The DOI matches its Crossref record; 58 of the 58 references it cites were found in a registry or an index.
Behavioral effects of chronic adolescent stress are sustained and sexually dimorphic
Open accessAbstract
Evidence suggests that women are more susceptible to stress-related disorders than men. Animal studies demonstrate a similar female sensitivity to stress and have been used to examine the underlying neurobiology of sex-specific effects of stress. Although our understanding of the sex-specific effects of chronic adolescent stress has grown in recent years, few studies have reported the effects of adolescent stress on depressive-like behavior. The purpose of this study was to determine if a chronic mixed modality stressor (consisting of isolation, restraint, and social defeat) during adolescence (PND 37-49) resulted in differential and sustained changes in depressive-like behavior in male and female Wistar rats. Female rats exposed to chronic adolescent stress displayed decreased sucrose consumption, hyperactivity in the elevated plus maze, decreased activity in the forced swim test, and a blunted corticosterone response to an acute forced swim stress compared to controls during both adolescence (PND 48-57) and adulthood (PND 96-104). Male rats exposed to chronic adolescent stress did not manifest significant behavioral changes at either the end of adolescence or in adulthood. These data support the proposition that adolescence may be a stress sensitive period for females and exposure to stress during adolescence results in behavioral effects that persist in females. Studies investigating the sex-specific effects of chronic adolescent stress may lead to a better understanding of the sexually dimorphic incidence of depressive and anxiety disorders in humans and ultimately improve prevention and treatment strategies.
Overview
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
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?
The cited source says what the claim attributes to it.
In the citing paper
“Preclinical studies show that during puberty, stressors have stronger behavioral effects on behavior in females than males (20–22).”
From Sexual differentiation of neural mechanisms of stress sensitivity during puberty (2023) · cites this paper as [22]
The cited source says what the claim attributes to it.
In the citing paper
“Sex differences in stress sensitivity emerge at puberty in both humans (63, 64) and other animals (20–22), coinciding with an increased incidence of anxiety in women (10, 12, 14, 15).”
From Sexual differentiation of neural mechanisms of stress sensitivity during puberty (2023) · cites this paper as [22]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Citations
Cites
Validation of open:closed arm entries in an elevated plus-maze as a measure of anxiety in the rat
Pellow, S., Chopin, P., File, S. E., & Briley, M. (1985) · Journal of Neuroscience Methods · doi:10.1016/0165-0270(85)90031-7 · Cited by 5,822
Depression: a new animal model sensitive to antidepressant treatments
PORSOLT, R. D., LE PICHON, M., & JALFRE, M. (1977) · Nature · doi:10.1038/266730a0 · Cited by 4,451
THE GENERAL ADAPTATION SYNDROME AND THE DISEASES OF ADAPTATION1
Selye, H. (1946) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem-6-2-117 · Cited by 2,296
Mood disorders in children and adolescents: an epidemiologic perspective
Kessler, R. C., Avenevoli, S., & Ries Merikangas, K. (2001) · Biological Psychiatry · doi:10.1016/s0006-3223(01)01129-5 · Cited by 1,181
Stress, sensitive periods and maturational events in adolescent depression
Andersen, S. L., & Teicher, M. H. (2008) · Trends in Neurosciences · doi:10.1016/j.tins.2008.01.004 · Cited by 1,005
Sapolsky, R. M., & Meaney, M. J. (1986) · Brain Research Reviews · doi:10.1016/0165-0173(86)90010-x · Cited by 999
Long-term behavioral and neuroendocrine adaptations to adverse early experience
Ladd, C. O., Huot, R. L., Thrivikraman, K. V., Nemeroff, C. B., Meaney, M. J., & Plotsky, P. M. (2000) · Progress in brain research · doi:10.1016/s0079-6123(08)62132-9 · Cited by 726
Laviola, G., Macrı̀, S., Morley-Fletcher, S., & Adriani, W. (2003) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(03)00006-x · Cited by 621
