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Early Life Stress and Their Effects: Maternal Separation

Yıl 2016, Cilt: 5 Sayı: 2, 454 - 466, 01.06.2016

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Negative experiences in early life periods are associated with an increase in incidences of psychopathological conditions including depression and anxiety. It has been reported that prenatal or early postnatal stressful environments impair the development and cause life-long health problems, and they particularly result in increased susceptibility to mental disorders. Chronic effects of the different manipulations on postnatal relationships between mother and pups have experimentally been studied for over 50 years in rats. As early life stress model; maternal separation ​​ MS and maternal deprivation MD has mainly been studied in mice and rats. MS and MD are defined as the separation of newborns from mothers for 3 h/day between postnatal 2nd and 14th days and 24 h in the postnatal 9th day, respectively. Using MS and MD experimental models in mice and rats, the effects of neonatal stress on behavioral and endocrine responses, etc. have been investigated in adults used as particularly to investigate. Rodents are dependent on their mothers during early postnatal 3 weeks, and particularly the first 2 week is critical for the development of the brain in rats. While the development of the brain reaches to its peak in the 9th month of pregnancy in man, this occurs during the postnatal 2nd week in rats. MS occurring in early life period can lead to consistent morphologic changes in the brain. Studies reveal that MS can cause lifelong hyperactivity in the hypothalamic–pituitary–adrenal HPA axis and long term MS induces permanent changes in serotonergic, noradrenergic, dopaminergic, GABAergic, glutamatergic systems and endocannabinoids systems and in amounts of BDNF. Conclusion: In present review, MS and MD have been discussed as early life stress experiences regarding their effects on neuronal, immune, endocrine, reproductive, and gastrointestinal systems and microbiota, metabolism, energy homeokinesis, metabolic syndrome, and body weight.

