Maternal separation as a model of early stress : effects on aspects of emotional behavior and neuroendocrine function

Part of : Hellenic journal of psychology ; Vol.9, No.1, 2012, pages 84-101

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Pages:
84-101
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Abstract:
A growing body of findings underlines the critical role of the early environment in normal growth and development. Human studies suggest that severe stress during childhood increases vulnerability to development of affective psychopathology in adulthood. Neonatal maternal separation in rodents (rats or mice) is an established model of early stress for studying the neuroendocrine and behavioral effects of early adversity. The article reviews the existing evidence regarding the effects of this postnatal manipulation on the neuroendocrine response to stress and on emotion-relevant behaviors, and attempts to explain the existing inconsistencies seen in the results. Although the prevailing idea is that maternal separation augments emotionality and potentiates the endocrine response to stress, methodological differences among studies prevent us from making definite conclusions. Further studies in which parameters related to neuroendocrine function, behavior, and neuronal plasticity will be concurrently examined are warranted. In addition, the need to investigate whether early stress may increase vulnerability to subsequent challenges during the postnatal period is discussed.
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Keywords:
early stress, maternal separation, neuroendocrine function
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  1. Aisa, B., Elizalde, N., Tordera, R., Lasheras, B., Del Río, J., & Ramírez, M. J. (2009). Effectsof neonatal stress on markers of synaptic plasticity in the hippocampus: Implications forspatial memory. Hippocampus,19(12), 1222-1231.Aisa, B., Tordera, R., Lasheras, B., Del Río, J., & Ramírez, M. J. (2007). Cognitive impairmentassociated to HPA axis hyperactivity after maternal separation in rats.Psychoneuroendocrinology, 32(3), 256-266.Andersen, S. L., & Teicher, M. H. (2004). Delayed effects of early stress on hippocampaldevelopment. Neuropsychopharmacology, 29(11),1988-1993.Arborelius, L., & Eklund, M. B. (2007). Both long and brief maternal separation producespersistent changes in tissue levels of brain monoamines in middle-aged female rats.Neuroscience, 145(2), 738-750.Barna, I., Bálint, E., Baranyi, J., Bakos, N., Makara, G. B., & Haller, J. (2003). Gender-specificeffect of maternal deprivation on anxiety and corticotropin-releasing hormonemRNA expression in rats. Brain Research Bulletin, 62(2), 85-91.Biagini, G., Pich, E. M., Carani, C., Marrama, P., & Agnati, L. F. (1998). Postnatal maternal separation during the stress hyporesponsive period enhances the adrenocortical responseto novelty in adult rats by affecting feedback regulation in the CA1 hippocampal field.International Journal of Developmental Neuroscience, 16(3-4), 187-197.Bohn, M. C. (1980). Granule cell genesis in the hippocampus of rats treated neonatally withhydrocortisone. Neuroscience, 5(11), 2003-2012.Brent, D., Melhem, N., Donohoe, M. B., & Walker, M. (2009). The incidence and course ofdepression in bereaved youth 21 months after the loss of a parent to suicide, accident, orsudden natural death. The American Journal of Psychiatry,166(7), 786-794.Breslau, N., & Anthony, J. C. (2007). Gender differences in the sensitivity to posttraumaticstress disorder: An epidemiological study of urban young