Cited by 125Sexual Differentiation and DisordersNeuroendocrine regulation and behaviorStress Responses and Cortisol

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

Ward, Ingeborg L., Stehm, Kathleen E.·1991·Physiology & Behavior

Open this paper in CoChat — free account

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.

Integrity signals

Registry

Crossref · 10.1016/0031-9384(91)90552-y

Cites

33 of 33 references verified0 citation errors · 0 not checkable

Statistics

Recomputing p-values needs the paper’s full text.

Claims the paper makes

This paper’s full text isn’t openly available, so its claims and self-check weren’t run. The registry and citation checks still apply.

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Plasma Testosterone and Progesterone Titers of Pregnant Rats, Their Male and Female Fetuses, and Neonatal Offspring*
WEISZ, J., & WARD, I. L. (1980) · Endocrinology · doi:10.1210/endo-106-1-306 · Cited by 830
Self-citation
Prenatal Stress Feminizes and Demasculinizes the Behavior of Males
Ward, I. L. (1972) · Science · doi:10.1126/science.175.4017.82 · Cited by 545
Self-citation
The ontogeny of play in rats
Panksepp, 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
Differential Effects of Maternal Stress on Circulating Levels of Corticosterone, Progesterone, and Testosterone in Male and Female Rat Fetuses and Their Mothers*
WARD, I. L., & WEISZ, J. (1984) · Endocrinology · doi:10.1210/endo-114-5-1635 · Cited by 447
Self-citation
A 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-citation
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
An investigation of individual, age and sexual differences in the play of Rattus norvegicus (Mammalia: Rodentia)
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