Kaynakça

  • Aisa B et al. (2009). Neonatal stress affects vulnerability of cholinergic neurons and cognition in the rat: involvement of the HPA axis. Psychoneuroendocrinology, 34, 1495–1505.
  • Aisa B, Tordera R, Lasheras B, Del Río J, Ramírez MJ (2007). Cognitive impairment associated to HPA axis hyperactivity after maternal separation in rats. Psychoneuroendocrinology, 32(3), 256-266.
  • Andersen SL, Tomada A, Vincow ES, Valente E, Polcari A, Teicher MH (2008). Preliminary evidence for sensitive periods in the effect of childhood sexual abuseon regional brain development. J. Neuropsychiatry Clin. Neurosci, 20: 292–301.
  • Arborelius L, Eklund MB (2007). Both long and brief maternal separation produces persistent changes in tissue levels of brain monoamines in middle-aged female rats. Neuroscience, 145, 738–750.
  • Arborelius L, Hawks BW, Owens MJ, Plotsky PM, Nemeroff CB (2004). Increased responsiveness of presumed 5-HT cells to citalopram in adult rats subjected to prolonged maternal separation relative to brief separation. Psychopharmacology, 176, 248–255.
  • Arias C, Solari AC, Mlewski EC, Miller S, Haymal B, Spear NE, Molina JC (2010). Social isolation and stress related hormones modulate the stimulating effect of ethanol in preweanling rats. Behav Brain Res, 211, 64–70..
  • Bailey MT, Coe CL (1999). Maternal separation disrupts the integrity of the intestinal microflora in infant rhesus monkeys. Dev Psychobiol, 35, 146–155.
  • Bale TL, Baram TZ, Brown AS, Goldstein JM, Insel TR, McCarthy MM, Nemeroff CB, Reyes TM, Simerly RB, Susser ES, Nestler EJ (2010). Early life programming and neurodevelopmental disorders. Biol. Psychiatry, 68, 314–319.
  • Barna I, Balint E, Baranyi J, Bakos N, Makara GB, Haller J (2003). Gender- specific effect of maternal deprivation on anxiety and corticotropin- releasing hormone mRNA expression in rats. Brain Res Bull, 62, 85–91.
  • Baroncelli L, Braschi C, Spolidoro M, Begenisic T, Sale a Maffei L (2010). Nurturing brain plasticity: impact of environmental enrichment. Cell Death and Differentiation, 17,1092–103.
  • Barreau F, Cartier C, Ferrier L, Fioramonti J, Bueno L (2004a). Nerve growth factor mediates alterations of colonic sensitivity and mucosal barrier induced by neonatal stress in rats. Gastroenterology, 127, 524–534.
  • Barreau F, Ferrier L, Fioramonti J, Bueno L (2004b). Neonatal maternal deprivation triggers long term alterations in colonic epithelial barrier and mucosal immunity in rats. Gut, 53, 501–506.
  • Barreau F, Salvador-Cartier C, Houdeau E, Bueno L, Fioramonti J (2008). Long-term alterations of colonic nerve–mast cell interactions induced by neonatal maternal deprivation in rats. Gut, 57, 582–590.
  • Bethea CL, Lu NZ, Gundlah C, Streicher JM (2002). Diverse actions of ovarian steroids in the serotonin neural system. Front. Neuroendocrinol, 23, 41—100.
  • adaptation to disease. Nat Rev Neurosci., 6, 463–475.
  • De la Fuente M, Llorente R, Baeza I, De Castro NM, Arranz L, Cruces J, Viveros MP (2009). Early maternal deprivation in rats: a proposed animal model for thestudy of developmental neuroimmunoendocrine interactions. Ann. N. Y. Acad.Sci., 1153, 176–183.
  • Desbonnet L, Garrett L, Daly E, McDermott KW, Dinan TG (2008). Sexually dimorphic effects of maternal separation stress on corticotrophin-releasing factor and vasopressin systems in the adult rat brain. Int J Dev Neurosci., 26, 259–268.
  • Desbonnet, L et al (2010). Effects of the probiotic Bifidobacterium infantis in the maternal separation model of depression. Neuroscience, 170, 1179–1188.
  • Dimatelis JJ, Stein DJ, Russell VA (2012). Behavioural changes after maternal separation are reversed by chronic constant light treatment. Brain Res., 1480, 61–71.
  • do Prado CH, Narahari T, Holland FH, Lee HN, Murthy SK, Brenhouse HC (2015). Effects of early adolescent environmental enrichment on cognitive dysfunction, prefrontal cortex development, and inflammatory cytokines after early life stress. Dev Psychobiol., 21.
  • Dong M, Giles WH, Felitti VJ, Dube SR, Williams JE, Chapman DP, Anda RF (2004). Insights into causal pathways for ischemic heart disease: adverse childhood experiences study. Circulation., 28, 110(13), 1761-1766.
  • Doupe AJ, Landis SC, Patterson PH (1985). Environmental influences in the development of neural crest derivatives: glucocorticoids, growth factors, and chromaffin cell plasticity. J. Neurosci., 5, 2119– 2142.
  • Duman RS, Monteggia LM (2006). A neurotrophic model for stress- related mood disorders. Biol Psychiatry, 59, 1116–27.
  • Eiland L, McEwen BS (2012). Early life stress followed by subsequent adult chronic stress potentiates anxiety and blunts hippocampal structural remodeling. Hippocampus. 22(1):82-91
  • Eklund MB, Johansson LM, Uvnäs-Moberg K, Arborelius L (2009). Differential effects of repeated long and brief maternal separation on behaviour and neuroendocrine parameters in Wistar dams. Behav Brain Res., 12, 203(1), 69-75.
  • Ellenbroek BA, Derks N, Park HJ (2005). Early maternal deprivation retards neurodevelopment in Wistar rats. Stress, 8, 247–257.
  • Eutamene H, Bueno L (2007). Role of probiotics in correcting abnormalities of colonic flora induced by stress. Gut, 56, 1495– 1497.
  • Fontella FU, Vendite DA, Tabajara AS, Porciuncula LO, da Silva Torres IL, Jardim FM, Martini L, Souza DO, Netto CA, Dalmaz C (2004). Repeated restraint stress alters hippocampal glutamate uptake and release in the rat. Neurochem. Res., 29, 1703–1709.
  • Francis DD, Champagne FC, Meaney MJ (2000). Variations inmaternal behavior are associated with differences in oxytocinreceptor levels in the rat. J. Neuroendocrinol., 12, 1145—1148.
  • Fuente-Martin E., Granado M, Garcia-Caceres C, Sanchez-Garrido MA, Frago LM, Tena-Sempere M, Argente J, Chowen JA (2012). Early nutritional changesinduce sexually dimorphic long-term effects on body weight gain and theresponse to sucrose intake in adult rats. Metabolism, 61, 812–822.
  • Garcia-Rodenas CL, Bergonzelli GE, Nutten S, Schumann A, Cherbut C, et al (2006). Nutritional approach to restore impaired intestinal barrier function and growth after neonatal stress in rats. J Pediatr Gastroenterol Nutr., 43, 16–24.
  • Gardner KL, Thrivikraman KV, Lightman SL, Plotsky PM, Lowry CA (2005). Early life experience alters behavior during social defeat: focus on serotonergic systems. Neuroscience, 136(1), 181-91.
  • Gareau MG, Jury J, MacQueen G, Sherman PM, Perdue MH (2007b). Probiotic treatment of rat pups normalises corticosterone release and ameliorates colonic dysfunction induced by maternal separation. Gut, 56, 1522–1528.
  • Gareau MG, Jury J, Perdue MH (2007a). Neonatal maternal separation of rat pups results in abnormal cholinergic regulation of epithelial permeability. Am. J. Physiol. Gastrointest. Liver Physiol., 293, 198– 203.
  • Gareau MG, Jury J, Yang PC, MacQueen G, Perdue MH (2006). Neonatal maternal separation causes colonic dysfunction in rat pups including impaired host resistance. Pediatr Res., 59, 83–88.
  • Gareau MG, Silva MA, Perdue MH (2008). Pathophysiological mechanisms of stress-induced intestinal damage. Curr. Mol. Med., 8, 274–281.
  • Gartside SE, Johnson DA, Leitch MM, Troakes C, Ingram CD (2003). Early life adversity programs changes in central 5-HT neuronal functioning in adulthood. Eur J Neurosci., 17, 2401–2408.
  • Geeraerts B, Van Oudenhove L, Fischler B, Vandenberghe J, Caenepeel P, Janssens J, Tack J (2009). Influence of abuse history on gastric sensorimotor function in functional dyspepsia, Neurogastroenterol. Motil., 21, 33–41.
  • Giachino C, Canalia N, Capone F, Fasolo A, Alleva E, Riva M, Peretto P (2007). Maternal deprivation and early handling affect density of calcium binding proteincontaining neurons in selected brain regions and emotional behavior in periadolescent rats. Neuroscience., 145(2), 568-578.
  • Gibney SM, Gosselin RD, Dinan TG, Cryan JF (2010). Colorectal distensioninduced prefrontal cortex activation in the Wistar-Kyoto rat: implications for irritable bowel syndrome. Neuroscience, 165, 675 683.
  • Giedd JN, Lalonde FM, Celano MJ, White SL, Wallace GL, Lee NR, Lenroot RK (2009). Anatomical brain magnetic resonance imaging of typically developing children and adolescents. J. Am. Acad. Child Adolesc. Psychiatry.,48, 465–470.
  • Girardi CEN, Zanta NC, Suchecki D (2014). Neonatal stress-induced affective changes in adolescent wistar rats: Early signs of schizophrenia-like behavior. Frontiers in Behavioral Neuroscience.; 8.
