Cited by 63Stress Responses and CortisolNeuroendocrine regulation and behaviorChild Abuse and Trauma

Altered corticosterone levels and social play behavior after prolonged maternal separation in adolescent male but not female Wistar rats.

Open access
Lundberg, Stina, Martinsson, My, Nylander, Ingrid, Roman, Erika·2017·Hormones and Behavior

Abstract

Early-life socio-environmental factors are crucial for normal developmental processes; adverse experiences early in life can therefore lead to detrimental effects in several physiological systems. The aim of this study was to examine short-term effects of early adverse experiences in a maternal separation (MS) rodent model. In this study two separation conditions were used: daily 15- (MS15) or 360-min (MS360) separation of the litter from the dam during postnatal day 1-21. In early adolescence, male and female offspring were subjected to a single-isolation procedure with analysis of corticosterone levels prior to and after isolation. In addition, social play behavior was assessed during mid-adolescence. There was a clear difference between male and female offspring in both tests performed. There was no difference in corticosterone levels between the female MS groups, whereas MS360 males showed higher baseline and recovery corticosterone levels than MS15 males. The amount of pinning, a specific social play behavior, was affected by rearing with MS360 males having a higher frequency than MS15 males, while there was no difference between the female MS groups. The observation that males but not females are affected by MS360 has previously been reported for adult animals, and herein we show that this difference is present already in adolescence. Changes in corticosterone levels and social behavior following early-life adversity have been associated with adult behavioral alterations, and our results confirm that these changes emerge already within adolescence.

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.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1016/j.yhbeh.2016.11.016

Cites

6 of 6 references verified0 citation errors · 0 not checkable

Statistics

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.

A few free checks a day · papers already verified open instantly · results are public

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?

  • In rats, 3-6 h of daily maternal separation in the first 2 or 3 weeks of life either increased, decreased, or did not affect play behavior.

    “In rats, 3–6 h of daily maternal separation in the first 2 or 3 weeks of life either increased (Veenema and Neumann, 2009; Zimmerberg and Sageser, 2011; Lundberg et al., 2017), decreased (Muhammad and Kolb, 2011), or did not affect (Arnold and Siviy, 2002) play behavior.”

