How postnatal insults may program development: Studies in animal models

Advances in Neurobiology

Volumn 10, Issue , 2015, Pages 121-147

  Dalmaz, Carla ^a   Noschang, Cristie ^a   Krolow, Rachel ^a   Raineki, Charlis ^a   Lucion, Aldo B ^a  

^a FEDERAL UNIVERSITY OF RIO GRANDE DO SUL   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84951942382     PISSN: 21905215     EISSN: None     Source Type: Book Series    
DOI: 10.1007/978-1-4939-1372-5_7     Document Type: Chapter

References (212)

1. Adler NT (1968) Effects of male's copulatory behavior in the initiation of pregnancy in the female rat. Anatomic Rec 160: 305
2. Adler NT, Resko JA, Goy RW (1970) The effect of copulatory behavior on hormonal change in the female rat prior to implantation. Physiol Behav 5(9): 1003-1007
3. Adolphs R (2001) The neurobiology of social cognition. Curr Opin Neurobiol 11: 231-239
4. Aguilar R, Carames JM, Espinet A (2009) Effects of neonatal handling on playfulness by means of reversal of the desire to play in rats (Rattus novergicus). J Comp Psychol 123: 347-356
5. Aguilera G (1994) Regulation of pituitary ACTH secretion during chronic stress. Front Neuroendocrinol 15: 321-350
6. Ainsworth MDS, Blehar MC, Waters E, Wall S (1978) Patterns of attachment: a psychological study of the strange situation. Lawrence Erlbaum Associates, Hillsdale
7. 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
8. Aisa B, Tordera R, Lasheras B, Del Río J, Ramírez MJ (2008) Effects of maternal separation on hypothalamic-pituitary-adrenal responses, cognition and vulnerability to stress in adult female rats. Neuroscience 154(4): 1218-12 26
9. Akbari EM, Budin R, Parada M, Fleming AS (2008) The effects of early isolation on sexual behavior and c-fos expression in naïve male long-evans rats. Dev Psychobiol 50: 298-306
10. Altman J, Bayer SA (1990) Migration and distribution of two populations of hippocampal granule cell precursors during the perinatal and postnatal periods. J Comp Neurol 301(3): 365-381
11. Amaral DG (2003) The amygdala, social behavior, and danger detection. Ann N Y Acad Sci 1000: 337-347
12. Arakawa H (2005) Interaction between isolation rearing and social development on exploratory behavior in male rats. Behav Process 70: 223-234
13. Avishai-Eliner S, Eghbal-Ahmadi M, Tabachnik E, Brunson KL, Baram TZ (2001) Down-regulation of hypothalamic corticotropin releasing hormone messenger ribonucleic acid (mRNA) precedes early-life experience-induced changes in hippocampal glucocorticoid receptor mRNA. Endocrinology 142: 89-97
14. Banihashemi L, O'Neill EJ, Rinaman L (2011) Central neural responses to restraint stress are altered in rats with an early life history of repeated brief maternal separation. Neuroscience 192: 413-428
15. Barbosa Neto JB, Tiba PA, Faturi CB, de Castro-Neto EF, da Graça Naffah-Mazacoratti M, de Jesus Mari J, de Mello MF, Suchecki D (2012) Stress during development alters anxiety-like behavior and hippocampal neurotransmission in male and female rats. Neuropharmacology 62(1): 518-5 26
16. Bartova A (1968) Functioning of the hypothalamo-pituitary-adrenal system during postnatal development in rats. Gen Comp Endocrinol 10: 235-239
17. Bateson P, Barker D, Clutton-Brock T, Deb D, D'Udine B, Foley RA, Gluckman P Godfrey K, Kirkwood T, Lahr MM, McNamara J, Metcalfe NB, Monaghan P, Spencer HG, Sultan SE (2004) Developmental plasticity and human health. Nature 430: 419-421
18. Bazak N, Kozlovsky N, Kaplan Z, Matar M, Golan H, Zohar J et al (2009) Pre-pubertal stress exposure affects adult behavioral response in association with changes in circulating corticosterone and brain-derived neurotrophic factor. Psychoneuroendocrinology 34: 844-858
19. Benekareddy M, Vadodaria KC, Nair AR, Vaidya VA (2011) Postnatal serotonin type 2 receptor blockade prevents the emergence of anxiety behavior, dysregulated stress-induced immediate early gene responses, and specific transcriptional changes that arise following early life stress. Biol Psychiatry 70(11): 1024-1032