  • Greco B, Lubbers LS, Blaustein JD (2003). Estrogen receptorbeta messenger ribonucleic acid expression in the forebrain ofproestrous, pregnant, and lactating female rats. Endocrinology, 144, 1869—1875.
  • Gubernick DJ, Alberts JR (1983). Maternal licking of young: resource exchange and proximate controls. Physiol Behav. 31, 593–601.
  • Herkenham M, Lynn AB, Little MD, Johnson MR, Melvin, LS, de Costa BR, Rice KC (1990). Cannabinoid receptor localization in brain. Proceedings of the National Academy of Sciences of the United States of America, 87(5), 1932-1936.
  • Hofer MA (1976). The organization of sleep and wakefulness after maternal separation in young rats. Dev Psychobiol., 9(2),189-205.
  • Hofer MA (1994). Early relationships as regulators of infant physiology and behavior. Acta Paediatr Suppl., 397, 9-18.
  • Holmes A, Le Guisquet AM, Vogel E, Millstein RA, Leman S, Belzung C (2005). Early life genetic, epigenetic and environmental factors shaping emotionality in rodents. Neurosci. Biobehav. Rev., 29, 1335–1346.
  • Hulshof HJ, Novati A, Sgoifo A, Luiten PG, den Boer JA, Meerlo P (2011). Maternal separation decreases adult hippocampal cell proliferation and impairs cognitive performance but has little effect on stress sensitivity and anxiety in adult Wistar rats. Behavioural Brain Research, 216, 552–560.
  • Huot RL, Plotsky PM, Lenox RH, McNamara RK (2002). Neonatal maternal separation reduces hippocampal mossy fiber density in adult Long Evans rats. Brain Research, 950, 52–63.
  • Huot RL, Thrivikraman KV, Meaney MJ, Plotsky PM (2001). Development of adult ethanol preference and anxiety as a consequence of neonatal maternal separation in Long Evans rats and reversal with antidepressant treatment. Psychopharmacology, 158, 366–373.
  • Hyland NP et al (2009). A distinct subset of submucosal mast cells undergoes hyperplasia following neonatal maternal separation: a role in visceral hypersensitivity? Gut, 58, 1029–1030.
  • Jakubowski M, Terkel J (1985). Transition from pup killing toparental behavior in male and virgin female albino rats. Physiol. Behav., 34, 683—686.
  • Kalinichev M, Easterling KW, Holtzman SG (2000). Periodic postpartum separation from the offspring results in long-lasting changes in anxiety-related behaviors and sensitivity to morphine in Long-Evans mother rats. Psychopharmacology, 152(17), 431–439.
  • Kalinichev M, Easterling KW, Holtzman SG (2001). Repeated neonatal maternal separation alters morphine induced antinociception in male rats. Brain Res. Bull., 54, 649–654.
  • McLaughlin RJ, Gobbi G (2012). Cannabinoids and emotionality: a neuroanatomical perspective. Neuroscience, 204, 134–144.
  • Meaney M J (2001). Maternal care, gene expression, and the transmission of individual differences in stress reactivity across generations. Annu. Rev. Neurosci., 24, 1161–1192.
  • Mechoulam R, Parker LA. (2013) The endocannabinoid system and the brain. Annu. Rev. Psychol., 64, 21–47.
  • Mela V, Llorente-Berzal A, Diaz F, Argente J, Viveros MP, Chowen JA (2012). Maternal deprivation exacerbates the response to a high fat diet in a sexually dimorphic manner. PLoS ONE, 7, e48915.
  • Mendez-Dıaz M, Rueda-Orozco PE, Ruiz-Contreras AE, Prospero-Garcia O (2012). The endocannabinoid system modulates the valence of the emotion associated to food ingestion. Addict Biol. 17, 725–735.
  • Meyer JS, Fairman KR (1985). Early adrenalectomy increases myelin content of the rat brain. Brain Res. 349, 1–9.
  • Mistry AM, Swick A, Romsos DR (1999). Leptin alters metabolic rates before acqui-sition of its anorectic effect in developing neonatal mice. Am. J. Physiol., 277, R742–R747.
  • Miyazaki T, Takase K, Nakajima W, Tada H, Ohya D, Sano A, et al (2012). Disrupted cortical function underlies behavior dysfunction due to social isolation. J. Clin.Invest., 122, 2690–2701.
  • Moffett MC, Vicentic A, Kozel M, Plotsky P, Francis DD, Kuhar MJ (2007). Maternal separation alters drug intake patterns in adulthood in rats. Biochem Pharmacol. 1, 73(3), 321-30.
  • Moghaddam B (1993). Stress preferentially increases extraneuronal levels of excitatory amino acids in the prefrontal cortex: comparison to hippocampus and basal ganglia. J. Neurochem., 60, 1650–1657.
  • Mogi K, Nagasawa M (2011). Developmental consequences and biological significance of mother-infant bonding. Progress in Neuro- Psychopharmacology & Biological Psychiatry, 35, 1232–1241.
  • Moloney RD et al (2012). Early-life stress induces visceral hypersensitivity in mice. Neurosci. Lett., 512, 99–102.
  • Monroy E, Hernández-Torres E, Flores G (2010). Maternal separation disrupts dendritic morphology of neurons in prefrontal cortex, hippocampus, and nucleus accumbens in male rat offspring. J. Chem.Neuroanat., 126, 497–505.
  • Morgane PJ, Mokler DJ, Galler JR (2002). Effects of prenatal protein malnutrition on the hippocampal formation. Neurosci. Biobehav. Rev., 26, 471–483.
  • Nam H, Clinton SM, Jackson NL, Kerman IA (2014). Learned helplessness and social avoidance in the Wistar-Kyoto rat. Front. Behav. Neurosci., 8, 109.
  • Neumann ID (2002). Involvement of the brain oxytocin system in stress coping: interactions with the hypothalamo–pituitary–adrenal axis. Prog Brain Res., 139, 147–62.
  • Noh SJ, Ryu V, Yoo SB, Lee JH, Min BM, Jahng JW (2008). Suppressed intake of highly palatable food and dysfunctiona lof HPA axis response to restraint stress in adolescent rats that experienced neonatal maternal separation. Appetite,51, 388.
  • Nylander I, Roman E (2012). Neuropeptides as mediators of the early- life impacton the brain; implications for alcohol use disorders. Front Mol Neurosci., 5, 77.
  • O’Mahony SM, Marchesi JR, Scully P, Codling C, Ceolho AM, Quigley EM, Cryan JF, Dinan TG (2009). Early life stress alters behavior, immunity, and microbiota in rats: implications for irritable bowel syndrome and psychiatric illnesses. Biol. Psychiatry, 65, 263–267.
  • O’Malley D, Julio-Pieper M, Gibney SM, Dinan TG, Cryan JF (2010). Distinct alterations in colonic morphology and physiology in two rat models of enhanced stress-induced anxiety- and depression-like behavior. Stress, 13, 114–122.
  • Okabe S, Nagasawa M, Mogi K (2012). The importance of mother- infant communication for social bond formation in mammals. Animal Science Journal, 83, 446–452.
  • O’Mahony SM, Hyland NP, Dinan TG, Cryan JF (2011). Maternal separation as a model of brain-gut axis dysfunction. Psychopharmacology (Berl), 214(1), 71-88.
  • Oreland S, Pickering C, Gokturk C, Oreland L, Arborelius L, Nylander I (2009). Two repeated maternal separation procedures differentially affect brain 5-hydroxytryptamine transporter and receptors in young and adult male and female rats. Brain Res. 1305(Suppl), S37– S49.
  • Oshima T, Fukui H, Watari J, Miwa H (2015). Childhood abuse history is associated with the development of dyspepsia: a population-based survey in Japan, J. Gastroenterol., 70, 744–750.
  • Ovtscharoff Jr W, Braun K (2001). Maternal separation and social isolation modulate the postnatal development of synaptic composition in the infralimbic cortex of Octodon degus. Neuroscience, 104, 33–40.
  • Panagiotaropoulos T, Pondiki S, Papaioannou A, Alikaridis F, Stamatakis A, Gerozissis K, Stylianopoulou F (2004). Neonatal handling and gender modulate brain monoamines and plasma corticosterone levels following repeated stressors in adulthood. Neuroendocrinology, 80, 181–191.
  • Patel S, Roelke CT, Rademacher DJ, Cullinan WE, Hillard CJ (2004). Endocannabinoid signaling negatively modulates stress- induced activation of the hypothalamic-pituitary-adrenal axis. Endocrinology, 145, 5431–5438.
  • Penasco S, Mela V, Lopez-Moreno JA, Viveros MP, Marco EM (2015). Early maternal deprivation enhances voluntary alcohol intake induced by exposure to stressful events later in life. Neural Plast, 342761.
  • Petrosini L, De Bartolo P, Foti F, Gelfo F, Cutuli D, Leggio MG, et al (2009). On whether the environmental enrichment may provide cognitive and brain reserves. Brain Research Reviews, 61, 221–39.
  • Pickering C, Gustafsson L, Cebere A, Nylander I, Liljequist S (2006). Repeated maternal separation of male Wistar rats alters glutamate receptor expression in the hippocampus but not the prefrontal cortex. Brain Res. 12, 1099(1):101-8.
  • Pierce AN, Ryals JM, Wang R, Christianson JA (2014). Vaginal hypersensitivity dysfunction as a result of neonatal maternal separation in female mice Neuroscience, 263, 216–230. axis
