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

Hormones and Behavior - Tập 87 - Trang 137-144 - 2017
Stina Lundberg1, My Martinsson1, Ingrid Nylander1, Erika Roman1
1Neuropharmacology, Addiction & Behavior, Department of Pharmaceutical Biosciences, Uppsala University, Box 591, SE -751 24 Uppsala, Sweden

Tài liệu tham khảo

Arnold, 2002, Effects of neonatal handling and maternal separation on rough-and-tumble play in the rat, Dev. Psychobiol., 41, 205, 10.1002/dev.10069 Auger, 2009, Brain sex differences and the organisation of juvenile social play behaviour, J. Neuroendocrinol., 21, 519, 10.1111/j.1365-2826.2009.01871.x Biggio, 2014, Maternal separation attenuates the effect of adolescent social isolation on HPA axis responsiveness in adult rats, Eur. Neuropsychopharmacol. J. Eur. Coll. Neuropsychopharmacol., 10.1016/j.euroneuro.2014.03.009 Brown, 2013, Steroid hormones, stress and the adolescent brain: a comparative perspective, Neuroscience, 249, 115, 10.1016/j.neuroscience.2012.12.016 Burke, 2014, Stress in adolescence and drugs of abuse in rodent models: role of dopamine, CRF, and HPA axis, Psychopharmacology, 231, 1557, 10.1007/s00213-013-3369-1 Castelhano-Carlos, 2009, The impact of light, noise, cage cleaning and in-house transport on welfare and stress of laboratory rats, Lab. Anim., 43, 311, 10.1258/la.2009.0080098 Daoura, 2011, Early environmental factors differentially affect voluntary ethanol consumption in adolescent and adult male rats, Alcohol. Clin. Exp. Res., 35, 506, 10.1111/j.1530-0277.2010.01367.x Daoura, 2013, Qualitative differences in pup-retrieval strategies in a maternal separation paradigm, J. Behav. Brain Sci., 3, 603, 10.4236/jbbs.2013.38064 de Kloet, 2005, Stress, genes and the mechanism of programming the brain for later life, Neurosci. Biobehav. Rev., 29, 271, 10.1016/j.neubiorev.2004.10.008 Dimatelis, 2015, Female rats are resistant to developing the depressive phenotype induced by maternal separation stress, Metab. Brain Dis. Ehlert, 2013, Enduring psychobiological effects of childhood adversity, Psychoneuroendocrinology, 38, 1850, 10.1016/j.psyneuen.2013.06.007 Eiland, 2013, Stress and the developing adolescent brain, Neuroscience, 249, 162, 10.1016/j.neuroscience.2012.10.048 Ferland, 2011, Cage mate separation in pair-housed male rats evokes an acute stress corticosterone response, Neurosci. Lett., 489, 154, 10.1016/j.neulet.2010.12.006 Goepfrich, 2013, Behavioral differences in three Wistar Han rat lines for emotional reactivity, cognitive processing and ethanol intake, Physiol. Behav., 110-111, 102, 10.1016/j.physbeh.2012.12.019 Granholm, 2015, Single housing during early adolescence causes time-, area- and peptide-specific alterations in endogenous opioids of rat brain, Br. J. Pharmacol., 172, 606, 10.1111/bph.12753 Gustafsson, 2005, Effects of maternal separation on voluntary ethanol intake and brain peptide systems in female Wistar rats, Pharmacol. Biochem. Behav., 81, 506, 10.1016/j.pbb.2005.03.016 Gustafsson, 2008, The impact of postnatal environment on opioid peptides in young and adult male Wistar rats, Neuropeptides, 42, 177, 10.1016/j.npep.2007.10.006 Heim, 2008, The link between childhood trauma and depression: insights from HPA axis studies in humans, Psychoneuroendocrinology, 33, 693, 10.1016/j.psyneuen.2008.03.008 Lai, 2011, Effects of early life stress on neuroendocrine and neurobehavior: mechanisms and implications, Pediatr. Neonatol., 52, 122, 10.1016/j.pedneo.2011.03.008 Lehmann, 