Show all 33 references

Sorted by citations

Theorizing the father–child relationship: mechanisms and developmental outcomes
Paquette, D. (2004) · Human Development · doi:10.1159/000078723 · Cited by 904
Human behavioral sex differences: A role for gonadal hormones during early development?
Collaer, M. L., & Hines, M. (1995) · Psychological Bulletin · doi:10.1037/0033-2909.118.1.55 · Cited by 779
Alterations induced by gestational stress in brain morphology and behaviour of the offspring
Weinstock, M. (2001) · Progress in Neurobiology · doi:10.1016/s0301-0082(01)00018-1 · Cited by 791
Annual Research Review: Prenatal stress and the origins of psychopathology: an evolutionary perspective
Glover, V. (2011) · Journal of Child Psychology and Psychiatry · doi:10.1111/j.1469-7610.2011.02371.x · Cited by 569
Sex differences, gender and addiction
Becker, J. B., McClellan, M. L., & Reed, B. G. (2016) · Journal of Neuroscience Research · doi:10.1002/jnr.23963 · Cited by 570
Epigenetic and transgenerational reprogramming of brain development
Bale, T. L. (2015) · Nature Reviews Neuroscience · doi:10.1038/nrn3818 · Cited by 505
Prenatal Anxiety Predicts Individual Differences in Cortisol in Pre-Adolescent Children
O’Connor, T. G., Ben‐Shlomo, Y., Heron, J., Golding, J., Adams, D., & Glover, V. A. S. (2005) · Biological Psychiatry · doi:10.1016/j.biopsych.2005.03.032 · Cited by 474
Maternal psychological distress during pregnancy in relation to child development at age two
DiPietro, J. A., Novak, M. F. S. X., Costigan, K. A., Atella, L. D., & Reusing, S. P. (2006) · Child Development · doi:10.1111/j.1467-8624.2006.00891.x · Cited by 390
Environmental enrichment during adolescence reverses the effects of prenatal stress on play behaviour and HPA axis reactivity in rats.
Morley‐Fletcher, S., Rea, M., Maccari, S., & Laviola, G. (2003) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2003.03070.x · Cited by 373
Gender Differences in the Effects of Prenatal Stress on Brain Development and Behaviour
Weinstock, M. (2007) · Neurochemical Research · doi:10.1007/s11064-007-9339-4 · Cited by 349
Prenatal exposure to a repeated variable stress paradigm elicits behavioral and neuroendocrinological changes in the adult offspring: potential relevance to schizophrenia
Koenig, J. I., Elmer, G. I., Shepard, P. D., Lee, P. R., Mayo, C. L., Joy, B., Hercher, E., & Brady, D. L. (2004) · Behavioural Brain Research · doi:10.1016/j.bbr.2004.05.030 · Cited by 297
Environmental Endocrine Modulators and Human Health: An Assessment of the Biological Evidence
Golden, R. J., Noller, K. L., Titus-Ernstoff, L. T., Kaufman, R. H., Mittendorf, R. L., Stillman, R. J., & Reese, E. A. (1998) · Critical Reviews in Toxicology · doi:10.1080/10408449891344191 · Cited by 239
The placenta and neurodevelopment: sex differences in prenatal vulnerability
Bale, T. L. (2016) · Dialogues in Clinical Neuroscience · doi:10.31887/dcns.2016.18.4/tbale · Cited by 236
The World Federation of Societies of Biological Psychiatry (WFSBP) guidelines for the biological treatment of paraphilias
Thibaut, F., Barra, F. D. L., Gordon, H., Cosyns, P., Bradford, J. M. W., & the WFSBP Task Force on Sexual Disorders (2010) · The World Journal of Biological Psychiatry · doi:10.3109/15622971003671628 · Cited by 274
Sexually Dimorphic Effects of Prenatal Stress on Cognition, Hormonal Responses, and Central Neurotransmitters
Bowman, R. E., MacLusky, N. J., Sarmiento, Y., Frankfurt, M., Gordon, M., & Luine, V. N. (2004) · Endocrinology · doi:10.1210/en.2003-1759 · Cited by 216
Social Behavior and Social Motivation in Adolescent Rats
Varlinskaya, E. I., Spear, L. P., & Spear, N. E. (1999) · Physiology & Behavior · doi:10.1016/s0031-9384(98)00285-6 · Cited by 194
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
Alcohol Stimulates ACTH Secretion in the Rat: Mechanisms of Action and Interactions with Other Stimuli
RIVIER, C. L. (1996) · Alcoholism Clinical and Experimental Research · doi:10.1111/j.1530-0277.1996.tb01636.x · Cited by 180