adults. Journal of AbnormalPsychology, 116(3), 607-611.Cannon, D. M., Ichise, M., Rollis, D., Klaver, J. M., Gandhi, S. K., Charney, D. S., Manji, H.K., & Drevets, W. C. (2007). Elevated serotonin transporter binding in major depressivedisorder assessed using positron emission tomography and [11C]DASB: Comparisonwith bipolar disorder. Biological Psychiatry, 62(8), 870-877.Champagne, F. A., Francis, D. D., Mar, A., & Meaney, M. J. (2003). Variations in maternalcare in the rat as a mediating influence for the effects of environment on development.Physiology and Behavior, 79(3), 359-371.Colorado, R. A., Shumake, J., Conejo, N. M., Gonzalez-Pardo, H., & Gonzalez-Lima, F.(2006). Effects of maternal separation, early handling, and standard facility rearing onorienting and impulsive behavior of adolescent rats. Behavioral Processes,71(1), 51-58.Conrad, C. D. (2008). Chronic stress-induced hippocampal vulnerability: The glucocorticoidvulnerability hypothesis. Reviews in the neurosciences, 19(6), 395-411.Daniels, W. M, Fairbairn, L. R, van Tilburg, G., McEvoy, C. R., Zigmond, M. J, Russell V.A., & Stein, D. J. (2009). Maternal separation alters nerve growth factor and corticosteronelevels but not the DNA methylation status of the exon 1(7) glucocorticoid receptorpromoter region. Metabolic Brain Disease, 24(4), 615-627.De Kloet, E. R., Vreugdenhil, E., Oitzl, M. S., & Joëls, M. (1998). Brain corticosteroid receptorbalance in health and disease. Endocrine Reviews, 19(3), 269-301.Desbonnet, L., Garrett, L., Daly, E., McDermott, K. W., & Dinan, T. G. (2008). Sexuallydimorphic effects of maternal separation stress on corticotrophin-releasing factor andvasopressin systems in the adult rat brain. International Journal of DevelopmentalNeuroscience, 26(3-4), 259-268.Eiland, L., & McEwen, B. S. (2010). Early life stress followed by subsequent adult chronicstress potentiates anxiety and blunts hippocampal structural remodeling. Hippocampus,n/a. doi: 10.1002/hipo.20862.Ehlert, U., Gaab, J., & Heinrichs, M. (2001). Psychoneuroendocrinological contributions tothe etiology of depression, posttraumatic stress disorder, and stress-related bodily disorders:The role of the hypothalamus-pituitary-adrenal axis. Biological Psychology, 57(1-3),141-152.Evans, D. L., & Nemeroff, C. B. (1983). The dexamethasone suppression test in mixed bipolardisorder. The American Journal of Psychiatry, 140(5), 615-617.Farkas, J., Reglodi, D., Gaszner, B., Szogyi, D., Horvath, G., Lubics, A., Tamas, A., Frank,F., Besirevic, D., & Kiss, P. (2009). Effects of maternal separation on the neurobehavioraldevelopment of newborn Wistar rats. Brain Research Bulletin, 79, 208-214.Faure, J., Uys, J. D., Marais, L., Stein, D. J., & Daniels, W. M. (2007). Early maternal separationalters the response to traumatization: Resulting in increased levels of hippocampalneurotrophic factors. Metabolic Brain Disease, 22(2), 183-195.Faturi, C. B, Tiba, P. A., Kawakami, S. E, Catallani, B., Kerstens, M., & Suchecki, D. (2010).Disruptions of the mother-infant relationship and stress-related behaviors: Altered corticosteronesecretion does not explain everything. Neuroscience and BiobehavioralReviews, 34(6), 821-834.Felitti, V. J., Anda, R. F., Nordenberg, D., Williamson, D. F., Spitz, A. M., Edwards, V.,Koss, M. P., & Marks, J. S. (1998). Relationship of childhood abuse and household dysfunctionto many of the leading causes of death in adults: The Adverse ChildhoodExperiences (ACE) Study. American Journal of Preventive Medicine, 14(4), 245-258.Francis, D. D., Diorio, J., Plotsky, P. M., & Meaney, M. J. (2002). Environmental