  • Pinheiro RM, de Lima MN, Portal BC, Busato SB, Falavigna L, Ferreira RD, Paz AC, de Aguiar BW, Kapczinski F, Schröder (2015). Long- lasting recognition memory impairment and alterations in brain levels of cytokines and BDNF induced by maternal deprivation: effects of valproic acid and topiramate. J Neural Transm (Vienna), 122(5), 709-719.
  • Pirker S, Schwarzer C, Wieselthaler A, Sieghart W, Sperk G (2000). GABAA receptors: Immunocytochemical distribution of 13 subunits in the adult rat brain. Neuroscience, 101(4), 815-850.
  • Plotsky PM, Meaney MJ (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, 195–200.
  • Plotsky PM, Thrivikraman KV, Nemeroff CB, Caldji C, Sharma S, Meaney MJ (2005). Long-term consequences of neonatal rearing on central corticotropin-releasing factor systems in adult male rat offspring. Neuropsychopharmacology, 30, 2192–2204.
  • Pollak SD, Nelson CA, Schlaak MF, Roeber BJ, Wewerka SS, Wiik KL, Frenn KA, Loman MM, Gunnar MR (2010). Neurodevelopmental effects of early deprivation in postinstitutionalized children. Child Dev., 81, 224–236.
  • Pryce CR, Feldon J (2003). Long-term neurobehavioural impact of the postnatal environment in rats: manipulations, effects and mediating mechanisms. Neurosci Biobehav Rev. 27, 57–71.
  • Pryce CR, Ruedi-Bettschen D, Dettling AC, Weston A, Russig H, Ferger BFeldon J (2005). Long-term effects of early-life environmental manipulations in rodents and primates: Potential animal models in depression research Neurosci Biobehav Rev., 29, 649–674.
  • Pusceddu MM, El Aidy S, Crispie F, O’Sullivan O, Cotter P, Stanton C, Kelly P, Cryan JF, Dinan TG (2015). N-3 Polyunsaturated Fatty Acids (PUFAs) Reverse the Impact of Early-Life Stress on the Gut Microbiota. PLoS One, 10(10), e0139721.
  • Sung Y-H, Shin M-S, Cho S, Baik H-H, Jin B-K, Chang H-K, et al (2010). Depression-like state in maternal rats induced by repeated separation of pups is accompanied by a decrease of cell proliferation and an increase of apoptosis in the hippocampus. Neuroscience Letters., 470, 86–90.
  • Takatsuru Y, Ishikawa T, Kohsaka S, Nabekura J, Koibuchi N (2015). Early- life stress increases the motility of microglia in adulthood. J. Physiol. Sci., 65, 187–194.
  • Tanapat P, Hastings NB, Rydel TA, Galea LA, Gould E (2001). Exposure to fox odor inhibits cell proliferation in the hippocampus of adult rats via an adrenal hormone-dependent mechanism. J Comp Neurol., 437, 496-504.
  • Tottenham N, Hare TA, Quinn BT, McCarry TW, Nurse M, Gilhooly T, Millner A, Galvan A, Davidson MC, Eigsti IM, Thomas KM, Freed PJ, Booma ES, Gunnar MR, Altemus M, Aronson, J, Casey BJ (2010). Prolonged institutional rearing is associated with atypically large amygdala volume and difficulties in emotion regulation. Dev. Sci., 13, 46–61.
  • Tractenberg SG, Levandowski ML, de Azeredo LA, Orso R, Roithmann LG, Hoffmann ES, Brenhouse H, Grassi-Oliveira R. An overview of maternal separation effects on behavioural outcomes in mice: Evidence from a four-stage methodological systematic review. Neurosci Biobehav Rev. 2016 Sep;68:489-503.
  • Treit D, Fundytus M (1988). Thigmotaxis as a test for anxiolytic activity in rats. Pharmacol Biochem Behav., 31, 959–62.
  • Valerio A, Ghisi V, Dossena M, Tonello C, Giordano A, Frontini A, Ferrario M, Pizzi M, Spano P, Carruba MO, Nisoli E (2006). Leptin increasesaxonal growth cone size in developing mouse cortical neurons by conver-gent signals inactivating glycogen synthase kinase-3beta. J. Biol. Chem., 281, 12950–12958.
  • van Harmelen, A.L., van Tol, M.J., van derWee, N.J., Veltman, D.J., Aleman, A., Spinhoven
  • P., van Buchem MA, Zitman FG, Penninx BW, Van Oudenhove L, Vandenberghe J, Dupont P, Geeraerts B, Vos R, Dirix S, Van Laere K, Bormans G, Vanderghinste D, Demyttenaere K, Fischler B, Tack J (2010). Regional brain activity in functional dyspepsia: a H (2) (15) O-PET study on the role of gastric sensitivity and abuse history, Gastroenterology, 139, 36–47.
  • Van Oudenhove L, Vandenberghe J, Vos R, Fischler B, Demyttenaere K, Tack J (2011). Abuse history, depression, and somatization are associated with gastric sensitivity and gastric emptying in functional dyspepsia Psychosom. Med., 73, 648–655.
  • van Praag HM (2004). Can stress cause depression? Prog Neuropsychopharmacol Biol Psychiatry., 28, 891-907.
  • Van Zyl PJ, Dimatelis JJ, Russell VA (2014). Changes in behaviour and ultrasonic vocalizations during antidepressant treatment in the maternally separated Wistar-Kyoto rat model of depression. Metab Brain Dis. 29, 495–507.
  • Varghese, A. K. et al (2006). Antidepressants attenuate increased susceptibility to colitis in a murine model of depression. Gastroenterology, 130, 1743–1753.
  • Vazquez DM, Lopez JF, Van Hoers H, Watson SJ, Levine S (2000). Maternal deprivation regulates serotonin 1A and 2A receptors in the infant rat. Brain Res., 855, 76–82.
  • Veenema AH (2009). Early life stress, the development of aggression and neuroendocrine and neurobiological correlates: What can we learn from animal models? Frontiers in Neuroendocrinology, 30(4), 497-518.
  • Veenema AH, Blume A, Niederle D, Buwalda B, Neumann ID (2006). Effects of early life stress on adult male aggression and hypothalamic vasopressin and serotonin. European Journal of Neuroscience, 24(6), 1711-1720.
  • Viveros MP, Diaz F, Mateos B, Rodriguez N, Chowen JA (2010a). Maternal deprivation induces a rapid decline in circulating leptin levels and sexually dimorphicmodifications in hypothalamic trophic factors and cell turnover. Horm. Behav., 57, 405–414.
  • Viveros MP, Llorente R, Diaz F, Romero-Zerbo SY, Bermudez-Silva FJ, Rodriguez de Fonseca F, Argente J, Chowen JA (2010b). Maternal deprivationhas sexually dimorphic long term effects on hypothalamic cell-turnover, bodyweight and circulating hormone levels. Horm. Behav., 58, 808–819.
  • Viveros MP, Llorente R, López-Gallardo M, Suarez J, Bermşdez-Silva F, De la Fuente M, Rodriguez F, de Fonseca RF, Garcia-Segura LM (2009). Sex-dependent alterations in response to maternal deprivation in rats. Psychoneuroendocrinology, 34, 217–26.
  • Viviani B, Boraso M, Valero M, Gardoni F, Marco EM, Llorente R, Corsini E, Galli CL, Di Luca M, Marinovich M, Lopez-Gallardo M, Viveros MP (2013). Early maternal deprivation immunologically primes hippocampal synapses byredistributing interleukin-1 receptor type I in a sex dependent manner. BrainBehav. Immun., 35, 135–143.
  • Wagner CK, Morrell JI (1996). Levels of estrogen receptorimmunoreactivity are altered in behaviorally-relevant brain regions in female rats during pregnancy. Brain Res. Mol. BrainRes., 42, 328—336.
  • Walker CD, Scribner KA, Cascio CS, Dallman MF (1991). The pituitary- adrenocortical system of neonatal rats is responsive to stress throughout development in a time-dependent and stressor-specific fashion. Endocrinology, 128, 1385–1395.
  • Weber BC, Manfredo HN, Rinaman L (2009). A potential gastrointestinal link between enhanced postnatal maternal care and reduced anxiety-like behavior in adolescent rats. Behav. Neurosci. 123, 1178–1184.
  • Wigger A, Neumann ID (1999). Periodic maternal deprivation induces gender-dependent alterations in behavioral and neuroendocrine responses to emotional stress in adult rats. Physiol. Behav. 66, 293–302.
  • Wotjak CT (2005). Role of endogenous cannabinoids in cognition and emotionality. Mini Rev. Med. Chem., 5, 659–670.
  • Wöhr M, van Gaalen MM, Schwarting RK (2015). Affective communication in rodents: serotonin and its modulating role in ultrasonic vocalizations. Behav. Pharmacol, 26, 506–521.
  • Yang PC, Jury J, Soderholm JD, Sherman PM, McKay DM, Perdue MH (2006). Chronic psychological stress in rats induces intestinal sensitization to luminal antigens. Am J Pathol., 168, 104–114.
  • Yoshihara T, Otsuki Y, Yamazaki A, Honma S, Yamasaki Y, Honma K (2005). Maternal deprivation in neonatal rats alters the expression of circadian system under light-dark cycles and restricted daily feeding in adulthood. Physiol. Behav., 85(5), 646-654.
  • Zamberletti E, Prini P, Speziali S, Gabaglio M, Solinas M, Parolaro D, Rubino T (2012). Gender-dependent behavioral and biochemical effects of adolescentdelta-9-tetrahydrocannabinol in adult maternally deprived rats. Neuroscience, 204, 245–257.
  • Zhang J, Qin L, Zhao H. Early repeated maternal separation induces alterations of hippocampus reelin expression in rats. J Biosci. 2013 Mar;38(1):27-33.