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

Flagged first, then by citations

Research works printed but not linked: 38

  1. Arnold, J.L., Siviy, S.M., 2002. Effects of neonatal handling and maternal separation on rough-and-tumble play in the rat. Dev. Psychobiol. 41:205-215. http://dx.doi.org/ 10.1002/dev.10069. · DOI
  2. Auger, A.P., Olesen, K.M., 2009. Brain sex differences and the organisation of juvenile so- cial play behaviour. J. Neuroendocrinol. 21:519-525. http://dx.doi.org/10.1111/j. 1365-2826.2009.01871.x. · DOI · Paper page
  3. Biggio, F., Pisu, M.G., Garau, A., Boero, G., Locci, V., Mostallino, M.C., Olla, P., Utzeri, C., Serra, M., 2014. Maternal separation attenuates the effect of adolescent social isolation on HPA axis responsiveness in adult rats. Eur. Neuropsychopharmacol. J. Eur. Coll. Neuropsychopharmacol. http://dx.doi.org/10.1016/j.euroneuro.2014.03.009. · DOI
  4. Brown, G.R., Spencer, K.A., 2013. Steroid hormones, stress and the adolescent brain: a comparative perspective. Neuroscience 249:115-128. http://dx.doi.org/10.1016/j. neuroscience.2012.12.016. · DOI
  5. Castelhano-Carlos, M.J., Baumans, V., 2009. The impact of light, noise, cage cleaning and in-house transport on welfare and stress of laboratory rats. Lab. Anim. 43:311-327. http://dx.doi.org/10.1258/la.2009.0080098. · DOI
  6. Daoura, L., Haaker, J., Nylander, I., 2011. Early environmental factors differentially affect voluntary ethanol consumption in adolescent and adult male rats. Alcohol. Clin. Exp. Res. 35:506-515. http://dx.doi.org/10.1111/j.1530-0277.2010.01367.x. · DOI
  7. Daoura, L., Nylander, I., Roman, E., 2013. Qualitative differences in pup-retrieval strategies in a maternal separation paradigm. J. Behav. Brain Sci. 3:603-616. http://dx.doi.org/ 10.4236/jbbs.2013.38064. · DOI
  8. de Kloet, E.R., Sibug, R.M., Helmerhorst, F.M., Schmidt, M.V., Schmidt, M., 2005. Stress, genes and the mechanism of programming the brain for later life. Neurosci. Biobehav. Rev. 29:271-281. http://dx.doi.org/10.1016/j.neubiorev.2004.10.008. · DOI
  9. Dimatelis, J.J., Vermeulen, I.M., Bugarith, K., Stein, D.J., Russell, V.A., 2015. Female rats are resistant to developing the depressive phenotype induced by maternal separation stress. Metab. Brain Dis. http://dx.doi.org/10.1007/s11011-015-9723-8. · DOI
  10. Ehlert, U., 2013. Enduring psychobiological effects of childhood adversity. Psychoneuroendocrinology 38:1850-1857. http://dx.doi.org/10.1016/j.psyneuen. 2013.06.007. · DOI · Paper page
  11. Eiland, L., Romeo, R.D., 2013. Stress and the developing adolescent brain. Neuroscience 249:162-171. http://dx.doi.org/10.1016/j.neuroscience.2012.10.048. · DOI
  12. Ferland, C.L., Schrader, L.A., 2011. Cage mate separation in pair-housed male rats evokes an acute stress corticosterone response. Neurosci. Lett. 489:154-158. http://dx.doi. org/10.1016/j.neulet.2010.12.006. · DOI
  13. Goepfrich, A.A., Gluch, C., Friemel, C.M., Schneider, M., 2013. Behavioral differences in three Wistar Han rat lines for emotional reactivity, cognitive processing and ethanol intake. Physiol. Behav. 110-111:102-108. http://dx.doi.org/10.1016/j.physbeh.2012. 12.019. · DOI
  14. Granholm, L., Roman, E., Nylander, I., 2015. Single housing during early adolescence causes time-, area-and peptide-specific alterations in endogenous opioids of rat brain. Br. J. Pharmacol. 172:606-614. http://dx.doi.org/10.1111/bph.12753. · DOI
  15. Gustafsson, L., Ploj, K., Nylander, I., 2005. Effects of maternal separation on voluntary eth- anol intake and brain peptide systems in female Wistar rats. Pharmacol. Biochem. Behav. 81:506-516. http://dx.doi.org/10.1016/j.pbb.2005.03.016. · DOI
  16. Gustafsson, L., Oreland, S., Hoffmann, P., Nylander, I., 2008. The impact of postnatal envi- ronment on opioid peptides in young and adult male Wistar rats. Neuropeptides 42: 177-191. http://dx.doi.org/10.1016/j.npep.2007.10.006. · DOI
  17. Heim, C., Newport, D.J., Mletzko, T., Miller, A.H., Nemeroff, C.B., 2008. The link between childhood trauma and depression: insights from HPA axis studies in humans. Psychoneuroendocrinology 33:693-710. http://dx.doi.org/10.1016/j.psyneuen.2008. 03.008. · DOI · Paper page
  18. Lai, M.-C., Huang, L.-T., 2011. Effects of early life stress on neuroendocrine and neurobehavior: mechanisms and implications. Pediatr. Neonatol. 52:122-129. http://dx.doi.org/10.1016/j.pedneo.2011.03.008. · DOI
  19. Levine, S., 2002. Regulation of the hypothalamic-pituitary-adrenal axis in the neonatal rat: the role of maternal behavior. Neurotox. Res. 4:557-564. http://dx.doi.org/10. 1080/10298420290030569. · DOI
  20. Lucion, A.B., Bortolini, M.C., 2014. Mother-pup interactions: rodents and humans. Front. Endocrinol. 5:17. http://dx.doi.org/10.3389/fendo.2014.00017. · DOI