enrichmentreverses the effects of maternal separation on stress reactivity. Journal of Neuroscience,22(18), 7840-7843.Gibb, B. E., Chelminski, I., & Zimmerman, M. (2007). Childhood emotional, physical, andsexual abuse, and diagnoses of depressive and anxiety disorders in adult psychiatric outpatients.Depression and Anxiety, 24(4), 256-263.Gould, E., Woolley, C. S., & McEwen, B. S. (1991). Adrenal steroids regulate postnataldevelopment of the rat dentate gyrus: I. Effects of glucocorticoids on cell death. Journalof Comparative Neurology, 313(3), 479-485.Grace, L., Hescham, S., Kellaway, L. A., Bugarith, K., & Russell, V. A. (2009). Effect of exerciseon learning and memory in a rat model of developmental stress. Metabolic BrainDisease, 24(4), 643-657.Heim, C., & Nemeroff, C. B. (1999). The impact of early adverse experiences on brain systemsinvolved in the pathophysiology of anxiety and affective disorders. BiologicalPsychiatry, 46, 1509–1522.Heim, C., Shugart, M., Craighead, W. E, & Nemeroff, C. B. (2010). Neurobiological and psychiatric consequences of child abuse and neglect. Developmental Psychobiology, 52(7), 671-690.Herman, J. P., & Cullinan, W. E. (1997). Neurocircuitry of stress: Central control of thehypothalamo-pituitary-adrenocortical axis. Trends in Neurosciences, 20(2), 78-84.Hulshof, H. J., Novati, A., Sgoifo, A., Luiten, P. G, den Boer, J. A., & Meerlo, P. (2011).Maternal separation decreases adult hippocampal cell proliferation and impairs cognitiveperformance but has little effect on stress sensitivity and anxiety in adult Wistar rats.Behavioural Brain Research, 216(2), 552-560.Huot, R. L., Plotsky, P. M., Lenox, R. H., & McNamara, R. K. (2002). Neonatal maternalseparation reduces hippocampal mossy fiber density in adult Long Evans rats. BrainResearch, 950(1-2), 52-63.Huot, R. L., Thrivikraman, K. V., Meaney, M. J., & Plotsky, P. M. (2001). Development ofadult ethanol preference and anxiety as a consequence of neonatal maternal separation in Long Evans rats and reversal with antidepressant treatment. Psychopharmacology(Berl), 158(4), 366-373.Jones, N. C., Kumar, G., O’Brien, T. J., Morris, M. J., Rees, S. M., & Salzberg, M. R. (2009).Anxiolytic effects of rapid amygdala kindling, and the influence of early life experiencein rats. Behavioral Brain Research, 203(1), 81-87.Kallinichev, M., Easterling, K. W., Plotsky, P. M., & Holtzman, S. G. (2002). Long-lastingchanges in stress-induced corticosterone response and anxiety-like behaviors as a consequenceof neonatal maternal separation in Long Evans rats. Pharmacology, Biochemistryand Behavior, 73(1), 131-140.Kent, J. M., Coplan, J. D., & Gorman, J. M. (1998). Clinical utility of the selective serotoninreuptake inhibitors in the spectrum of anxiety. Biological Psychiatry, 44(9), 812-824.Knuth, E. D, & Etgen, A. M. (2005). Corticosterone secretion induced by chronic isolationin neonatal rats is sexually dimorphic and accompanied by elevated ACTH. Hormonesand Behavior, 47(1), 65-75.Knuth, E. D., & Etgen, A. M. (2007). Long-term behavioral consequences of brief, repeatedneonatal isolation. Brain Research, 1128(1), 139-147.Kosten, T. A., Karanian, D. A., Yeh, J., Haile, C. N, Kim J. J, Kehoe, P., & Bahr, B. A.