Erken Yaşam Stresi ve Etkileri: Maternal Separasyon

Yıl 2016, Cilt: 5 Sayı: 2, 454 - 466, 01.06.2016

Öz

Özbilgi/Amaç: Yaşamın erken dönemlerindeki kötü deneyimler sonraki yaşam süreçlerinde depresyonu ve anksiyeteyi de içeren psikopatolojik durumların insidansını artırmaktadır. İnsanlarda prenatal veya erken postnatal stresli bir çevrenin gelişmeyi olumsuz etkilediği ve yaşam boyu sağlık problemlerine neden olduğu, özellikle de mental hastalıklara yatkınlığı artırdığı rapor edilmiştir. Sıçanlarda anne-yavru ilişkisine postnatal manipülasyonların kronik etkisi 50 yılı aşkın süredir deneysel olarak çalışılmaktadır. Erken yaşam stresi modeli olarak fare ve sıçanlarda maternal separasyon MS ve maternal deprivasyon MD protokolleri yaygın şekilde kullanılmaktadır. MS postnatal 2-14. günler arasında günde 3 saatlik anneden ayırma, MD ise postnatal 9. günde 24 saatlik anneden ayırma periyodu olarak tanımlanmaktadır. Fare ve sıçanda MS ve MD deney modelleri kullanılarak insanlarda neonatal stresin yetişkin dönemdeki etkileri davranış, endokrin cevap, vb. incelenmektedir. Rodentler postnatal ilk 3 haftalık dönemde annelerine bağımlıdır ve özellikle ilk 2 hafta sıçan beyninin gelişmesinde kritik öneme sahiptir. Beyin gelişimi insanlarda gebeliğin 9. ayında pik yaparken, sıçanlarda postnatal 2. haftada gerçekleşmektedir. Erken dönemde yaşanan bir MS beyinde kalıcı morfolojik değişiklikler oluşturabilir. Çalışmalar MS’in yaşam boyu hipotalamo-hipofizer-adrenal HPA eksenin hiperaktivitesine neden olabildiğini ve uzun süreli MS’in beyin bölgelerinin serotonerjik, noradrenerjik, dopaminerjik, GABAerjik, glutamaterjik ve endokannoboid sistemler ile BDNF miktarlarında kalıcı değişikliklere neden olduğunu ortaya koymaktadır. Sonuç: Bu derlemede bir erken yaşam stresi modeli olarak MS ve MD; nöral, immun, endokrin, üreme, gastro-intestinal sistem, intestinal mikrobiyota, enerji döngüsü, metabolik süreçler, metabolik sendrom ve vücut ağırlığı üzerine etkileri yönünden değerlendirilmektedir.

