not in prenatally stressed male rats
Rhees, R. W., Badger, D. S., & Fleming, D. E. (1983) · Bulletin of the Psychonomic Society · doi:10.3758/bf03330021 · Cited by 6
Prenatal stress suppresses hunger-induced rat-pup killing in Long-Evans rats
Miley, W. M. (1983) · Bulletin of the Psychonomic Society · doi:10.3758/bf03330019 · Cited by 4
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Metadata
- Authors
- Ward, I. L., & Stehm, K. E.
- Affiliations
- Villanova University (US)
- Venue
- Physiology & Behavior
- Publisher
- Elsevier BV
- Published
- 1991-09
- Volume
- 50
- Issue
- 3
- Pages
- 601-605
- ISSN
- 0031-9384 (ISSN-L)
- OpenAlex
- W2010391369
- Cited by
- 125
- References
- 33
- Citations by year
- 2025: 2 · 2023: 2 · 2021: 2 · 2020: 2 · 2019: 1 · 2018: 3 · 2017: 1 · 2016: 5 · 2015: 4 · 2014: 9 · 2013: 3 · 2012: 3
- FWCI
- 0.93
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Physiology & Behavior (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health (5k05mh000049-15, 5r01hd004688-23)
- National Institute of Mental Health (2 KO5 MH00049)
- Eunice Kennedy Shriver National Institute of Child Health and Human Development (HD04688)
- Topics
- Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Sexual Differentiation and Disorders
- Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Neuroendocrine regulation and behavior
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Keywords
- prenatal stress, maternal stress, rough-and-tumble play, sex differences, juvenile social behavior, lordosis, sexual differentiation, testosterone, masculinization, male rats
- MeSH terms
- Animals, Behavior, Animal, Ejaculation, Female, Male, Pregnancy, Prenatal Exposure Delayed Effects, Rats, Inbred Strains, Sexual Behavior, Animal, Sexual Maturation, Stress, Psychological, Testosterone, Rats
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