20. Bielsky IF, Young LJ (2004) Oxytocin, vasopressin, and social recognition in mammals. Peptides 25: 1565-1574
21. Boccia ML, Pedersen CA (2001) Brief vs. long maternal separations in infancy: contrasting relationships with adult maternal behavior and lactation levels of aggression and anxiety. Psychoneuroendocrinology 26: 657-672
22. Boufleur N, Antoniazzi CT, Pase CS, Benvegnú DM, Dias VT, Segat HJ, Roversi K, Roversi K, Nora MD, Koakoskia G, Rosa JG, Barcellos LJ, Bürger ME (2012) Neonatal handling prevents anxiety-like symptoms in rats exposed to chronic mild stress: behavioral and oxidative parameters. Stress. [Epub ahead of print]
23. Bowlby J (1969) Attachment and loss, vol 1. Basic Books, New York
24. Breslau N, Wilcox H, Storr C, Lucia V, Anthony J (2004) Trauma exposure and posttraumatic stress disorder: a study of youths in urban America. J Urban Health 81: 530-544
25. Buck Louis GM, Gray LE, Marcus M, Ojeda SR, Pescovitz OH, Witchel SF et al (2008) Environmental factors and puberty timing: expert panel research needs. Pediatrics 121: 192-207
26. Caldji C, Tannenbaum B, Sharma S, Francis D, Plotsky P M., Meaney MJ (1998) Maternal care during infancy regulates the development of neural systems mediating the expression of fearfulness in the rat. Proc Natl Acad Sci U S A 95(9): 5335-5340
27. Caldji C, Francis D, Sharma S, Plotsky PM, Meaney MJ (2000) The effects of early rearing environment on the development of GABAA and central benzodiazepine receptor levels and novelty-induced fearfulness in the rat. Neuropsychopharmacology 22(3): 219-229
28. Cameron NM, Champagne FA, Parent C, Fish EW, Ozaki-Kuroda K, Meaney MJ (2005) The programming of individual differences in defensive responses and reproductive strategies in the rat though variations in maternal care. Neurosci Biobehav Rev 29: 843-865
29. Camozzato TSC, Winkekmann-Duarte EC, Padilha CB, Miguel SPR, Bonzanini L, Anselmo-Franci JA, Fernandes MC, Lucion AB (2009) Neonatal handling reduces the number of cells in the medial preoptic area of female rats. Brain Res 1247: 92-99
30. Carlson M, Earls F (1997) Psychological and neuroendocrinological sequelae of early social deprivation in institutionalized children in Romania. Ann N Y Acad Sci 807: 419-428
31. Champoux M, Coe CL, Shanberg S, Kuhn C, Suomi SJ (1989) Hormonal effects of early rearing conditions in the infant rhesus monkey. Am J Primatol 19 111-117
32. Charil A, Laplante DP, Vaillancourt C, King S (2010) Prenatal stress and brain development. Brain Res Rev 65: 56-79
33. Chrousos GP, Gold PW (1992) The concepts of stress and stress system disorders. Overview of physical and behavioral homeostasis. JAMA 267: 1244-1252
34. Crews F, He J, Hodge C (2007) Adolescent cortical development: a critical period of vulnerability for addiction. Pharmacol Biochem Behav 86: 189-199
35. Dahl RE (2004) Adolescent brain development: a period of vulnerabilities and opportunities. Ann N Y Acad Sci 1021: 1-22
36. Dalle Molle R, Portella AK, Goldani MZ, Kapczinski FP, Leistner-Segala S, Salum GA, Manfro GG, Silveira PP (2012) Associations between parenting behavior and anxiety in a rodent model and a clinical sample: relationship to peripheral BDNF levels. Transl Psychiatry 2(11): 2195
37. De Kloet ER, Wallach G, McEwen BS (1975) Differences in corticosterone and dexamethasone binding to rat brain and pituitary. Endocrinology 96: 598-609
38. 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
39. Diehl LA, Silveira PP, Leite MC, Crema LM, Portella AK, Billodre MN, Nunes E, Henriques TP, Fidelix-da-Silva LB, Heis MD, Gonçalves CA, Quillfeldt JA, Dalmaz C (2007) Long lasting sex-specific effects upon behavior and S100b levels after maternal separation and exposure to a model of post-traumatic stress disorder in rats. Brain Res 1144: 107-116