Kaynakça

  • Aisa B et al. (2009). Neonatal stress affects vulnerability of cholinergic neurons and cognition in the rat: involvement of the HPA axis. Psychoneuroendocrinology, 34, 1495–1505.
  • Aisa B, Tordera R, Lasheras B, Del Río J, Ramírez MJ (2007). Cognitive impairment associated to HPA axis hyperactivity after maternal separation in rats. Psychoneuroendocrinology, 32(3), 256-266.
  • Andersen SL, Tomada A, Vincow ES, Valente E, Polcari A, Teicher MH (2008). Preliminary evidence for sensitive periods in the effect of childhood sexual abuseon regional brain development. J. Neuropsychiatry Clin. Neurosci, 20: 292–301.
  • Arborelius L, Eklund MB (2007). Both long and brief maternal separation produces persistent changes in tissue levels of brain monoamines in middle-aged female rats. Neuroscience, 145, 738–750.
  • Arborelius L, Hawks BW, Owens MJ, Plotsky PM, Nemeroff CB (2004). Increased responsiveness of presumed 5-HT cells to citalopram in adult rats subjected to prolonged maternal separation relative to brief separation. Psychopharmacology, 176, 248–255.
  • Arias C, Solari AC, Mlewski EC, Miller S, Haymal B, Spear NE, Molina JC (2010). Social isolation and stress related hormones modulate the stimulating effect of ethanol in preweanling rats. Behav Brain Res, 211, 64–70..
  • Bailey MT, Coe CL (1999). Maternal separation disrupts the integrity of the intestinal microflora in infant rhesus monkeys. Dev Psychobiol, 35, 146–155.
  • Bale TL, Baram TZ, Brown AS, Goldstein JM, Insel TR, McCarthy MM, Nemeroff CB, Reyes TM, Simerly RB, Susser ES, Nestler EJ (2010). Early life programming and neurodevelopmental disorders. Biol. Psychiatry, 68, 314–319.
  • Barna I, Balint E, Baranyi J, Bakos N, Makara GB, Haller J (2003). Gender- specific effect of maternal deprivation on anxiety and corticotropin- releasing hormone mRNA expression in rats. Brain Res Bull, 62, 85–91.
  • Baroncelli L, Braschi C, Spolidoro M, Begenisic T, Sale a Maffei L (2010). Nurturing brain plasticity: impact of environmental enrichment. Cell Death and Differentiation, 17,1092–103.
  • Barreau F, Cartier C, Ferrier L, Fioramonti J, Bueno L (2004a). Nerve growth factor mediates alterations of colonic sensitivity and mucosal barrier induced by neonatal stress in rats. Gastroenterology, 127, 524–534.
  • Barreau F, Ferrier L, Fioramonti J, Bueno L (2004b). Neonatal maternal deprivation triggers long term alterations in colonic epithelial barrier and mucosal immunity in rats. Gut, 53, 501–506.
  • Barreau F, Salvador-Cartier C, Houdeau E, Bueno L, Fioramonti J (2008). Long-term alterations of colonic nerve–mast cell interactions induced by neonatal maternal deprivation in rats. Gut, 57, 582–590.
  • Bethea CL, Lu NZ, Gundlah C, Streicher JM (2002). Diverse actions of ovarian steroids in the serotonin neural system. Front. Neuroendocrinol, 23, 41—100.
  • adaptation to disease. Nat Rev Neurosci., 6, 463–475.
  • De la Fuente M, Llorente R, Baeza I, De Castro NM, Arranz L, Cruces J, Viveros MP (2009). Early maternal deprivation in rats: a proposed animal model for thestudy of developmental neuroimmunoendocrine interactions. Ann. N. Y. Acad.Sci., 1153, 176–183.
  • Desbonnet L, Garrett L, Daly E, McDermott KW, Dinan TG (2008). Sexually dimorphic effects of maternal separation stress on corticotrophin-releasing factor and vasopressin systems in the adult rat brain. Int J Dev Neurosci., 26, 259–268.
  • Desbonnet, L et al (2010). Effects of the probiotic Bifidobacterium infantis in the maternal separation model of depression. Neuroscience, 170, 1179–1188.
  • Dimatelis JJ, Stein DJ, Russell VA (2012). Behavioural changes after maternal separation are reversed by chronic constant light treatment. Brain Res., 1480, 61–71.
  • do Prado CH, Narahari T, Holland FH, Lee HN, Murthy SK, Brenhouse HC (2015). Effects of early adolescent environmental enrichment on cognitive dysfunction, prefrontal cortex development, and inflammatory cytokines after early life stress. Dev Psychobiol., 21.
  • Dong M, Giles WH, Felitti VJ, Dube SR, Williams JE, Chapman DP, Anda RF (2004). Insights into causal pathways for ischemic heart disease: adverse childhood experiences study. Circulation., 28, 110(13), 1761-1766.
  • Doupe AJ, Landis SC, Patterson PH (1985). Environmental influences in the development of neural crest derivatives: glucocorticoids, growth factors, and chromaffin cell plasticity. J. Neurosci., 5, 2119– 2142.
  • Duman RS, Monteggia LM (2006). A neurotrophic model for stress- related mood disorders. Biol Psychiatry, 59, 1116–27.
  • Eiland L, McEwen BS (2012). Early life stress followed by subsequent adult chronic stress potentiates anxiety and blunts hippocampal structural remodeling. Hippocampus. 22(1):82-91
  • Eklund MB, Johansson LM, Uvnäs-Moberg K, Arborelius L (2009). Differential effects of repeated long and brief maternal separation on behaviour and neuroendocrine parameters in Wistar dams. Behav Brain Res., 12, 203(1), 69-75.
  • Ellenbroek BA, Derks N, Park HJ (2005). Early maternal deprivation retards neurodevelopment in Wistar rats. Stress, 8, 247–257.
  • Eutamene H, Bueno L (2007). Role of probiotics in correcting abnormalities of colonic flora induced by stress. Gut, 56, 1495– 1497.
  • Fontella FU, Vendite DA, Tabajara AS, Porciuncula LO, da Silva Torres IL, Jardim FM, Martini L, Souza DO, Netto CA, Dalmaz C (2004). Repeated restraint stress alters hippocampal glutamate uptake and release in the rat. Neurochem. Res., 29, 1703–1709.
  • Francis DD, Champagne FC, Meaney MJ (2000). Variations inmaternal behavior are associated with differences in oxytocinreceptor levels in the rat. J. Neuroendocrinol., 12, 1145—1148.
  • Fuente-Martin E., Granado M, Garcia-Caceres C, Sanchez-Garrido MA, Frago LM, Tena-Sempere M, Argente J, Chowen JA (2012). Early nutritional changesinduce sexually dimorphic long-term effects on body weight gain and theresponse to sucrose intake in adult rats. Metabolism, 61, 812–822.
  • Garcia-Rodenas CL, Bergonzelli GE, Nutten S, Schumann A, Cherbut C, et al (2006). Nutritional approach to restore impaired intestinal barrier function and growth after neonatal stress in rats. J Pediatr Gastroenterol Nutr., 43, 16–24.
  • Gardner KL, Thrivikraman KV, Lightman SL, Plotsky PM, Lowry CA (2005). Early life experience alters behavior during social defeat: focus on serotonergic systems. Neuroscience, 136(1), 181-91.
  • Gareau MG, Jury J, MacQueen G, Sherman PM, Perdue MH (2007b). Probiotic treatment of rat pups normalises corticosterone release and ameliorates colonic dysfunction induced by maternal separation. Gut, 56, 1522–1528.
  • Gareau MG, Jury J, Perdue MH (2007a). Neonatal maternal separation of rat pups results in abnormal cholinergic regulation of epithelial permeability. Am. J. Physiol. Gastrointest. Liver Physiol., 293, 198– 203.
  • Gareau MG, Jury J, Yang PC, MacQueen G, Perdue MH (2006). Neonatal maternal separation causes colonic dysfunction in rat pups including impaired host resistance. Pediatr Res., 59, 83–88.
  • Gareau MG, Silva MA, Perdue MH (2008). Pathophysiological mechanisms of stress-induced intestinal damage. Curr. Mol. Med., 8, 274–281.
  • Gartside SE, Johnson DA, Leitch MM, Troakes C, Ingram CD (2003). Early life adversity programs changes in central 5-HT neuronal functioning in adulthood. Eur J Neurosci., 17, 2401–2408.
  • Geeraerts B, Van Oudenhove L, Fischler B, Vandenberghe J, Caenepeel P, Janssens J, Tack J (2009). Influence of abuse history on gastric sensorimotor function in functional dyspepsia, Neurogastroenterol. Motil., 21, 33–41.
  • Giachino C, Canalia N, Capone F, Fasolo A, Alleva E, Riva M, Peretto P (2007). Maternal deprivation and early handling affect density of calcium binding proteincontaining neurons in selected brain regions and emotional behavior in periadolescent rats. Neuroscience., 145(2), 568-578.
  • Gibney SM, Gosselin RD, Dinan TG, Cryan JF (2010). Colorectal distensioninduced prefrontal cortex activation in the Wistar-Kyoto rat: implications for irritable bowel syndrome. Neuroscience, 165, 675 683.
  • Giedd JN, Lalonde FM, Celano MJ, White SL, Wallace GL, Lee NR, Lenroot RK (2009). Anatomical brain magnetic resonance imaging of typically developing children and adolescents. J. Am. Acad. Child Adolesc. Psychiatry.,48, 465–470.
  • Girardi CEN, Zanta NC, Suchecki D (2014). Neonatal stress-induced affective changes in adolescent wistar rats: Early signs of schizophrenia-like behavior. Frontiers in Behavioral Neuroscience.; 8.