2000, Long-term biobehavioral effects of maternal separation in the rat: consistent or confusing?, Rev. Neurosci., 11, 383, 10.1515/REVNEURO.2000.11.4.383 Levine, 2001, Primary social relationships influence the development of the hypothalamic–pituitary–adrenal axis in the rat, Physiol. Behav., 73, 255, 10.1016/S0031-9384(01)00496-6 Levine, 2002, Regulation of the hypothalamic-pituitary-adrenal axis in the neonatal rat: the role of maternal behavior, Neurotox. Res., 4, 557, 10.1080/10298420290030569 Levine, 1957, Infantile experience and the maturation of the pituitary adrenal axis, Science, 126, 1347, 10.1126/science.126.3287.1347 Lucion, 2014, Mother-pup interactions: rodents and humans, Front. Endocrinol., 5, 17, 10.3389/fendo.2014.00017 Macrì, 2006, Developmental plasticity of HPA and fear responses in rats: a critical review of the maternal mediation hypothesis, Horm. Behav., 50, 667, 10.1016/j.yhbeh.2006.06.015 Meaney, 1982, The influence of glucocorticoids during the neonatal period on the development of play-fighting in Norway rat pups, Horm. Behav., 16, 475, 10.1016/0018-506X(82)90054-X Momeni, 2015, Supplier-dependent differences in intermittent voluntary alcohol intake and response to naltrexone in Wistar rats, Front. Neurosci., 9, 424, 10.3389/fnins.2015.00424 Nelson, 1998, Brain substrates of infant-mother attachment: contributions of opioids, oxytocin, and norepinephrine, Neurosci. Biobehav. Rev., 22, 437, 10.1016/S0149-7634(97)00052-3 Niesink, 1989, Involvement of opioid and dopaminergic systems in isolation-induced pinning and social grooming of young rats, Neuropharmacology, 28, 411, 10.1016/0028-3908(89)90038-5 Noguchi, 2012, nparLD: an R software package for the nonparametric analysis of longitudinal data in factorial experiments, J. Stat. Softw., 50, 1, 10.18637/jss.v050.i12 Nylander, 2012, Neuropeptides as mediators of the early-life impact on the brain; implications for alcohol use disorders, Front. Mol. Neurosci., 5, 77, 10.3389/fnmol.2012.00077 Nylander, 2013, Is the rodent maternal separation model a valid and effective model for studies on the early-life impact on ethanol consumption?, Psychopharmacology, 229, 555, 10.1007/s00213-013-3217-3 Oreland, 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, 10.1016/j.npep.2010.06.001 Palm, 2011, 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, 10.1016/j.applanim.2011.08.010 Palm, 2011, Differences in voluntary ethanol consumption in Wistar rats from five different suppliers, Alcohol Fayettev. N, 45, 607, 10.1016/j.alcohol.2010.11.005 Palm, 2012, Differences in basal and ethanol-induced levels of opioid peptides in Wistar rats from five different suppliers, Peptides, 36, 1, 10.1016/j.peptides.2012.04.016 Panksepp, 1984, The psychobiology of play: theoretical and methodological perspectives, Neurosci. Biobehav. Rev., 8, 465, 10.1016/0149-7634(84)90005-8 Parent, 2008, The influence of natural variations in maternal care on play fighting in the rat, Dev. Psychobiol., 50, 767, 10.1002/dev.20342 Patchev, 1999, Ontogeny of gender-specific responsiveness to stress and glucocorticoids in the rat and its determination by the neonatal gonadal steroid environment, Stress Amst. Neth., 3, 41, 10.3109/10253899909001111 Pellis, 1997, Multiple differences in the play fighting of male and female rats, Implications for the causes and functions of play. Neurosci. Biobehav. Rev., 21, 105, 10.1016/0149-7634(95)00060-7 Ploj, 2002, Effects of maternal separation on brain nociceptin/orphanin