40. Doremus-Fitzwater TL, Varlinskaya EI, Spear LP (2009) Social and non-social anxiety in adolescent and adult rats after repeated restraint. Physiol Behav 97: 484-494
41. Douglas L, Varlinskaya E, Spear LP (2004) Rewarding properties of social interactions in adolescent and adult male and female rates: impact of social versus isolate housing of subjects and partners. Dev Psychobiol 45: 153-162
42. Eiland L, Ramroop J, Hill MN, Manely J, McEwen BS (2012) Chronic juvenile stress produces corticolimbic dendritic architectural remodeling and modulates emotional behavior in male and female rats. Psychoneuroendocrinology 37: 39-47
43. Einon DF, Morgan MJ (1977) A critical period for social isolation in the rat. Dev Psychobiol 10: 123-132
44. Engelmann M, Ludwig M, Landgraft R (1994) Simultaneous monitoring of intracerebral release and behavior: endogenous vasopressin improves social recognition. J Neuroendocrinol 6: 391-395
45. Fenoglio KA, Brunson KL, Avishai-Eliner S, Stone BA, Kapadia BJ, Baram TZ (2005) Enduring, handling-evoked enhancement of hippocampal memory function and glucocorticoid receptor expression involves activation of the corticotropin-releasing factor type 1 receptor. Endocrinology 146(9): 4090-4096
46. Fenoglio KA, Chen Y, Baram TZ (2006) Neuroplasticity of the hypothalamic-pituitary-adrenal axis early in life requires recurrent recruitment of stress-regulating brain regions. J Neurosci 26(9): 2434-2442
47. Ferguson JN, Young LJ, Insel TR (2002) The neuroendocrine basis of social recognition. Front Neuroendocrinol 23: 200-224
48. Ferris C (1992) Role of vasopressin in aggressive and dominant/subordinate behaviors. Ann N Y Acad Sci 652: 212-226
49. Foilb AR, Lui P, Romeo RD (2011) The transformation of hormonal stress responses throughout puberty and adolescence. J Endocrinol 210: 391-398
50. Ford JD, Kidd P (1998) Early childhood trauma and disorders of extreme stress as predictors of treatment outcome with chronic posttraumatic stress disorder. J Trauma Stress 11: 743-761
51. Francis DD, Meaney MJ (1999) Maternal care and the development of stress responses. Curr Opin Neurobiol 9: 128-134
52. Freeman ME (2006) Neuroendocrine control of the ovarian cycle of the rat. In: Neill JD (ed) Knobil and Neill's physiology of reproduction. Raven Press, New York, pp 2327-2388
53. Frisone DF, Frye CA, Zimmerberg B (2002) Social isolation stress during the third week of life has age-dependent effects on spatial learning in rats. Behav Brain Res 128: 153-160
54. Garoflos E, Panagiotaropoulos T, Pondiki S, Stamatakis A, Philippidis E, Stylianopoulou F (2005) Cellular mechanisms underlying the effects of an early experience on cognitive abilities and affective states. Ann Gen Psychiatry 4(1): 8
55. Giovenardi M, de Azevedo MS, da Silva SP, Hermel EES, Gomes CM, Lucion AB (2005) Neonatal handling increases fear and aggression in lactating rats. Physiol Behav 86 209-217
56. Gobrogge KL, Liu Y, Young LJ, Wang Z (2009) Anterior hypothalamic vasopressin regulates pairbonding and drug-induced aggression in a monogamous rodent. Proc Natl Acad Sci U S A 106: 19144-19149
57. Gogtay N, Giedd JN, Lusk L, Hayashi KM, Greenstein D, Vaituzis AC, Nugent TF, Herman DH, Clasen LS, Toga AW, Rappoport JL, Thompson PM (2004) Dynamic mapping of human cortical development during childhood through early adulthood. Proc Natl Acad Sci U S A 101: 8174-8179
58. Goldman L, Winget C, Hollingshead GW, Levine S (1973) Postweaning development of negative feedback in the pituitary-adrenal system of the rat. Neuroendocrinology 12: 199-211
59. Gomes CM, Frantz PJ, Sanvitto GL, Anselmo-Franci JA, Lucion AB (1999) Neonatal handling induces anovulatory estrous cycles in rats. Braz J of Med Biol Res 32: 1239-1242
60. Gomes CM, Raineki C, Ramos de Paula P, Severino GS, Helena CVV, Anselmo-Franci JA, Franci CR, Sanvitto GL, Lucion AB (2005) Neonatal handling and reproductive function in female rats. J of Endocrinol 184: 435-445