  • Greco B, Lubbers LS, Blaustein JD (2003). Estrogen receptorbeta messenger ribonucleic acid expression in the forebrain ofproestrous, pregnant, and lactating female rats. Endocrinology, 144, 1869—1875.
  • Gubernick DJ, Alberts JR (1983). Maternal licking of young: resource exchange and proximate controls. Physiol Behav. 31, 593–601.
  • Herkenham M, Lynn AB, Little MD, Johnson MR, Melvin, LS, de Costa BR, Rice KC (1990). Cannabinoid receptor localization in brain. Proceedings of the National Academy of Sciences of the United States of America, 87(5), 1932-1936.
  • Hofer MA (1976). The organization of sleep and wakefulness after maternal separation in young rats. Dev Psychobiol., 9(2),189-205.
  • Hofer MA (1994). Early relationships as regulators of infant physiology and behavior. Acta Paediatr Suppl., 397, 9-18.
  • Holmes A, Le Guisquet AM, Vogel E, Millstein RA, Leman S, Belzung C (2005). Early life genetic, epigenetic and environmental factors shaping emotionality in rodents. Neurosci. Biobehav. Rev., 29, 1335–1346.
  • Hulshof HJ, Novati A, Sgoifo A, Luiten PG, den Boer JA, Meerlo P (2011). Maternal separation decreases adult hippocampal cell proliferation and impairs cognitive performance but has little effect on stress sensitivity and anxiety in adult Wistar rats. Behavioural Brain Research, 216, 552–560.
  • Huot RL, Plotsky PM, Lenox RH, McNamara RK (2002). Neonatal maternal separation reduces hippocampal mossy fiber density in adult Long Evans rats. Brain Research, 950, 52–63.
  • Huot RL, Thrivikraman KV, Meaney MJ, Plotsky PM (2001). Development of adult ethanol preference and anxiety as a consequence of neonatal maternal separation in Long Evans rats and reversal with antidepressant treatment. Psychopharmacology, 158, 366–373.
  • Hyland NP et al (2009). A distinct subset of submucosal mast cells undergoes hyperplasia following neonatal maternal separation: a role in visceral hypersensitivity? Gut, 58, 1029–1030.
  • Jakubowski M, Terkel J (1985). Transition from pup killing toparental behavior in male and virgin female albino rats. Physiol. Behav., 34, 683—686.
  • Kalinichev M, Easterling KW, Holtzman SG (2000). Periodic postpartum separation from the offspring results in long-lasting changes in anxiety-related behaviors and sensitivity to morphine in Long-Evans mother rats. Psychopharmacology, 152(17), 431–439.
  • Kalinichev M, Easterling KW, Holtzman SG (2001). Repeated neonatal maternal separation alters morphine induced antinociception in male rats. Brain Res. Bull., 54, 649–654.
  • McLaughlin RJ, Gobbi G (2012). Cannabinoids and emotionality: a neuroanatomical perspective. Neuroscience, 204, 134–144.
  • Meaney M J (2001). Maternal care, gene expression, and the transmission of individual differences in stress reactivity across generations. Annu. Rev. Neurosci., 24, 1161–1192.
  • Mechoulam R, Parker LA. (2013) The endocannabinoid system and the brain. Annu. Rev. Psychol., 64, 21–47.
  • Mela V, Llorente-Berzal A, Diaz F, Argente J, Viveros MP, Chowen JA (2012). Maternal deprivation exacerbates the response to a high fat diet in a sexually dimorphic manner. PLoS ONE, 7, e48915.
  • Mendez-Dıaz M, Rueda-Orozco PE, Ruiz-Contreras AE, Prospero-Garcia O (2012). The endocannabinoid system modulates the valence of the emotion associated to food ingestion. Addict Biol. 17, 725–735.
  • Meyer JS, Fairman KR (1985). Early adrenalectomy increases myelin content of the rat brain. Brain Res. 349, 1–9.
  • Mistry AM, Swick A, Romsos DR (1999). Leptin alters metabolic rates before acqui-sition of its anorectic effect in developing neonatal mice. Am. J. Physiol., 277, R742–R747.
  • Miyazaki T, Takase K, Nakajima W, Tada H, Ohya D, Sano A, et al (2012). Disrupted cortical function underlies behavior dysfunction due to social isolation. J. Clin.Invest., 122, 2690–2701.
  • Moffett MC, Vicentic A, Kozel M, Plotsky P, Francis DD, Kuhar MJ (2007). Maternal separation alters drug intake patterns in adulthood in rats. Biochem Pharmacol. 1, 73(3), 321-30.
  • Moghaddam B (1993). Stress preferentially increases extraneuronal levels of excitatory amino acids in the prefrontal cortex: comparison to hippocampus and basal ganglia. J. Neurochem., 60, 1650–1657.
  • Mogi K, Nagasawa M (2011). Developmental consequences and biological significance of mother-infant bonding. Progress in Neuro- Psychopharmacology & Biological Psychiatry, 35, 1232–1241.
  • Moloney RD et al (2012). Early-life stress induces visceral hypersensitivity in mice. Neurosci. Lett., 512, 99–102.
  • Monroy E, Hernández-Torres E, Flores G (2010). Maternal separation disrupts dendritic morphology of neurons in prefrontal cortex, hippocampus, and nucleus accumbens in male rat offspring. J. Chem.Neuroanat., 126, 497–505.
  • Morgane PJ, Mokler DJ, Galler JR (2002). Effects of prenatal protein malnutrition on the hippocampal formation. Neurosci. Biobehav. Rev., 26, 471–483.
  • Nam H, Clinton SM, Jackson NL, Kerman IA (2014). Learned helplessness and social avoidance in the Wistar-Kyoto rat. Front. Behav. Neurosci., 8, 109.
  • Neumann ID (2002). Involvement of the brain oxytocin system in stress coping: interactions with the hypothalamo–pituitary–adrenal axis. Prog Brain Res., 139, 147–62.
  • Noh SJ, Ryu V, Yoo SB, Lee JH, Min BM, Jahng JW (2008). Suppressed intake of highly palatable food and dysfunctiona lof HPA axis response to restraint stress in adolescent rats that experienced neonatal maternal separation. Appetite,51, 388.
  • Nylander I, Roman E (2012). Neuropeptides as mediators of the early- life impacton the brain; implications for alcohol use disorders. Front Mol Neurosci., 5, 77.
  • O’Mahony SM, Marchesi JR, Scully P, Codling C, Ceolho AM, Quigley EM, Cryan JF, Dinan TG (2009). Early life stress alters behavior, immunity, and microbiota in rats: implications for irritable bowel syndrome and psychiatric illnesses. Biol. Psychiatry, 65, 263–267.
  • O’Malley D, Julio-Pieper M, Gibney SM, Dinan TG, Cryan JF (2010). Distinct alterations in colonic morphology and physiology in two rat models of enhanced stress-induced anxiety- and depression-like behavior. Stress, 13, 114–122.
  • Okabe S, Nagasawa M, Mogi K (2012). The importance of mother- infant communication for social bond formation in mammals. Animal Science Journal, 83, 446–452.
  • O’Mahony SM, Hyland NP, Dinan TG, Cryan JF (2011). Maternal separation as a model of brain-gut axis dysfunction. Psychopharmacology (Berl), 214(1), 71-88.
  • Oreland S, Pickering C, Gokturk C, Oreland L, Arborelius L, Nylander I (2009). Two repeated maternal separation procedures differentially affect brain 5-hydroxytryptamine transporter and receptors in young and adult male and female rats. Brain Res. 1305(Suppl), S37– S49.
  • Oshima T, Fukui H, Watari J, Miwa H (2015). Childhood abuse history is associated with the development of dyspepsia: a population-based survey in Japan, J. Gastroenterol., 70, 744–750.
  • Ovtscharoff Jr W, Braun K (2001). Maternal separation and social isolation modulate the postnatal development of synaptic composition in the infralimbic cortex of Octodon degus. Neuroscience, 104, 33–40.
  • Panagiotaropoulos T, Pondiki S, Papaioannou A, Alikaridis F, Stamatakis A, Gerozissis K, Stylianopoulou F (2004). Neonatal handling and gender modulate brain monoamines and plasma corticosterone levels following repeated stressors in adulthood. Neuroendocrinology, 80, 181–191.
  • Patel S, Roelke CT, Rademacher DJ, Cullinan WE, Hillard CJ (2004). Endocannabinoid signaling negatively modulates stress- induced activation of the hypothalamic-pituitary-adrenal axis. Endocrinology, 145, 5431–5438.
  • Penasco S, Mela V, Lopez-Moreno JA, Viveros MP, Marco EM (2015). Early maternal deprivation enhances voluntary alcohol intake induced by exposure to stressful events later in life. Neural Plast, 342761.
  • Petrosini L, De Bartolo P, Foti F, Gelfo F, Cutuli D, Leggio MG, et al (2009). On whether the environmental enrichment may provide cognitive and brain reserves. Brain Research Reviews, 61, 221–39.
  • Pickering C, Gustafsson L, Cebere A, Nylander I, Liljequist S (2006). Repeated maternal separation of male Wistar rats alters glutamate receptor expression in the hippocampus but not the prefrontal cortex. Brain Res. 12, 1099(1):101-8.
  • Pierce AN, Ryals JM, Wang R, Christianson JA (2014). Vaginal hypersensitivity dysfunction as a result of neonatal maternal separation in female mice Neuroscience, 263, 216–230. axis
  • Pinheiro RM, de Lima MN, Portal BC, Busato SB, Falavigna L, Ferreira RD, Paz AC, de Aguiar BW, Kapczinski F, Schröder (2015). Long- lasting recognition memory impairment and alterations in brain levels of cytokines and BDNF induced by maternal deprivation: effects of valproic acid and topiramate. J Neural Transm (Vienna), 122(5), 709-719.