Anhedonia and motivational deficits in rats: Impact of chronic social stress
Rygula, R., Abumaria, N., Flügge, G., Fuchs, E., Rüther, E., & Havemann-Reinecke, U. (2005) · Behavioural Brain Research · doi:10.1016/j.bbr.2005.03.009 · Cited by 554
Principles and pitfalls in the analysis of prenatal treatment effects in multiparous species
Holson, R. R., & Pearce, B. A. (1992) · Neurotoxicology and Teratology · doi:10.1016/0892-0362(92)90020-b · Cited by 503
McCormick, C. M., & Zovkic, I. B. (2006) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2006.07.012 · Cited by 397
Kirby, E. D., Geraghty, A. C., Ubuka, T., Bentley, G. E., & Kaufer, D. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0901176106 · Cited by 379
Stress and the adolescent brain
ROMEO, R. D., & McEWEN, B. S. (2006) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1376.022 · Cited by 379
McCormick, C. M., Smith, C. L., & Mathews, I. Z. (2007) · Behavioural Brain Research · doi:10.1016/j.bbr.2007.09.005 · Cited by 278
Ruis, M. A. W., Brake, J. H. A. T., Buwalda, B., de Boer, S. F., Meerlo, P., Korte, S. M., Blokhuis, H. J., & Koolhaas, J. M. (1999) · Psychoneuroendocrinology · doi:10.1016/s0306-4530(98)00050-x · Cited by 275
Corticosterone response to the plus-mazeHigh correlation with risk assessment in rats and mice
Rodgers, R. J., Haller, J., Holmes, A., Halász, J., WALTON, T., & Brain, P. F. (1999) · Physiology & Behavior · doi:10.1016/s0031-9384(99)00140-7 · Cited by 261
Haller, J., Fuchs, E., Halász, J., & Makara, G. B. (1999) · Brain Research Bulletin · doi:10.1016/s0361-9230(99)00087-8 · Cited by 256
Conditioned defeat in male and female syrian hamsters
Huhman, K. L., Solomon, M. B., Janicki, M., Harmon, A. C., Lin, S. M., Israel, J. E., & Jasnow, A. M. (2003) · Hormones and Behavior · doi:10.1016/j.yhbeh.2003.05.001 · Cited by 239
Avital, A., & Richter‐Levin, G. (2005) · The International Journal of Neuropsychopharmacology · doi:10.1017/s1461145704004808 · Cited by 227
Oldehinkel, A. J., & Bouma, E. M. C. (2011) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2010.10.013 · Cited by 225
Iwasaki-Sekino, A., Mano‐Otagiri, A., Ohata, H., Yamauchi, N., & Shibasaki, T. (2008) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2008.09.003 · Cited by 222
Leussis, M. P., & Andersen, S. L. (2008) · Synapse · doi:10.1002/syn.20462 · Cited by 220
Plasma Adrenal and Gonadal Sex Steroids in Human Pubertal Development
Ducharme, J.-R., Forest, M. G., PERETTI, E. D., Sempe, M., COLLU, R., & Bertrand, J. (1976) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem-42-3-468 · Cited by 203
Social and non-social anxiety in adolescent and adult rats after repeated restraint
Doremus‐Fitzwater, T. L., Varlinskaya, E. I., & SPEAR, L. P. (2009) · Physiology & Behavior · doi:10.1016/j.physbeh.2009.03.025 · Cited by 197
Perinatal environment and its influences on metabolic programming of offspring
Tamashiro, K. L., & Moran, T. H. (2010) · Physiology & Behavior · doi:10.1016/j.physbeh.2010.04.008 · Cited by 195
Enduring and sex-specific effects of adolescent social isolation in rats on adult stress reactivity
Weintraub, A. Y., Singaravelu, J., & Bhatnagar, S. (2010) · Brain Research · doi:10.1016/j.brainres.2010.04.068 · Cited by 186
The Prepuberal and Puberal Growth of the Adrenal (Adrenarche)
Dhom, G. (1973) · Beiträge zur Pathologie · doi:10.1016/s0005-8165(73)80086-1 · Cited by 170
McCormick, C. M., Robarts, D., Kopeikina, K. J., & Kelsey, J. E. (2005) · Hormones and Behavior · doi:10.1016/j.yhbeh.2005.01.008 · Cited by 165
Chronic social stress during adolescence induces cognitive impairment in aged mice
Sterlemann, V., Rammes, G., Wolf, M., Liebl, C., Ganea, K., Müller, M. B., & Schmidt, M. V. (2009) · Hippocampus · doi:10.1002/hipo.20655 · Cited by 147
Pignatelli, D., Xiao, F., Gouveia, A., Ferreira, J. G. G., & Vinson, G. P. (2006) · Journal of Endocrinology · doi:10.1677/joe.1.06972 · Cited by 140
Adriani, W., & Giovanni Laviola, A. (2000) · Neuropharmacology · doi:10.1016/s0028-3908(99)00115-x · Cited by 137
Terranova, M. L., Cirulli, F., & Laviola, G. (1999) · Psychoneuroendocrinology · doi:10.1016/s0306-4530(99)00019-0 · Cited by 126
Sex differences and the HPA axis: implications for psychiatric disease.