61. Gomes CM, Donadio MVF, Anselmo-Franci JA, Franci CR, Lucion AB, Sanvitto GL (2006) Neonatal handling induces alteration in progesterone secretion after sexual behavior but not in angiotensin II receptor density in the medial amygdala: implication for reproductive success. Life Sci 78: 2867-2871
62. Gross C, Hen R (2004) The developmental origins of anxiety. Nat Rev Neurosci 5(7): 545-552
63. Haltmeyer GC, Denenberg VH, Thatcher J, Zarrow MX (1966) Response of the adrenal cortex of the neonatal rat after subjection to stress. Nature. 212: 1371-1373
64. Harlow HF, Dodsworth RO, Harlow MK (1965) Total social isolation in monkeys. Proc Natl Acad Sci U S A 54(1): 90-97
65. He J, Crews FT (2007) Neurogenesis decreases during brain maturation from adolescence to adulthood. Pharmacol Biochem Behav 86: 327-333
66. Heim C, Nemeroff CB (2001) The role of childhood trauma in the neurobiology of mood and anxiety disorders: preclinical and clinical studies. Biol Psychiatry 49: 1023-1039
67. Heim C, Plotsky PM, Nemeroff CB (2004) Importance of studying the contributions of early adverse experience to neurobiological findings in depression. Neuropsychopharmacology 29: 641-648
68. Herman JP, Figueiredo H, Mueller NK, Ulrich-Lai Y, Ostander MM, Choi DC, Cullinan WE (2003) Central mechanisms of stress integration: hierarchical circuitry controlling hypothalamic-pituitary-adrenocortical responsiveness. Front Neuroendocrinol 24: 151-180
69. Hinde RA, Spencer-Booth Y (1971) Towards understanding individual differences in rhesus mother-infant interaction. Anim Behav 19: 165-173
70. Hinde RA, Spencer-Booth Y, Bruce M (1966) Effects of 6-day maternal deprivation on rhesus monkey infants. Nature 210: 1021-1023
71. Hodes GE, Shors TJ (2005) Distinctive stress effects on learning during puberty. Horm Behav 48: 163-171
72. Hofer MA, Sullivan RM (2008) Towards a neurobiology of attachment. In: Nelson CA, Luciana M (eds) Handbook of developmental cognitive neuroscience. MIT Press, Cambridge, pp 787-806
73. 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(8): 1335-1346
74. Howland JG, Wang YT (2008) Synaptic plasticity in learning and memory: stress effects in the hippocampus. Prog Brain Res 169: 145-158
75. Hubel D, Wiesel T (2012) David Hubel and Torsten Wiesel. Neuron 75(2): 182-184
76. 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 (Berl) 158(4): 366-373
77. Huot RL, Plotsky PM, Lenox RH, McNamara RK (2002) Neonatal maternal separation reduces hippocampal mossy fiber density in adult Long Evans rats. Brain Res 950(1-2): 52-63
78. Insel TR (2010) The challenge of translation in social neuroscience: a review of oxytocin, vasopressin, and affiliative behavior. Neuron 65: 768-779
79. Ivy AS, Brunson KL, Sandman C, Baram TZ (2008) Dysfunctional nurturing behavior in rat dams with limited access to nesting material: a clinically relevant model for early-life stress. Neuroscience 154(3): 1132-1142
80. Iwasaki S, Inoue K, Kiriike N, Hikiji K (2000) Effect of maternal separation on feeding behavior of rats in later life. Physiol Behav 70(5): 551-556
81. Jahng JW (2011) An animal model of eating disorders associated with stressful experience in early life. Horm Behav 59(2): 213-220
82. Kember RL, Dempster EL, Lee TH, Schalkwyk LC, Mill J, Fernandes C (2012) Maternal separation is associated with strain-specific responses to stress and epigenetic alterations to Nr3c1, Avp, and Nr4a1 in mouse. Brain Behav 2(4): 455-467
83. Kessler RC, Magee WJ (1993) Childhood adversities and adult depression: basic patterns of association in a US national survey. Psychol Med 23: 679-690
84. Kiosterakis G, Stamatakis A, Diamantopoulou A, Fameli M, Stylianopoulou F (2009) Long-term effects of neonatal handling on mu-opioid receptor levels in the brain of the offspring. Dev Psychobiol 51(5): 439-449
85. Klein ZA, Padow VA, Romeo RD (2010) The effects of stress on play and home cage behaviors in adolescent male rats. Dev Psychobiol 52: 62-70