A role for ovarian hormones in sexual differentiation of the brain
FITCH, R. H., & Denenberg, V. H. (1998) · Behavioral and Brain Sciences · doi:10.1017/s0140525x98001216 · Cited by 178
The influence of natural variations in maternal care on play fighting in the rat
Parent, C. I., & Meaney, M. J. (2008) · Developmental Psychobiology · doi:10.1002/dev.20342 · Cited by 175
Critical age windows for neurodevelopmental psychiatric disorders: evidence from animal models
Marco, E. M., Macrì, S., & Laviola, G. (2011) · Neurotoxicity Research · doi:10.1007/s12640-010-9205-z · Cited by 144
Beneficial effects of enriched environment on adolescent rats from stressed pregnancies.
Laviola, G., Rea, M., Morley‐Fletcher, S., Di Carlo, S., Bacosi, A., De Simone, R., Bertini, M., & Pacifici, R. (2004) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2004.03597.x · Cited by 155
Sex Differences in Play Fighting Revisited: Traditional and Nontraditional Mechanisms of Sexual Differentiation in Rats
Pellis, S. M. (2002) · Archives of Sexual Behavior · doi:10.1023/a:1014070916047 · Cited by 124
Stress in pregnancy and infant HPA axis function: Conceptual and methodological issues relating to the use of salivary cortisol as an outcome measure
Egliston, K.-A., McMahon, C. A., & Austin, M. (2006) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2006.10.003 · Cited by 130
Animal models of obstetric complications in relation to schizophrenia
Boksa, P. (2004) · Brain Research Reviews · doi:10.1016/j.brainresrev.2004.01.001 · Cited by 125
Prenatal stress potentiates stress-induced behavior and reduces the propensity to play in juvenile rats
Takahashi, L. K., HAGLIN, C., & Kalin, N. H. (1992) · Physiology & Behavior · doi:10.1016/0031-9384(92)90147-t · Cited by 122
Sex differences in learning deficits induced by prenatal stress in juvenile rats
Gué, M., Bravard, A., Meunier, J., Veyrier, R., Gaillet, S., Récasens, M., & Maurice, T. (2003) · Behavioural Brain Research · doi:10.1016/s0166-4328(03)00250-x · Cited by 116
Intrinsic and extrinsic influences on play fighting in rats: effects of dominance, partner's playfulness, temperament and neonatal exposure to testosterone propionate
Pellis, S. M., & McKenna, M. M. (1992) · Behavioural Brain Research · doi:10.1016/s0166-4328(05)80295-5 · Cited by 134
Testosterone intake and aggressiveness: Real effect or anticipation?
Björkqvist, K., Nygren, T., Björklund, A.-C., & Björkqvist, S.-E. (1994) · Aggressive Behavior · doi:10.1002/1098-2337(1994)20:1 · Cited by 44
Long-term effects of prenatal stress: Changes in adult cardiovascular regulation and sensitivity to stress
Mastorci, F., Vicentini, M., Viltart, O., Manghi, M., Graiani, G., Quaini, F., Meerlo, P., Nalivaiko, E., Maccari, S., & Sgoifo, A. (2009) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2008.08.001 · Cited by 99
Reversal of sex differences in morphine analgesia elicited from the ventrolateral periaqueductal gray in rats by neonatal hormone manipulations
Krzanowska, E. K., Ogawa, S., Pfaff, D. W., & Bodnar, R. J. (2002) · Brain Research · doi:10.1016/s0006-8993(01)03350-9 · Cited by 88
Impact of Prenatal Stress on Neuroendocrine Programming
Viltart, O., & Vanbesien-Mailliot, C. (2007) · The Scientific World JOURNAL · doi:10.1100/tsw.2007.204 · Cited by 91
Prenatal social stress masculinizes the females' behaviour in guinea pigs
Sachser, N., & Kaiser, S. (1996) · Physiology & Behavior · doi:10.1016/s0031-9384(96)80036-9 · Cited by 85
Prenatal hormones and childhood sex segregation: Playmate and play style preferences in girls with congenital adrenal hyperplasia
Pasterski, V., Geffner, M. E., Brain, C. E., Hindmarsh, P. C., Brook, C. G. D., & Hines, M. (2011) · Hormones and Behavior · doi:10.1016/j.yhbeh.2011.02.007 · Cited by 78
Corticosterone Mediates Some but Not Other Behavioural Changes Induced by Prenatal Stress in Rats
Salomon, S., Bejar, C., Schorer-Apelbaum, D., & Weinstock, M. (2010) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2010.02097.x · Cited by 79