(2007). Memory impairments and hippocampal modifications in adult rats with neonatalisolation stress experience. Neurobiology of Learning and Memory, 88(2), 167-176.Kudielka, B. M., & Kirschbaum, C. (2005). Sex differences in HPA axis responses to stress:A review. Biological Psychology, 69(1), 113-132.Ladd, C. O., Huot, R. L., Thrivikraman, K. V., Nemeroff, C. B., & Plotsky, P. M. (2004).Long-term adaptations in glucocorticoid receptor and mineralocorticoid receptormRNA and negative feedback on the hypothalamo-pituitary-adrenal axis followingneonatal maternal separation. Biological Psychiatry, 55(4), 367-375.Lambás-Señas, L., Mnie-Filali, O., Certin, V., Faure, C., Lemoine, L., Zimmer, L., & Haddjeri,N. (2009). Functional correlates for 5-HT(1A) receptors in maternally deprived rats displayinganxiety and depression-like behaviors. Progress in Neuropsychopharmacology andBiological Psychiatry, 33(2), 262-268.Lee, J. H., Kim, H. J., Kim, J. G., Ryu, V., Kim, B. T., Kang, D. W., & Jahng, J. W. (2007).Depressive behaviors and decreased expression of serotonin reuptake transporter in ratsthat experienced neonatal maternal separation. Neuroscience Research, 58(1), 32-39.Lehmann, J., Pryce, C. R., Jongen-Rêlo, A. L., Stöhr, T., Pothuizen, H. H., & Feldon, J.(2002). Comparison of maternal separation and early handling in terms of their neurobehavioraleffects in aged rats. Neurobiology of Aging, 23(3), 457-466.Levine, S. (1967). Maternal and environmental influences on the adrenocortical response tostress in weanling rats. Science, 156, 258-260.Levine, S. (2005). Developmental determinants of sensitivity and resistance to stress.Psychoneuroendocrinology, 30(10), 939-946.Lippmann, M., Bress, A., Nemeroff, C. B., Plotsky, P. M., & Monteggia, L. M. (2007). Longtermbehavioural and molecular alterations associated with maternal separation in rats.The European Journal of Neuroscience, 25(10), 3091-3098.Lister, R. G. (1990). Ethologically-based animal models of anxiety disorders. Pharmacologyand Therapeutics, 46(3), 321-340.Liu, D., Diorio, J., Tannenbaum, B., Caldji, C., Francis, D., Freedman, A., Sharma, S.,Pearson, D., Plotsky, P. M., & Meaney, M. J. (1997). Maternal care, hippocampal glucocorticoidreceptors, and hypothalamic-pituitary-adrenal responses to stress. Science,277, 1659-1662.Loman, M. M, & Gunnar, M. R. (2010). Early experience and the development of stress reactivityand regulation in children. Neuroscience Biobehavioral Reviews, 34(6), 867-876.MacMillan, H. L., Fleming, J. E, Streiner, D., L., Lin, E., Boyle, M. H., Jamieson, E., Duku, E.K., Walsh, C. A., Wong, M. Y., & Beardslee, W. R. (2001). Childhood abuse and lifetime psychopathologyin a community sample. The American Journal of Psychiatry, 158(11), 1878-1883.MacQueen, G. M., Ramakrishnan, K., Ratnasingan, R., Chen, B., & Young, L. T. (2003).Desipramine treatment reduces the long-term behavioural and neurochemical sequelaeof early-life maternal separation. The International Journal of Neuropsychopharmacology,6(4), 391-396.Macrì, S., Chiarotti, F., & Würbel, H. (2008). Maternal separation and maternal care actindependently on the development of HPA responses in male rats. Behavioural BrainResearch, 191(2), 227-234.Marais, L, van Rensburg, S. J, van Zyl, J. M, Stein, D. J., & Daniels, W. M. (2008). Maternalseparation of rat pups increases the risk of developing depressive-like behavior after subsequent chronic stress by altering corticosterone and neurotrophin levels in the hippocampus.Neuroscience Research, 61(1), 106-112.Marcos, B., Aisa, B., & Ramirez, M. J. (2008). Functional interaction between 5-HT(6) receptors and hypothalamic–pituitary–adrenal axis: Cognitive implications. Neuropharmacology, 54,708–714.McCormick, C. M, Kehoe, P., & Kovacs, S. (1998). Corticosterone release in response torepeated, short episodes of neonatal isolation: Evidence of sensitization. InternationalJournal of Developmental