  21. Macrì, S., Würbel, H., 2006. Developmental plasticity of HPA and fear responses in rats: a critical review of the maternal mediation hypothesis. Horm. Behav. 50:667-680. http://dx.doi.org/10.1016/j.yhbeh.2006.06.015. · DOI
  22. Meaney, M.J., Stewart, J., Beatty, W.W., 1982. The influence of glucocorticoids during the neonatal period on the development of play-fighting in Norway rat pups. Horm. Behav. 16:475-491. http://dx.doi.org/10.1016/0018-506X(82)90054-X. · DOI
  23. Momeni, S., Segerström, L., Roman, E., 2015. Supplier-dependent differences in intermit- tent voluntary alcohol intake and response to naltrexone in Wistar rats. Front. Neurosci. 9:424. http://dx.doi.org/10.3389/fnins.2015.00424. · DOI
  24. Nylander, I., Roman, E., 2012. Neuropeptides as mediators of the early-life impact on the brain; implications for alcohol use disorders. Front. Mol. Neurosci. 5:77. http://dx.doi. org/10.3389/fnmol.2012.00077. · DOI
  25. Nylander, I., Roman, E., 2013. Is the rodent maternal separation model a valid and effec- tive model for studies on the early-life impact on ethanol consumption? Psychophar- macology 229:555-569. http://dx.doi.org/10.1007/s00213-013-3217-3. · DOI
  26. Oreland, S., Gustafsson-Ericson, L., Nylander, I., 2010. Short-and long-term consequences of different early environmental conditions on central immunoreactive oxytocin and arginine vasopressin levels in male rats. Neuropeptides 44:391-398. http://dx.doi. org/10.1016/j.npep.2010.06.001. · DOI
  27. Palm, S., Hävermark, Å., Meyerson, B.J., Nylander, I., Roman, E., 2011a. When is a Wistar a Wistar? Behavioral profiling of outbred Wistar rats from five different suppliers using the MCSF test. Appl. Anim. Behav. Sci. 135:128-137. http://dx.doi.org/10.1016/j. applanim.2011.08.010. · DOI
  28. Palm, S., Roman, E., Nylander, I., 2011b. Differences in voluntary ethanol consumption in Wistar rats from five different suppliers. Alcohol Fayettev. N 45:607-614. http://dx. doi.org/10.1016/j.alcohol.2010.11.005. · DOI
  29. Palm, S., Roman, E., Nylander, I., 2012. Differences in basal and ethanol-induced levels of opioid peptides in Wistar rats from five different suppliers. Peptides 36:1-8. http:// dx.doi.org/10.1016/j.peptides.2012.04.016. · DOI
  30. Parent, C.I., Meaney, M.J., 2008. The influence of natural variations in maternal care on play fighting in the rat. Dev. Psychobiol. 50:767-776. http://dx.doi.org/10.1002/dev. 20342. · DOI · Paper page
  31. Patchev, V.K., Hayashi, S., Orikasa, C., Almeida, O.F., 1999. Ontogeny of gender-specific re- sponsiveness to stress and glucocorticoids in the rat and its determination by the neonatal gonadal steroid environment. Stress Amst. Neth. 3:41-54. http://dx.doi. org/10.3109/10253899909001111. · DOI
  32. Roman, E., Ploj, K., Nylander, I., 2004. Maternal separation has no effect on voluntary eth- anol intake in female Wistar rats. Alcohol Fayettev. N 33:31-39. http://dx.doi.org/10. 1016/j.alcohol.2004.04.002. · DOI
  33. Roman, E., Gustafsson, L., Berg, M., Nylander, I., 2006. Behavioral profiles and stress-in- duced corticosteroid secretion in male Wistar rats subjected to short and prolonged periods of maternal separation. Horm. Behav. 50:736-747. http://dx.doi.org/10. 1016/j.yhbeh.2006.06.016. · DOI
  34. Teicher, M.H., Tomoda, A., Andersen, S.L., 2006. Neurobiological consequences of early stress and childhood maltreatment: are results from human and animal studies com- parable? Ann. N. Y. Acad. Sci. 1071:313-323. http://dx.doi.org/10.1196/annals.1364. 024. · DOI
  35. Trezza, V., Baarendse, P.J.J., Vanderschuren, L.J.M.J., 2010. The pleasures of play: pharma- cological insights into social reward mechanisms. Trends Pharmacol. Sci. 31: 463-469. http://dx.doi.org/10.1016/j.tips.2010.06.008. · DOI · Paper page
  36. van Hasselt, F.N., Tieskens, J.M., Trezza, V., Krugers, H.J., Vanderschuren, L.J.M.J., Joëls, M., 2012. Within-litter variation in maternal care received by individual pups correlates with adolescent social play behavior in male rats. Physiol. Behav. 106:701-706. http://dx.doi.org/10.1016/j.physbeh.2011.12.007. · DOI · Paper page
  37. Veenema, A.H., Neumann, I.D., 2009. Maternal separation enhances offensive play-fight- ing, basal corticosterone and hypothalamic vasopressin mRNA expression in juvenile male rats. Psychoneuroendocrinology 34:463-467. http://dx.doi.org/10.1016/j. psyneuen.2008.10.017. · DOI · Paper page
  38. Wood, C.M., Nicolas, C.S., Choi, S.-L., Roman, E., Nylander, I., Fernandez-Teruel, A., Kiianmaa, K., Bienkowski, P., de Jong, T.R., Colombo, G., Chastagnier, D., Wafford, K.A., Collingridge, G.L., Wildt, S.J., Conway-Campbell, B.L., Robinson, E.S.J., Lodge, D., 2016. Prevalence and influence of cys407* Grm2 mutation in Hannover-derived Wistar rats: mGlu2 receptor loss links to alcohol intake, risk taking and emotional be- haviour. Neuropharmacology http://dx.doi.org/10.1016/j.neuropharm.2016.03.020. · DOI