Stress During Pregnancy Alters Rat Offspring Morphology and Ultrasonic Vocalizations
Williams, M. T., Hennessy, M. B., & Davis, H. N. (1998) · Physiology & Behavior · doi:10.1016/s0031-9384(97)00428-9 · Cited by 75
Mild Prenatal Stress-Modulated Behavior and Neuronal Spine Density without Affecting Amphetamine Sensitization
Muhammad, A., & Kolb, B. E. (2011) · Developmental Neuroscience · doi:10.1159/000324744 · Cited by 73
Prenatal Stress Effects Are Partially Ameliorated by Prenatal Administration of the Neurosteroid Allopregnanolone
Zimmerberg, B., & Blaskey, L. G. (1998) · Pharmacology Biochemistry and Behavior · doi:10.1016/s0091-3057(97)00540-6 · Cited by 71
Play, copulation, anatomy, and testosterone in gonadally intact male rats prenatally exposed to flutamide
Casto, J. M., Ward, O. B., & Bartke, A. (2003) · Physiology & Behavior · doi:10.1016/s0031-9384(03)00120-3 · Cited by 67
Prenatal stress diminishes gender differences in behavior and in expression of hippocampal synaptic genes and proteins in rats
Biala, Y. N., Bogoch, Y., Bejar, C., Linial, M., & Weinstock, M. (2010) · Hippocampus · doi:10.1002/hipo.20825 · Cited by 68
Changes in the Hormonal Concentrations of Pregnant Rats and Their Fetuses Following Multiple Exposures to a Stressor During the Third Trimester
Williams, M. T., Davis, H. N., McCrea, A. E., Long, S. J., & Hennessy, M. B. (1999) · Neurotoxicology and Teratology · doi:10.1016/s0892-0362(98)00060-9 · Cited by 65
Social stress during pregnancy and lactation affects in guinea pigs the male offsprings' endocrine status and infantilizes their behaviour
Kaiser, S., & Sachser, N. (2001) · Psychoneuroendocrinology · doi:10.1016/s0306-4530(01)00009-9 · Cited by 64
Prenatal stress does not alter innate novelty-seeking behavioral traits, but differentially affects individual differences in neuroendocrine stress responsivity
Clinton, S. M., Miller, S., Watson, S. J., & Akil, H. (2008) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2007.10.012 · Cited by 65
Endocrine and Energetic Mediation of Play Behavior in Free-Living Belding's Ground Squirrels
Nunes, S., Muecke, E.-M., Anthony, J. A., & Batterbee, A. S. (1999) · Hormones and Behavior · doi:10.1006/hbeh.1999.1538 · Cited by 62
Prenatal Stress and Gender Role Behavior in Girls and Boys: A Longitudinal, Population Study
Hines, M., Johnston, K. J., Golombok, S. E., Rust, J. N., Stevens, M., & Golding, J. (2002) · Hormones and Behavior · doi:10.1006/hbeh.2002.1814 · Cited by 61
Perinatal Exposure to Low Levels of the Environmental Antiandrogen Vinclozolin Alters Sex-Differentiated Social Play and Sexual Behaviors in the Rat
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
“Maternal stress during the last week of pregnancy lowers the surge of plasma testosterone that is normally present in male rat fetuses during GD18 and GD19 (Ward and Weisz 1984).”
Background
Sex steroids and human behavior: prenatal androgen exposure and sex-typical play behavior in children
HINES, M. (2003) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1286.026 · Cited by 82
The Social Environment During Pregnancy and Lactation Affects the Female Offsprings’ Endocrine Status and Behaviour in Guinea Pigs
Kaiser, S., & Sachser, N. (1998) · Physiology & Behavior · doi:10.1016/s0031-9384(97)00435-6 · Cited by 57
Effects of neonatal handling and maternal separation on rough‐and‐tumble play in the rat
Arnold, J. L., & Siviy, S. M. (2002) · Developmental Psychobiology · doi:10.1002/dev.10069 · Cited by 54
La relation père-enfant et l'ouverture au monde
Paquette, D. (2004) · Enfance · doi:10.3917/enf.562.0205 · Cited by 80
Prenatal protein malnutrition affects the social interactions of juvenile rats
Almeida, S. S., Tonkiss, J., & Galler, J. R. (1996) · Physiology & Behavior · doi:10.1016/0031-9384(95)02236-8 · Cited by 54
CRF administered to pregnant rats alters offspring behavior and morphology