86. Koike H, Ibi D, Mizoguchi H, Nagai T, Nitta A, Takuma K et al (2009) Behavioral abnormality and pharmacological response in social isolation-reared mice. Behav Brain Res 202: 114-121
87. Kosten TA, Miserendino MJ, Bombace JC, Lee HJ, Kim JJ (2005) Sex-selective effects of neonatal isolation on fear conditioning and foot shock sensitivity. Behav Brain Res 157(2): 235-244
88. Kosten TA, Lee HJ, Kim JJ (2006) Early life stress impairs fear conditioning in adult male and female rats. Brain Res 1087(1): 142-150
89. Kosten TA, Lee HJ, Kim JJ (2007) Neonatal handling alters learning in adult male and female rats in a task-specific manner. Brain Res 1154: 144-153
90. Kosten TA, Kim JJ, Lee HJ (2012) Early life manipulations alter learning and memory in rats. Neurosci Biobehav Rev 36(9): 1985-2006
91. Kraemer GW (2003) Psychobiology of early social attachment in rhesus monkey. Clinical implications. Ann N Y Acad Sci 15: 401-408
92. Krolow R, Noschang C, Weis SN, Pettenuzzo LF, Huffell AP, Arcego DM, Marcolin M, Mota CS, Kolling J, Scherer EB, Wyse AT, Dalmaz C (2012) Isolation stress during the prepubertal period in rats induces long-lasting neurochemical changes in the prefrontal cortex. Neurochem Res 37: 1063-1073
93. Krolow R, Noschang C, Arcego DM, Pettenuzzo LF, Weis SN, Marcolin ML, Huffell AP, Mota CS, Dalmaz C (2013) Isolation stress exposure and consumption of palatable diet during the prepubertal period leads to cellular changes in the hippocampus. Neurochem Res 38: 262-272
94. Ladd CO, Huot RL, Thrivikraman KV, Nemeroff CB, Plotsky PM (2004) Long-term adaptations in glucocorticoid receptor and mineralocorticoid receptor mRNA and negative feedback on the hypothalamo-pituitary-adrenal axis following neonatal maternal separation. Biol Psychiatry 55(4): 367-375
95. Lau C, Klinefelter G, Cameron AM (1996) Reproductive development and functions in the rat after repeated maternal deprivation stress. Fundam Appl Toxicol 30: 298-301
96. Lehmann J, Pryce CR, Bettschen D, Feldon J (1999) The maternal separation paradigm and adult emotionality and cognition in male and female Wistar rats. Pharmacol Biochem Behav 64(4): 705-715
97. Lenz KM, Graham MD, Parada M, Fleming AS, Sengelaub DR, Monks DA (2008) Tactile stimulation during artificial rearing influences adult function and morphology in a sexually dimorphic neuromuscular system. Dev Neurobiol 68: 542-557
98. Leussis MP, Andersen SL (2008) Is adolescence a sensitive period for depression? Behavioral and neuroanatomical findings from a social stress model. Synapse 62: 22-30
99. Leussis MP, Lawson K, Stone K, Andersen SL (2008) The enduring effects of an adolescent social stressor on synaptic density, part II: poststress reversal of synaptic loss in the cortex by adinazolam and MK-801. Synapse 62: 185-192
100. Levine S (1957) Infantile experience and resistance to physiological stress. Science 126: 405-406
101. Levine S, Haltmeyer G, Karas G, Denenberg V (1967) Physiological and behavioral effects of infantile stimulation. Physiol Behav 2: 55-59
102. Levy F, Melo AI, Galef Jr BG, Madden M, Fleming AS (2003) Complete maternal deprivation affects social, but not spatial, learning in adult rats. Dev Psychobiol 43: 177-191
103. Lim MM, Young LJ (2006) Neuropeptidergic regulation of affiliative behavior and social bonding in animals. Horm Behav 50: 506-517
104. Lippmann M, Bress A, Nemeroff CB, Plotsky PM, Monteggia LM (2007) Long-term behavioural and molecular alterations associated with maternal separation in rats. Eur J Neurosci 25(10): 3091-3098
105. Liu D, Diorio J, Tannenbaum B, Caldji C, Francis D, Freedman A, Sharma S, Pearson D, Plotsky PM, Meaney MJ (1997) Maternal care, hippocampal glucocorticoid receptors, and hypothalamic-pituitary-adrenal responses to stress. Science 277(5332): 1659-1662