Cited by

Sorted by citations

Authors
Lundberg, S., Martinsson, M., Nylander, I., & Roman, E.
Affiliations
Uppsala University (SE)
Corresponding author
Lundberg, Stina
Venue
Hormones and Behavior
Publisher
Elsevier BV
Published
2017-01
Volume
87
Pages
137-144
ISSN
0018-506X (ISSN-L)
OpenAlex
W2555294804
Cited by
63
References
6
Citations by year
2026: 4 · 2025: 5 · 2024: 3 · 2023: 9 · 2022: 7 · 2021: 11 · 2020: 8 · 2019: 5 · 2018: 7 · 2017: 4
FWCI
3.41
Type
journal article
Language
en
Open access
Locations
  • Hormones and Behavior (publishedVersion, cc-by-nc-nd)
  • PubMed (publishedVersion)
  • KTH Publication Database DiVA (KTH Royal Institute of Technology) (submittedVersion, other-oa)
Funders
  • Vetenskapsrådet
  • Systembolaget Aktiebolag
Topics
  • Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
  • Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
  • Social Sciences › Psychology › Clinical Psychology › Child Abuse and Trauma
Keywords
maternal separation, corticosterone, social play, childhood adversity, adolescence, sex differences, Wistar rats, hypothalamic-pituitary-adrenal axis, postnatal development
MeSH terms
Animals, Animals, Newborn, Behavior, Animal, Corticosterone, Female, Male, Maternal Deprivation, Play and Playthings, Sex Characteristics, Sexual Maturation, Social Behavior, Time Factors, Rats, Wistar, 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