Williams, M. T., Hennessy, M. B., & Davis, H. N. (1995) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(95)00082-8 · Cited by 51
Here today, not gone tomorrow: long-term effects of corticosterone
Schoech, S. J., Rensel, M. A., & Wilcoxen, T. E. (2012) · Journal für Ornithologie · doi:10.1007/s10336-012-0820-8 · Cited by 45
SDN-MPOA volume in male rats is decreased by prenatal stress, but is not related to ejaculatory behavior
Kerchner, M., & Ward, I. L. (1992) · Brain Research · doi:10.1016/0006-8993(92)90714-k · Cited by 44
Self-citation
Prenatal Stress Alters Reproductive Responses of Rats in Behavioral Estrus and Paced Mating of Hormone-Primed Rats
Frye, C. A., & Orecki, Z. A. (2002) · Hormones and Behavior · doi:10.1006/hbeh.2002.1834 · Cited by 43
Postnatal protein malnutrition affects play behavior and other social interactions in juvenile rats
Almeida, S. S., & de Araújo, M. J. (2001) · Physiology & Behavior · doi:10.1016/s0031-9384(01)00554-6 · Cited by 42
Exposure to prenatal life events stress is associated with masculinized play behavior in girls
Barrett, E. S., Redmon, J. B., Wang, C., Sparks, A. E., & Swan, S. H. (2014) · NeuroToxicology · doi:10.1016/j.neuro.2013.12.011 · Cited by 38
The influence of aripiprazole, olanzapine and enriched environment on depressant-like behavior, spatial memory dysfunction and hippocampal level of BDNF in prenatally stressed rats
Nowakowska, E., Kus, K., Ratajczak, P., Cichocki, M., & Woźniak, A. (2014) · Pharmacological Reports · doi:10.1016/j.pharep.2013.12.008 · Cited by 33
Lack of evidence for endocrine disrupting effects in rats exposed to fenitrothion in utero and from weaning to maturation
Okahashi, N., Sano, M., Miyata, K., Tamano, S., Higuchi, H., Kamita, Y., & Seki, T. (2004) · Toxicology · doi:10.1016/j.tox.2004.04.020 · Cited by 32
Effects of Maternal Stress on Development and Behaviour in Rat Offspring
Weinstock, M. (2001) · Stress · doi:10.3109/10253890109035015 · Cited by 34
Prenatal Alcohol Exposure Blunts Interleukin‐1‐Induced ACTH and β‐Endorphin Secretion by Immature Rats
Lee, S., & RIVIER, C. L. (1993) · Alcoholism Clinical and Experimental Research · doi:10.1111/j.1530-0277.1993.tb05645.x · Cited by 31
Early life stress alters opioid receptor mRNA levels within the nucleus accumbens in a sex-dependent manner
Chang, L., Kigar, S. L., Ho, J. H., Cuarenta, A., Gunderson, H. C., Baldo, B. A., Bakshi, V. P., & Auger, A. P. (2018) · Brain Research · doi:10.1016/j.brainres.2018.12.040 · Cited by 33
Early life overnutrition induced by litter size manipulation decreases social play behavior in adolescent male rats
Carvalho, A. L. O., Ferri, B. G., de Sousa, F. A. L., Vilela, F. C., & Giusti‐Paiva, A. (2016) · International Journal of Developmental Neuroscience · doi:10.1016/j.ijdevneu.2016.07.005 · Cited by 29
Prenatal tactile stimulation attenuates drug-induced behavioral sensitization, modifies behavior, and alters brain architecture
Muhammad, A., & Kolb, B. E. (2011) · Brain Research · doi:10.1016/j.brainres.2011.05.038 · Cited by 29
Gonadal steroids, brain, and behavior: role of context
Rubinow, D. R., & Schmidt, P. J. (2002) · Dialogues in Clinical Neuroscience · doi:10.31887/dcns.2002.4.2/drubinow · Cited by 27
Is mom too sensitive? Impact of maternal stress during gestation
Bale, T. L. (2005) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2005.03.002 · Cited by 29
Sexual Behavior
Ward, I. L. (1992) · Handbook of behavioral neurobiology · doi:10.1007/978-1-4899-2453-7_5 · Cited by 30
Self-citation
Development of Aggression
Delville, Y., Newman, M. L., Wommack, J. C., Taravosh‐Lahn, K., & Cervantes, M. (2005) · Oxford University Press eBooks · doi:10.1093/acprof:oso/9780195168761.003.0014 · Cited by 28
Double Helix: Reciprocity between juvenile play and brain development
Cooke, B. M., & Shukla, D. (2011) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2011.07.001 · Cited by 27
Children's Use of Slope to Guide Navigation: Sex Differences Relate to Spontaneous Slope Perception