Young, E. A. (1998) · PubMed · Cited by 126
Macrı̀, S., Zoratto, F., & Laviola, G. (2011) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2010.12.014 · Cited by 122
Gutman, D. A., & Nemeroff, C. B. (2003) · Physiology & Behavior · doi:10.1016/s0031-9384(03)00166-5 · Cited by 115
Vidal, J., de Bie, J., Granneman, R. A., Wallinga, A. E., Koolhaas, J. M., & Buwalda, B. (2007) · Physiology & Behavior · doi:10.1016/j.physbeh.2007.06.004 · Cited by 112
Giovanni Laviola, A., Adriani, W., Morley‐Fletcher, S., & Terranova, M. L. (2002) · Behavioural Brain Research · doi:10.1016/s0166-4328(01)00420-x · Cited by 105
Desbonnet, L., Garrett, L., Daly, E., McDermott, K. W. G., & Dinan, T. G. (2008) · International Journal of Developmental Neuroscience · doi:10.1016/j.ijdevneu.2008.02.004 · Cited by 98
Zovkic, I. B., Wilton, A., Styles, A., & McCormick, C. M. (2008) · Behavioural Brain Research · doi:10.1016/j.bbr.2008.02.004 · Cited by 97
Aggression persists after ovariectomy in female rats
DeBold, J. F., & Miczek, K. A. (1984) · Hormones and Behavior · doi:10.1016/0018-506x(84)90041-2 · Cited by 91
Rivest, S., Plotsky, P. M., & RIVIER, C. L. (2008) · Neuroendocrinology · doi:10.1159/000126365 · Cited by 89
Coping strategies in male and female rats exposed to multiple stressors
Campbell, T., Lin, S. M., DeVries, C., & Lambert, K. G. (2003) · Physiology & Behavior · doi:10.1016/s0031-9384(03)00033-7 · Cited by 86
(2006) · PubMed · Cited by 77
Resilience and vulnerability are dose-dependently related to neonatal stressors in mice
Macrı̀, S., Granstrem, O., Shumilina, M. V., Santos, F. J., Berry, A., Saso, L., & Laviola, G. (2009) · Hormones and Behavior · doi:10.1016/j.yhbeh.2009.07.006 · Cited by 68
Tõnissaar, M., Mällo, T., Eller, M., Häidkind, R., Kõiv, K., & Harro, J. (2007) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2007.08.001 · Cited by 67
den Berg, C. L. V., Lamberts, R. R., Wolterink, G., Wiegant, V. M., & van Ree, J. M. (1998) · Brain Research · doi:10.1016/s0006-8993(98)00397-7 · Cited by 67
Sex and estrous cycle differences in the display of conditioned defeat in Syrian hamsters
Solomon, M. B., Karom, M. C., & Huhman, K. L. (2007) · Hormones and Behavior · doi:10.1016/j.yhbeh.2007.04.007 · Cited by 65
Effects of pair-housing after social defeat experience on elevated plus-maze behavior in rats
Nakayasu, T., & Ishii, K. (2008) · Behavioural Processes · doi:10.1016/j.beproc.2008.02.007 · Cited by 61
The corticomedial amygdala and learning in an agonistic situation in the rat
Bolhuis, J. J., FitzGerald, R., Dijk, D., & KOOLHAAS, J. (1984) · Physiology & Behavior · doi:10.1016/0031-9384(84)90311-1 · Cited by 55
Neuropeptides, Neurotransmitters, Neurosteroids, and the Onset of Puberty
Genazzani, A. R., Bernardi, F., Monteleone, P., Luisi, S. V., & Luisi, M. (2000) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2000.tb06210.x · Cited by 48
Faruzzi, A. N., Solomon, M. B., Demas, G. E., & Huhman, K. L. (2005) · Hormones and Behavior · doi:10.1016/j.yhbeh.2004.11.023 · Cited by 47
Li, X. F., Edward, J., Mitchell, J. C., Shao, B., Bowes, J., Coen, C. W., Lightman, S. L., & O'Byrne, K. T. (2004) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2004.01209.x · Cited by 45
Apter, S., & Eriksson, C. J. P. (2005) · Alcohol and Alcoholism · doi:10.1093/alcalc/agh220 · Cited by 26