Neuroscience, 16(3-4), 175-185.McCormick, C. M., Kehoe, P., Mallinson, K., Cecchi, L., & Frye, C. A. (2002). Neonatal isolationalters stress hormone and mesolimbic dopamine release in juvenile rats.Pharmacology Biochemistry and Behavior, 73(1), 77-85.Muscat, R., Papp, M., & Willner, P. (1992). Reversal of stress-induced anhedonia by theatypical antidepressants, fluoxetine and maprotiline. Psychopharmacology (Berl), 109(4),433-438.Nutt, D. J. (2002). The neuropharmacology of serotonin and noradrenaline in depression.International Clinical Psychopharmacology. Suppl 1:S1-12.Pellow, S., Chopin, P., File, S. E., & Briley, M. (1985) Validation of open:closed arm entriesin an elevated plus-maze as a measure of anxiety in the rat. Journal of NeuroscienceMethods, 14(3), 149-167.Pfeffer, C. R., Altemus, M., Heo, M., & Jiang, H. (2007). Salivary cortisol and psychopathologyin children bereaved by the September 11, 2001 terror attacks. Biological Psychiatry,61(8), 957-965.Poldrack, R. A., & Packard, M. G. (2003). Competition among multiple memory systems:Converging evidence from animal and human brain studies. Neuropsychologia, 41(3),245-251.Porsolt, R. D., Le Pichon, M., & Jalfre, M. (1977) Depression: A new animal model sensitiveto antidepressant treatments. Nature, 266, 730-732.Prut, L., & Belzung, C. (2003). The open field as a paradigm to measure the effects of drugson anxiety-like behaviors: A review. European Journal of Pharmacology, 463(1-3), 3-33.Pryce, C. R., Rüedi-Bettschen, D., Dettling, A. C., Weston, A., Russig, H., Ferger, B., &Feldon, J. (2005). Long-term effects of early-life environmental manipulations in rodentsand primates: Potential animal models in depression research. Neuroscience andBiobehavioral Reviews, 29(4-5), 649-674.Renard, G. M., Rivarola, M. A., & Suarez, M. M. (2007). Sexual dimorphism in rats: effectsof early maternal separation and variable chronic stress on pituitary-adrenal axis andbehavior. International Journal of Developmental Neuroscience, 25(6), 373-379.Reul, J. M., & de Kloet, E. R. (1985). Two receptor systems for corticosterone in rat brain:Microdistribution and differential occupation. Endocrinology, 117(6), 2505-2511.Roceri, M., Cirulli, F., Pessina, C., Peretto, P., Racagni, G., & Riva, M. A. (2004). Postnatalrepeated maternal deprivation produces age-dependent changes of brain-derived neurotrophicfactor expression in selected rat brain regions. Biological Psychiatry, 55(7), 708-714.Rodier, P. M. (1980). Chronology of neuron development: Animal studies and their clinicalimplications. Developmental Medicine and Child Neurology, 22(4), 525-545.Rosenfeld, P., Wetmore, J. B., & Levine, S. (1992). Effects of repeated maternal separationson the adrenocortical response to stress of preweanling rats. Physiology and Behavior,52(4), 787-791.Rubin, R. T., Poland, R. E., Lesser, I. M., Winston, R. A., & Blodgett, A. L. (1987).Neuroendocrine aspects of primary endogenous depression. I .Cortisol secretory dynamicsin patients and matched controls. Archives in General Psychiatry, 44, 328–336.Salzberg, M., Kumar, G., Supit, L., Jones, N. C., Morris, M. J., Rees, S., & O’Brien, T. J.