Holmes, C. A., Nardi, D., Newcombe, N. S., & Weisberg, S. M. (2015) · Spatial Cognition and Computation · doi:10.1080/13875868.2015.1015131 · Cited by 27
Development of Play Behavior in Neonatally Undernourished Rats
Loranca, A., Torrero, C., & Salas, M. (1999) · Physiology & Behavior · doi:10.1016/s0031-9384(98)00235-2 · Cited by 28
Sensitive Periods for Hormonal Programming of the Brain
Vries, G. J. D., Fields, C. T., Peters, N. V., Whylings, J., & Paul, M. J. (2014) · Current topics in behavioral neurosciences · doi:10.1007/7854_2014_286 · Cited by 30
Increased time to pregnancy is associated with less optimal neurological condition in 4-year-old singletons, in vitro fertilization itself is not
Schendelaar, P., van den Heuvel, E. R., Heineman, M. J., Gemert, S. L. B., Middelburg, K. J., Seggers, J., & Hadders‐Algra, M. (2014) · Human Reproduction · doi:10.1093/humrep/deu252 · Cited by 25
Disrupted Circadian Rhythm as a Common Player in Developmental Models of Neuropsychiatric Disorders
Marco, E. M., Velarde, E., Llorente, R., & Laviola, G. (2015) · Current topics in behavioral neurosciences · doi:10.1007/7854_2015_419 · Cited by 25
Prenatal stress alters the developmental pattern of behavioral indices of sexual maturation and copulation in male rats
Hernández‐Arteaga, E., González, M. H., Ramírez‐Rentería, M. L., Almanza-Sepúlveda, M. L., Guevara, M. Á., Silva, M. A., & Jaime, H. B. (2016) · Physiology & Behavior · doi:10.1016/j.physbeh.2016.05.008 · Cited by 27
Androgen Threshold to Activate Copulation Differs in Male Rats Prenatally Exposed to Alcohol, Stress, or Both Factors
Ward, I. L., Bennett, A. L., Ward, O. B., Hendricks, S. E., & French, J. A. (1999) · Hormones and Behavior · doi:10.1006/hbeh.1999.1534 · Cited by 25
Self-citation
The Behavior and Postnatal Development in Infant and Juvenile Rats After Ultrasound-Induced Chronic Prenatal Stress
Abramova, O. V., Ushakova, V. M., Zorkina, Y., Zubkov, E. A., Storozheva, Z. I., Morozova, A. Y., & Chekhonin, V. P. (2021) · Frontiers in Physiology · doi:10.3389/fphys.2021.659366 · Cited by 25
Naloxone Treatment Prevents Prenatal Stress Effects on Peritoneal Macrophage Activity in Mice Offspring
Fonseca, E. S. M., Sakai, M., Carvalho-Freitas, M. I. R., & Neto, J. P. (2005) · Neuroendocrinology · doi:10.1159/000088759 · Cited by 21
Glucocorticoids, Stress, and Development
Walker, C., Welberg, L., & Plotsky, P. M. (2002) · Elsevier eBooks · doi:10.1016/b978-012532104-4/50074-3 · Cited by 21
When the individual comes into play: The role of self and the partner in the dyadic play fighting of rats
Achterberg, E. J. M., Burke, C. J., & Pellis, S. M. (2023) · Behavioural Processes · doi:10.1016/j.beproc.2023.104933 · Cited by 20
Sex differences in juvenile play behavior differ among rat strains
Northcutt, K. V., & Nwankwo, V. C. (2018) · Developmental Psychobiology · doi:10.1002/dev.21760 · Cited by 20
Maternal gestational androgens are associated with decreased juvenile play in white-faced marmosets (Callithrix geoffroyi)
Birnie, A. K., Hendricks, S. E., Smith, A. S., Milam, R., & French, J. A. (2012) · Hormones and Behavior · doi:10.1016/j.yhbeh.2012.05.014 · Cited by 18
Neonatal inhalatory anesthetic exposure: reproductive changes in male rats
Arena, A. C., & Pereira, O. C. M. (2002) · Comparative Biochemistry and Physiology Part C Toxicology & Pharmacology · doi:10.1016/s1532-0456(02)00182-5 · Cited by 17
Relationships between play and responses to tickling in male juvenile rats.
Hammond, T., Bombail, V., Nielsen, B. L., Meddle, S. L., Lawrence, A. B., & Brown, S. M. (2019) · Applied Animal Behaviour Science · doi:10.1016/j.applanim.2019.104879 · Cited by 18
Prenatal Stress Alters Progestogens to Mediate Susceptibility to Sex-Typical, Stress-Sensitive Disorders, such as Drug Abuse: A Review
Frye, C. A., Paris, J. J., Osborne, D. M., Campbell, J. C., & Kippin, T. E. (2011) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2011.00052 · Cited by 18