Acute restraint stress produces behavioral despair in weanling rats in the forced swim test
Bernal‐Morales, B., Contreras, C. M., & Cueto‐Escobedo, J. (2009) · Behavioural Processes · doi:10.1016/j.beproc.2009.06.006 · Cited by 25
Kinsey‐Jones, J. S., Li, X. F., Bowe, J. E., Lightman, S. L., & O'Byrne, K. T. (2006) · Stress · doi:10.1080/10253890601040535 · Cited by 24
Cruz, F. C., Leão, R. M., Marin, M. T., & Planeta, C. S. (2010) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2010.05.001 · Cited by 24
Kinkead, B. L., Yan, F., Owens, M. J., & Nemeroff, C. B. (2007) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2007.11.005 · Cited by 21
Role of noradrenaline in behavioral changes after defeat in male and female rats
Scholtens, J., Roozen, M., Mirmiran, M., & van de Poll, N. E. (1990) · Behavioural Brain Research · doi:10.1016/0166-4328(90)90057-l · Cited by 15
Flagged first, then by citations
Cited by
Sorted by citations
Stress and the developing adolescent brain
Eiland, L. R., & Romeo, R. D. (2012) · Neuroscience · doi:10.1016/j.neuroscience.2012.10.048 · Cited by 539
Factors influencing behavior in the forced swim test
Bogdanova, O. V., Kanekar, S., D’Anci, K. E., & Renshaw, P. F. (2013) · Physiology & Behavior · doi:10.1016/j.physbeh.2013.05.012 · Cited by 494
Sex Differences in Vulnerability and Resilience to Stress Across the Life Span
Hodes, G. E., & Epperson, C. N. (2019) · Biological Psychiatry · doi:10.1016/j.biopsych.2019.04.028 · Cited by 417
Sex differences in anxiety and emotional behavior
Donner, N. C., & Lowry, C. A. (2013) · Pflügers Archiv - European Journal of Physiology · doi:10.1007/s00424-013-1271-7 · Cited by 379
Sex differences in the neuro-immune consequences of stress: Focus on depression and anxiety
Bekhbat, M., & Neigh, G. N. (2017) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2017.02.006 · Cited by 376
Self-citation
Metadata
- Authors
- Bourke, C. H., & Neigh, G. N.
- Affiliations
- Emory University (US)
- Corresponding author
- Neigh, Gretchen N.
- Venue
- Hormones and Behavior
- Publisher
- Elsevier BV
- Published
- 2011-06
- Volume
- 60
- Issue
- 1
- Pages
- 112-120
- ISSN
- 0018-506X (ISSN-L)
- PMC
- PMC3112263
- OpenAlex
- W1988474369
- Cited by
- 201
- References
- 58
- Citations by year
- 2026: 5 · 2025: 9 · 2024: 9 · 2023: 11 · 2022: 12 · 2021: 23 · 2020: 5 · 2019: 25 · 2018: 13 · 2017: 16 · 2016: 14 · 2015: 13 · 2014: 17 · 2013: 15 · 2012: 13
- FWCI
- 5.78
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Hormones and Behavior (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institute of Environmental Health Sciences (T32ES012870)
- Topics
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Neuroendocrine regulation and behavior
- Keywords
- sex differences, depression-like behavior, social defeat, restraint stress, isolation stress, forced swim test, sucrose intake, hyperactivity, anxiety disorders
- MeSH terms
- Adolescent, Adolescent Behavior, Animals, Corticosterone, Dominance-Subordination, Female, Humans, Male, Restraint, Physical, Sex Characteristics, Sex Factors, Social Behavior, Stress, Psychological, Swimming, Rats, Wistar, Maze Learning, Rats, Long-Evans, 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