(2007). Early postnatal stress confers enduring vulnerability to limbic epileptogenesis.Epilepsia, 48(11), 2079-2085.Sapolsky, R. M., & Meaney, M. J. (1986). Maturation of the adrenocortical stress response:Neuroendocrine control mechanisms and the stress hyporesponsive period. BrainResearch, 396(1), 64-76.Slotten, H. A., Kalinichev, M., Hagan, J. J., Marsden, C. A., & Fone, K. C. (2006). Long-lastingchanges in behavioural and neuroendocrine indices in the rat following neonatalmaternal separation: Gender-dependent effects. Brain Research, 1097(1), 123-132.Springer, K. W., Sheridan, J., Kuo, D., & Carnes, M. (2007). Long-term physical and mentalhealth consequences of childhood physical abuse: Results from a large population-basedsample of men and women. Child Abuse and Neglect, 31(5), 517-530.Stanton, M. E., Gutierrez, Y. R., & Levine, S. (1988). Maternal deprivation potentiates pituitary-adrenalstress responses in infant rats. Behavioral Neuroscience, 102(5), 692-700.Stevenson, C. W., Meredith, J. P., Spicer, C. H., Mason, R., & Marsden, C. A. (2009). Earlylife programming of innate fear and fear learning in adult female rats. Behavioural BrainResearch, 198, 51-57.Stroud, L. R., Salovey, P., & Epel, E. S. (2002). Sex differences in stress responses: Socialrejection versus achievement stress. Biological Psychiatry, 52(4), 318-327.Suchecki, D., Duarte Palma, B., & Tufik, S. (2000). Pituitary-adrenal axis and behaviouralresponses of maternally deprived juvenile rats to the open field. Behavioural BrainResearch, 111(1-2), 99-106.Tsuneishi, S., Takada, S., Motoike, T., Ohashi, T., Sano, K., & Nakamura, H. (1991). Effectsof dexamethasone on the expression of myelin basic protein, proteolipid protein, andglial fibrillary acidic protein genes in developing rat brain. Developmental Brain Research,61(1), 117-123.Vazquez, V., Farley, S., Giros, B., & Daugé, V. (2005). Maternal deprivation increasesbehavioural reactivity to stressful situations in adulthood: suppression by the CCK2antagonist L365, 260. Psychopharmacology (Berl), 181(4), 706-713.Veenema, A. H., Blume, A., Niederle, D., Buwalda, B., & Neumann, I. D. (2006). Effects ofearly life stress on adult male aggression and hypothalamic vasopressin and serotonin.The European Journal of Neuroscience, 24(6), 1711-1720.Walf, A. A., & Frye, C. A. (2007). The use of the elevated plus maze as an assay of anxietyrelatedbehavior in rodents. Nature Protocols, 2(2), 322-328.Walker, C. D., Perrin, M., Vale, W., & Rivier, C. (1986). Ontogeny of the stress response inthe rat: Role of the pituitary and the hypothalamus. Endocrinology, 118(4), 1445-1451.Walsh, R. N., & Cummins, R. A (1976). The Open-Field Test: A critical review. PsychologicalBulletin, 83(3), 482-504.Wigger, A., & Neumann, I. D. (1999). Periodic maternal deprivation induces gender-dependentalterations in behavioral and neuroendocrine responses to emotional stress in adultrats. Physiology and Behavior, 66(2), 293-302.Wilber, A. A., Southwood, C. J., Sokoloff, G., Steinmetz, J. E., & Wellman, C. L. (2007).Neonatal maternal separation alters adult eyeblink conditioning and glucocorticoidreceptor expression in the interpositus nucleus of the cerebellum. DevelopmentalNeurobiology, 67(13), 1751-1764.Wilber, A. A., & Wellman, C. L. (2009). Neonatal maternal separation alters the developmentof glucocorticoid receptor expression in the interpositus nucleus of the cerebellum.International Journal of Developmental Neuroscience, 27(7), 649-654.Young, E., & Korszun, A. (2010). Sex, trauma, stress hormones and depression. MolecularPsychiatry, 15(1), 23-28.Zimmerberg, B., Foote, H. E., & Van Kempen, T. A. (2009). Olfactory association learningand brain-derived neurotrophic factor in an animal model of early deprivation.Developmental Psychobiology, 51(4), 333-344.Zimmerberg, B., & Kajunski, E. W. (2004). Sexually-dimorphic effects of neonatal allopregnanoloneon the development of anxiety behavior after early deprivation. Pharmacology,Biochemistry and Behavior, 78, 465-471.