  • Pirker S, Schwarzer C, Wieselthaler A, Sieghart W, Sperk G (2000). GABAA receptors: Immunocytochemical distribution of 13 subunits in the adult rat brain. Neuroscience, 101(4), 815-850.
  • Plotsky PM, Meaney MJ (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, 195–200.
  • Plotsky PM, Thrivikraman KV, Nemeroff CB, Caldji C, Sharma S, Meaney MJ (2005). Long-term consequences of neonatal rearing on central corticotropin-releasing factor systems in adult male rat offspring. Neuropsychopharmacology, 30, 2192–2204.
  • Pollak SD, Nelson CA, Schlaak MF, Roeber BJ, Wewerka SS, Wiik KL, Frenn KA, Loman MM, Gunnar MR (2010). Neurodevelopmental effects of early deprivation in postinstitutionalized children. Child Dev., 81, 224–236.
  • Pryce CR, Feldon J (2003). Long-term neurobehavioural impact of the postnatal environment in rats: manipulations, effects and mediating mechanisms. Neurosci Biobehav Rev. 27, 57–71.
  • Pryce CR, Ruedi-Bettschen D, Dettling AC, Weston A, Russig H, Ferger BFeldon J (2005). Long-term effects of early-life environmental manipulations in rodents and primates: Potential animal models in depression research Neurosci Biobehav Rev., 29, 649–674.
  • Pusceddu MM, El Aidy S, Crispie F, O’Sullivan O, Cotter P, Stanton C, Kelly P, Cryan JF, Dinan TG (2015). N-3 Polyunsaturated Fatty Acids (PUFAs) Reverse the Impact of Early-Life Stress on the Gut Microbiota. PLoS One, 10(10), e0139721.
  • Sung Y-H, Shin M-S, Cho S, Baik H-H, Jin B-K, Chang H-K, et al (2010). Depression-like state in maternal rats induced by repeated separation of pups is accompanied by a decrease of cell proliferation and an increase of apoptosis in the hippocampus. Neuroscience Letters., 470, 86–90.
  • Takatsuru Y, Ishikawa T, Kohsaka S, Nabekura J, Koibuchi N (2015). Early- life stress increases the motility of microglia in adulthood. J. Physiol. Sci., 65, 187–194.
  • Tanapat P, Hastings NB, Rydel TA, Galea LA, Gould E (2001). Exposure to fox odor inhibits cell proliferation in the hippocampus of adult rats via an adrenal hormone-dependent mechanism. J Comp Neurol., 437, 496-504.
  • Tottenham N, Hare TA, Quinn BT, McCarry TW, Nurse M, Gilhooly T, Millner A, Galvan A, Davidson MC, Eigsti IM, Thomas KM, Freed PJ, Booma ES, Gunnar MR, Altemus M, Aronson, J, Casey BJ (2010). Prolonged institutional rearing is associated with atypically large amygdala volume and difficulties in emotion regulation. Dev. Sci., 13, 46–61.
  • Tractenberg SG, Levandowski ML, de Azeredo LA, Orso R, Roithmann LG, Hoffmann ES, Brenhouse H, Grassi-Oliveira R. An overview of maternal separation effects on behavioural outcomes in mice: Evidence from a four-stage methodological systematic review. Neurosci Biobehav Rev. 2016 Sep;68:489-503.
  • Treit D, Fundytus M (1988). Thigmotaxis as a test for anxiolytic activity in rats. Pharmacol Biochem Behav., 31, 959–62.
  • Valerio A, Ghisi V, Dossena M, Tonello C, Giordano A, Frontini A, Ferrario M, Pizzi M, Spano P, Carruba MO, Nisoli E (2006). Leptin increasesaxonal growth cone size in developing mouse cortical neurons by conver-gent signals inactivating glycogen synthase kinase-3beta. J. Biol. Chem., 281, 12950–12958.
  • van Harmelen, A.L., van Tol, M.J., van derWee, N.J., Veltman, D.J., Aleman, A., Spinhoven
  • P., van Buchem MA, Zitman FG, Penninx BW, Van Oudenhove L, Vandenberghe J, Dupont P, Geeraerts B, Vos R, Dirix S, Van Laere K, Bormans G, Vanderghinste D, Demyttenaere K, Fischler B, Tack J (2010). Regional brain activity in functional dyspepsia: a H (2) (15) O-PET study on the role of gastric sensitivity and abuse history, Gastroenterology, 139, 36–47.
  • Van Oudenhove L, Vandenberghe J, Vos R, Fischler B, Demyttenaere K, Tack J (2011). Abuse history, depression, and somatization are associated with gastric sensitivity and gastric emptying in functional dyspepsia Psychosom. Med., 73, 648–655.
  • van Praag HM (2004). Can stress cause depression? Prog Neuropsychopharmacol Biol Psychiatry., 28, 891-907.
  • Van Zyl PJ, Dimatelis JJ, Russell VA (2014). Changes in behaviour and ultrasonic vocalizations during antidepressant treatment in the maternally separated Wistar-Kyoto rat model of depression. Metab Brain Dis. 29, 495–507.
  • Varghese, A. K. et al (2006). Antidepressants attenuate increased susceptibility to colitis in a murine model of depression. Gastroenterology, 130, 1743–1753.
  • Vazquez DM, Lopez JF, Van Hoers H, Watson SJ, Levine S (2000). Maternal deprivation regulates serotonin 1A and 2A receptors in the infant rat. Brain Res., 855, 76–82.
  • Veenema AH (2009). Early life stress, the development of aggression and neuroendocrine and neurobiological correlates: What can we learn from animal models? Frontiers in Neuroendocrinology, 30(4), 497-518.
  • Veenema AH, Blume A, Niederle D, Buwalda B, Neumann ID (2006). Effects of early life stress on adult male aggression and hypothalamic vasopressin and serotonin. European Journal of Neuroscience, 24(6), 1711-1720.
  • Viveros MP, Diaz F, Mateos B, Rodriguez N, Chowen JA (2010a). Maternal deprivation induces a rapid decline in circulating leptin levels and sexually dimorphicmodifications in hypothalamic trophic factors and cell turnover. Horm. Behav., 57, 405–414.
  • Viveros MP, Llorente R, Diaz F, Romero-Zerbo SY, Bermudez-Silva FJ, Rodriguez de Fonseca F, Argente J, Chowen JA (2010b). Maternal deprivationhas sexually dimorphic long term effects on hypothalamic cell-turnover, bodyweight and circulating hormone levels. Horm. Behav., 58, 808–819.
  • Viveros MP, Llorente R, López-Gallardo M, Suarez J, Bermşdez-Silva F, De la Fuente M, Rodriguez F, de Fonseca RF, Garcia-Segura LM (2009). Sex-dependent alterations in response to maternal deprivation in rats. Psychoneuroendocrinology, 34, 217–26.
  • Viviani B, Boraso M, Valero M, Gardoni F, Marco EM, Llorente R, Corsini E, Galli CL, Di Luca M, Marinovich M, Lopez-Gallardo M, Viveros MP (2013). Early maternal deprivation immunologically primes hippocampal synapses byredistributing interleukin-1 receptor type I in a sex dependent manner. BrainBehav. Immun., 35, 135–143.
  • Wagner CK, Morrell JI (1996). Levels of estrogen receptorimmunoreactivity are altered in behaviorally-relevant brain regions in female rats during pregnancy. Brain Res. Mol. BrainRes., 42, 328—336.
  • Walker CD, Scribner KA, Cascio CS, Dallman MF (1991). The pituitary- adrenocortical system of neonatal rats is responsive to stress throughout development in a time-dependent and stressor-specific fashion. Endocrinology, 128, 1385–1395.
  • Weber BC, Manfredo HN, Rinaman L (2009). A potential gastrointestinal link between enhanced postnatal maternal care and reduced anxiety-like behavior in adolescent rats. Behav. Neurosci. 123, 1178–1184.
  • Wigger A, Neumann ID (1999). Periodic maternal deprivation induces gender-dependent alterations in behavioral and neuroendocrine responses to emotional stress in adult rats. Physiol. Behav. 66, 293–302.
  • Wotjak CT (2005). Role of endogenous cannabinoids in cognition and emotionality. Mini Rev. Med. Chem., 5, 659–670.
  • Wöhr M, van Gaalen MM, Schwarting RK (2015). Affective communication in rodents: serotonin and its modulating role in ultrasonic vocalizations. Behav. Pharmacol, 26, 506–521.
  • Yang PC, Jury J, Soderholm JD, Sherman PM, McKay DM, Perdue MH (2006). Chronic psychological stress in rats induces intestinal sensitization to luminal antigens. Am J Pathol., 168, 104–114.
  • Yoshihara T, Otsuki Y, Yamazaki A, Honma S, Yamasaki Y, Honma K (2005). Maternal deprivation in neonatal rats alters the expression of circadian system under light-dark cycles and restricted daily feeding in adulthood. Physiol. Behav., 85(5), 646-654.
  • Zamberletti E, Prini P, Speziali S, Gabaglio M, Solinas M, Parolaro D, Rubino T (2012). Gender-dependent behavioral and biochemical effects of adolescentdelta-9-tetrahydrocannabinol in adult maternally deprived rats. Neuroscience, 204, 245–257.
  • Zhang J, Qin L, Zhao H. Early repeated maternal separation induces alterations of hippocampus reelin expression in rats. J Biosci. 2013 Mar;38(1):27-33.
Toplam 124 adet kaynakça vardır.

Ayrıntılar

Birincil Dil Türkçe
Bölüm Research Article
Yazarlar

Mehmet Ekici

Muharrem Balkaya Bu kişi benim

Yayımlanma Tarihi 1 Haziran 2016
Yayımlandığı Sayı Yıl 2016 Cilt: 5 Sayı: 2

Kaynak Göster

APA Ekici, M., & Balkaya, M. (2016). Erken Yaşam Stresi ve Etkileri: Maternal Separasyon. Animal Health Production and Hygiene, 5(2), 454-466.