Análise motivacional, causal e funcional da brincadeira em duas espécies de roedores
Vieira, M. L., & Sartorio, R. (2002) · Estudos de Psicologia (Natal) · doi:10.1590/s1413-294x2002000100020 · Cited by 15
Endocrine-Disrupting Chemicals
Frye, C. A. (2014) · Vitamins & Hormones · doi:10.1016/b978-0-12-800095-3.00003-1 · Cited by 22
Sex Steroids and Human Behavior: Implications for Developmental Psychopathology
Alexander, G. M., & Peterson, B. S. (2001) · CNS Spectrums · doi:10.1017/s1092852900022896 · Cited by 14
Perinatal exposures to rotating magnetic fields `demasculinize' neuronal density in the medial preoptic nucleus of male rats
Mulligan, S., & Persinger, M. A. (1998) · Neuroscience Letters · doi:10.1016/s0304-3940(98)00594-1 · Cited by 14
Maternal adverse childhood experiences impact fetal adrenal volume in a sex-specific manner
Duffy, K. A., Sammel, M. D., Johnson, R. L., Kim, D. R., Wang, E. Y., Ewing, G., Hantsoo, L. V., Kornfield, S. L., Bale, T. L., & Epperson, C. N. (2023) · Biology of Sex Differences · doi:10.1186/s13293-023-00492-0 · Cited by 13
Immobilization stress responses in adult rats exposed in utero to immobilization
Mayer, N., Greco, C. R., Bertuzzi, M. L., Rodríguez, N., Vivas, A. B., & Gauna, H. F. (2010) · Stress and Health · doi:10.1002/smi.1329 · Cited by 12
Sexual Differentiation of Brain and Behavior
Forger, N. G., Vries, G. J. D., & Breedlove, S. M. (2014) · Elsevier eBooks · doi:10.1016/b978-0-12-397175-3.00047-8 · Cited by 13
Importance of mother/young contact at parturition and across lactation for the expression of maternal behavior in rabbits
González‐Mariscal, G., Melo, Á. I., Chirino, R., Jim�nez, P., Beyer, C., & Rosenblatt, J. S. (1998) · Developmental Psychobiology · doi:10.1002/(sici)1098-2302(199803)32:2 · Cited by 67
Effects of ACTH applications during pregnancy on the female offsprings' endocrine status and behavior in guinea pigs
Kaiser, S., Brendel, H., & Sachser, N. (2000) · Physiology & Behavior · doi:10.1016/s0031-9384(00)00248-1 · Cited by 12
Gestational chronic mild stress: Effects on acoustic startle in male offspring of rats
Hougaard, K. S., Mandrup, K. R., Kjaer, S. L., Bøgh, I. B., Rosenberg, R., & Wegener, G. (2011) · International Journal of Developmental Neuroscience · doi:10.1016/j.ijdevneu.2011.01.002 · Cited by 10
Differences induced by incubation temperature, versus androgen manipulation, in male leopard geckos (Eublepharis macularius)
Huang, V., & Crews, D. P. (2012) · Physiology & Behavior · doi:10.1016/j.physbeh.2012.06.014 · Cited by 10
Perinatal hypothyroidism increases play behaviors in juvenile rats
Smith, S. G., & Northcutt, K. V. (2017) · Hormones and Behavior · doi:10.1016/j.yhbeh.2017.11.012 · Cited by 9
Early postnatal hypothyroidism reduces juvenile play behavior, but prenatal hypothyroidism compensates for these effects
Northcutt, K. V., Leal-Medina, T. S., & Yoon, Y. S. (2021) · Physiology & Behavior · doi:10.1016/j.physbeh.2021.113594 · Cited by 7
Application of an antiandrogen during pregnancy infantilizes the male offsprings’ behaviour
Wewers, D., Kaiser, S., & Sachser, N. (2004) · Behavioural Brain Research · doi:10.1016/j.bbr.2004.08.009 · Cited by 7
Critical Age Windows for Neurodevelopmental Psychiatric Disorders: Evidence from Animal Models
Marco, E. M., Macrì, S., & Laviola, G. (2010) · Springer eBooks · doi:10.1007/978-1-4614-0785-0_26 · Cited by 7

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)
DOI: 10.1016/0031-9384(91)90552-y
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
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
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

About these checks

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.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review

Prenatal stress feminizes juvenile play patterns in male rats

Abstract

Overview

Integrity signals

Verification

Claims the paper makes

Claims other papers make about this one

Citations

Cites

Cited by

Related

Metadata

Record

About these checks