106. Liu D, Caldji C, Sharma S, Plotsky PM, Meaney MJ (2000) Influence of neonatal rearing conditions on stress-induced adrenocorticotropin responses and norepinepherine release in the hypothalamic paraventricular nucleus. J Neuroendocrinol 12(1): 5-12
107. Lucion AB, Pereira FM, Winkelman EC, Anselmo-Franci JA, Sanvitto GL (2003) Neonatal handling reduces the number of cells in the locus coeruleus of rats. Behav Neurosci 117(5): 894-903
108. Lummaa V, Clutton-Brock T (2002) Early development, survival and reproduction in humans. Trends Ecol Evol 17: 141-147
109. Lupien SJ, Fiocco A, Wan N, Maheu F, Lord C, Schramek T, Tu MT (2005) Stress hormones and human memory function across the lifespan. Psychoneuroendocrinology 30: 225-242
110. Lutter M, Nestler EJ (2009) Homeostatic and hedonic signals interact in the regulation of food intake. J Nutr 139(3): 629-632
111. Madruga C, Xavier LL, Achaval M, Sanvitto GL, Lucion AB (2006) Early handling, but not maternal separation, decreases emotional responses in two paradigms of fear without changes in mesolimbic dopamine. Behav Brain Res 166(2): 241-246
112. Makena N, Bugarith K, Russell VA (2012) Maternal separation enhances object location memory and prevents exercise-induced MAPK/ERK signalling in adult Sprague-Dawley rats. Metab Brain Dis 27(3): 377-385
113. Matthews SG (2002) Early programming of the hypothalamo-pituitary-adrenal axis. Trend Endocrinol Metabol 13: 373-380
114. Mazaro R, Lamano-Carvalho TL (2006) Prolonged deleterious effects of neonatal handling on reproductive parameters of pubertal male rats. Reprod Fertil Dev 18: 497-500
115. McCormick CM, Mathews IZ (2007) HPA function in adolescence: role of sex hormones in its regulation and the enduring consequences of exposure to stressors. Pharmacol Biochem Behav 86: 220-233
116. McEwen BS (1994) Corticosteroids and hippocampal plasticity. Ann N Y Acad Sci 746: 134-142
117. McEwen BS (2007) Physiology and neurobiology of stress and adaptation: central role of the brain. Physiol Rev 87: 873-904
118. McEwen BS, Weiss JM, Schwartz LS (1968) Selective retention of corticosterone by limbic structure in rat brain. Nature 220: 911-912
119. McIntosh J, Anisman H, Merali Z (1999) Short-and long-periods of neonatal maternal separation differentially affect anxiety and feeding in adult rats: gender-dependent effects. Brain Res Dev Brain Res 113(1-2): 97-106
120. McLeod J, Sinal CJ, Perrot-Sinal TS (2007) Evidence for non-genomic transmission of ecological information via maternal behavior in female rats. Genes Brain Behav 6: 19-29
121. Meaney MJ, Aitken DH (1985) The effects of early postnatal handling on hippocampal glucocorticoid receptor concentrations: temporal parameters. Brain Res 354(2): 301-304
122. Meaney MJ, Aitken DH, Bodnoff SR, Iny LJ, Tatarewicz JE, Sapolsky RM (1985) Early postnatal handling alters glucocorticoid receptor concentrations in selected brain regions. Behav Neurosci 99(4): 765-770
123. Meaney MJ, Aitken DH, Sharma S, Viau V, Sarrieau A (1989) Postnatal handling increases hippocampal type II, glucocorticoid receptors and enhances adrenocortical negative-feedback efficacy in the rat. Neuroendocrinology 51: 597-604
124. Meaney MJ, Mitchell JB, Aitken DH, Bhatnagar S, Bodnoff SR, Iny LJ, Sarrieau A (1991) The effects of neonatal handling on the development of the adrenocortical response to stress: implications for neuropathology and cognitive deficits in later life. Psychoneuroendocrinology 16(1-3): 85-103
125. Meaney MJ, Diorio J, Francis D, Widdowson J, LaPlante P, Caldji C, Sharma S, Seckl JR, Plotsky PM (1996) Early environmental regulation of forebrain glucocorticoid receptor gene expression: implications for adrenocortical responses to stress. Dev Neurosci 18(1-2): 49-72
126. Meerlo P, Horvath KM, Nagy GM, Bohus B, Koolhaas JM (1999) The influence of postnatal handling on adult neuroendocrine and behavioural stress reactivity. J Neuroendocrinol 11: 925-933
127. Meinlschmidt G, Heim C (2005) Decreased cortisol awakening response after early loss experience. Psychoneuroendocrinology 30: 568-576