FQ peptide levels in male Wistar rats, Pharmacol. Biochem. Behav., 73, 123, 10.1016/S0091-3057(02)00778-5 Plotsky, 1993, Early, postnatal experience alters hypothalamic corticotropin-releasing factor (CRF) mRNA, median eminence CRF content and stress-induced release in adult rats, Brain Res. Mol. Brain Res., 18, 195, 10.1016/0169-328X(93)90189-V Pryce, 2003, Long-term neurobehavioural impact of the postnatal environment in rats: manipulations, effects and mediating mechanisms, Neurosci. Biobehav. Rev., 27, 57, 10.1016/S0149-7634(03)00009-5 Pryce, 2001, Comparison of the effects of infant handling, isolation, and nonhandling on acoustic startle, prepulse inhibition, locomotion, and HPA activity in the adult rat, Behav. Neurosci., 115, 71, 10.1037/0735-7044.115.1.71 Pryce, 2001, Comparison of the effects of early handling and early deprivation on maternal care in the rat, Dev. Psychobiol., 38, 239, 10.1002/dev.1018 Pryce, 2002, Early life stress: long-term physiological impact in rodents and primates, News Physiol. Sci. Int. J. Physiol. Prod. Jointly Int. Union Physiol. Sci. Am. Physiol. Soc., 17, 150 R Core Team, 2014 Roman, 2005, The impact of emotional stress early in life on adult voluntary ethanol intake-results of maternal separation in rats, Stress Amst. Neth., 8, 157, 10.1080/10253890500188666 Roman, 2004, Maternal separation has no effect on voluntary ethanol intake in female Wistar rats, Alcohol Fayettev. N, 33, 31, 10.1016/S0741-8329(04)00077-1 Roman, 2005, Short and prolonged periods of maternal separation and voluntary ethanol intake in male and female ethanol-preferring AA and ethanol-avoiding ANA rats, Alcohol. Clin. Exp. Res., 29, 591, 10.1097/01.ALC.0000158933.70242.FC Roman, 2006, Behavioral profiles and stress-induced corticosteroid secretion in male Wistar rats subjected to short and prolonged periods of maternal separation, Horm. Behav., 50, 736, 10.1016/j.yhbeh.2006.06.016 Teicher, 2003, The neurobiological consequences of early stress and childhood maltreatment, Neurosci. Biobehav. Rev., 27, 33, 10.1016/S0149-7634(03)00007-1 Teicher, 2006, Neurobiological consequences of early stress and childhood maltreatment: are results from human and animal studies comparable?, Ann. N. Y. Acad. Sci., 1071, 313, 10.1196/annals.1364.024 Trezza, 2010, The pleasures of play: pharmacological insights into social reward mechanisms, Trends Pharmacol. Sci., 31, 463, 10.1016/j.tips.2010.06.008 Tsigos, 2002, Hypothalamic-pituitary-adrenal axis, neuroendocrine factors and stress, J. Psychosom. Res., 53, 865, 10.1016/S0022-3999(02)00429-4 van Hasselt, 2012, Within-litter variation in maternal care received by individual pups correlates with adolescent social play behavior in male rats, Physiol. Behav., 106, 701, 10.1016/j.physbeh.2011.12.007 Vanderschuren, 1995, Influence of environmental factors on social play behavior of juvenile rats, Physiol. Behav., 58, 119, 10.1016/0031-9384(94)00385-I Veenema, 2009, Maternal separation enhances offensive play-fighting, basal corticosterone and hypothalamic vasopressin mRNA expression in juvenile male rats, Psychoneuroendocrinology, 34, 463, 10.1016/j.psyneuen.2008.10.017 Weininger, 1954, Physiological damage under emotional stress as a function of early experience, Science, 119, 285, 10.1126/science.119.3087.285 Wood, 2016, Prevalence and influence of cys407* Grm2 mutation in Hannover-derived Wistar rats: mGlu2 receptor loss links to alcohol intake, risk taking and emotional behaviour, Neuropharmacology