128. Neumann ID (2008) Brain oxytocin: a key regulator of emotional and social behaviours in both male and females. J Neuroendocrinol 20: 858-865
129. Nishi M, Horii-Hayashi N, Sasagawa T, Matsunaga W (2013) Effects of early life stress on brain activity: implications from maternal separation model in rodents. Gen Comp Endocrinol 181: 306-309
130. Noschang CG, Krolow R, Fontella FU, Arcego DM, Diehl LA, Weis SN, Arteni NS, Dalmaz C (2010) Neonatal handling impairs spatial memory and leads to altered nitric oxide production and DNA breaks in a sex specific manner. Neurochem Res 35(7): 1083-1091
131. Noschang C, Krolow R, Arcego DM, Toniazzo AP, Huffell AP, Dalmaz C (2012) Neonatal handling affects learning, reversal learning and antioxidant enzymes activities in a sex-specific manner in rats. Int J Dev Neurosci 30: 285-291
132. Núñez JF, Ferré P, García E, Escorihuela RM, Fernández-Teruel A, Tobeña A (1995) Postnatal handling reduces emotionality ratings and accelerates two-way active avoidance in female rats. Physiol Behav 57(5): 831-835
133. Ogawa T, Mikuni M, Kuroda Y, Muneoka K, Mori KJ, Takahashi K (1994) Periodic maternal deprivation alters stress response in adult offspring: potentiates the negative feedback regulation of restraint stress-induced adrenocortical response and reduces the frequencies of open fieldinduced behaviors. Pharmacol Biochem Behav 49(4): 961-967
134. Oomen CA, Soeters H, Audureau N, Vermunt L, van Hasselt FN, Manders EM, Joëls M, Krugers H, Lucassen PJ (2011) Early maternal deprivation affects dentate gyrus structure and emotional learning in adult female rats. Psychopharmacology (Berl) 214(1): 249-260
135. 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
136. Padoin MJ, Cadore LP, Gomes CM, Barros HMT, Lucion AB (2001) Long-lasting effects of neonatal stimulation on the behavior of rats. Behav Neurosci 115: 1332-1340
137. 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
138. Panksepp JB, Lahvis GP (2007) Social reward among juvenile mice. Genes Brain Behav 6: 661-671
139. Panksepp JB, Jochman KA, Kim JU, Koy JJ, Wilson ED, Chen Q et al (2007) Affiliative behavior, ultrasonic communication and social reward are influenced by genetic variation in adolescent mice. PLoS ONE 2(4): e351
140. Pellis SM, Pellis VC (1987) Play-fighting differs from serious fighting in both target of attack and tactics of fighting in the laboratory rat Rattus norvegicus. Aggress Behav 13: 227-242
141. Penza KM, Heim C, Nemeroff CB (2003) Neurobiological effects of childhood abuse: implications for the pathophysiology of depression and anxiety. Arch Women Ment Health 6: 15-22
142. Pibiri F, Nelson M, Guidotti A, Costa E, Pinna G (2008) Decreased corticolimbic allopregnanolone expression during social isolation enhances contextual fear: a model relevant for posttraumatic stress disorder. Proc Natl Acad Sci U S A 105: 5567-5572
143. Pinna G, Dong E, Matsumoto K, Costa E, Guidotti A (2003) In socially isolated mice, the reversal of brain allopregnanolone down-regulation mediates the antiaggressive action of fluoxetine. Proc Natl Acad Sci U S A 100: 2035-2040
144. Pinna G, Costa E, Guidotti A (2006) Fluoxetine and norfluoxetine stereospecifically and selectively increase brain neurosteroid content at doses that are inactive on 5-HT reuptake. Psychopharmacology 186: 362-372
145. Pinna G, Costa E, Guidotti A (2009) SSRIs act as selective brain steroidogenic stimulants (SBSSs) at low doses that are inactive on 5-HT reuptake. Curr Opin Pharmacol 9: 24-30
146. Plotsky PM, Meaney MJ (1993) Early, postnatal experience alters hypothalamic corticotropinreleasing factor (CRF) mRNA, median eminence CRF content and stress-induced release in adult rats. Brain Res Mol Brain Res 18(3): 195-200
147. Plotsky PM, Owens MJ, Nemeroff CB (2008) Psychoneuroendocrinology of depression. Hypothalamic-pituitary-adrenal axis. Psychiatr Clin North Am 21: 293-307
148. Pryce CR, Feldon J (2003) The role of corticotropin-releasing factor-norepinephrine systems in mediating the effects of early experience on the development of behavioral and endocrine responses to stress. Neurosci Biobehav Rev 27: 57-71
149. Pryce CR, Ruedi-Bettschen D, Dettling AC, Feldon J (2005a) Early-life environmental manipulations in rodents and primates: potential animal models in depression research. In: Steckler T, Kalin NH, Reul JMHM (eds) Handbook of stress and the brain. Elsevier, Amsterdam, pp 23-50
150. Pryce CR, Rüedi-Bettschen D, Dettling AC, Weston A, Russig H, Ferger B, Feldon J (2005b) The role of corticotropin-releasing factor-norepinephrine systems in mediating the effects of early experience on the development of behavioral and endocrine responses to stress. Neurosci Biobehav Rev 29(4-5): 649-674
151. Qiang M, Chen YC, Wang R et al (1997) Nitric oxide is involved in the formation of learning and memory in rats: studies using passive avoidance response and Morris water maze task. Behav Pharmacol 8: 183-187
152. Quillfeldt JA (2010) Behavioral methods to study learning and memory in rats. In: Levy-Andersen M, Tufik S (eds) Animal models as tools in ethical biomedical research (pp 227-269). AFIP, São Paulo
153. Radley JJ, Rocher AB, Janssen WGM, Hof PR, McEwen BS, Morrison JH (2005) Reversibility of apical dendritic retraction in the rat medial prefrontal cortex following repeated stress. Exp Neurol 196: 199-203
154. Raineki C, Szawka RE, Gomes CM, Lucion MK, Barp J, Bello-Klein A, Franci CR, Anselmo-Franci JA, Sanvitto GL, Lucion AB (2008) Effects of neonatal handling on central noradrenergic and nitric oxidergic systems and reproductive parameters in female rats. Neuroendocrinology 87: 151-159
155. Raineki C, Souza MA, Szawka RE, Lutz ML, Vasconcellos LFT, Sanvitto GL Izquierdo I, Bevilaqua LR, Cammarota M, Lucion AB (2009) Neonatal handling and maternal odor preference in rat pups: involvement of monoamines and cyclic AMP response element-binding protein pathway in the olfactory bulb. Neuroscience 159: 31-38
156. Raineki C, Lutz ML, Sebben V, Ribeiro RA, Lucion AB (2013) Neonatal handling induces deficits in infant mother preference and adult partner preference. Dev Psychobiol 55(5): 496-507
157. Rhees RW, Laphart ED, Eliason D (2001) Effects of maternal separation during early postnatal development on male sexual behavior and female reproductive function. Behav Brain Res 123: 1-10
158. Roman E, Gustafsson L, Berg M, Nylander I (2006) Behavioral profiles and stress-induced corticosteroid secretion in male Wistar rats subjected to short and prolonged periods of maternal separation. Horm Behav 50: 736-747
159. Romeo RD (2010) Adolescence: a central event in shaping stress reactivity. Dev Psychobiol 52: 244-253
160. Romeo RD, Lee SJ, Chhua N, McPherson CR, McEwen BS (2004a) Testosterone cannot activate an adult-like stress response in prepubertal male rats. Neuroendocrinology 79: 125-132
161. Romeo RD, Lee SJ, McEwen BS (2004b) Differential stress reactivity in intact and ovariectomized prepubertal and adult female rats. Neuroendocrinology 80: 387-393
162. Romeo RD, Bellani R, Karatsoreos IN, Chhua N, Vernov M, Conrad CD, McEwen BS (2006) Stress history and pubertal development interact to shape hypothalamic pituitary adrenal axis plasticity. Endocrinology 147: 1664-1674
163. Romeo RD, Tang AC, Sullivan RM (2009) Early-life experiences: enduring behavioral, neurological, and endocrinological consequences, In: Pfaff DW, Etgen AM, Fahrbach SE, Rubin RT (eds) Hormones, brain and behavior, Elsevier, New York, 20 pp (1975-2004)
164. Ross HE, Young LJ (2009) Oxytocin and neural mechanisms regulating social cognition and affiliative behavior. Front Neuroendocrinol 30: 534-547
165. Ryu V, Lee JH, Yoo SB, Gu XF, Moon YW, Jahng JW (2008) Sustained hyperphagia in adolescent rats that experienced neonatal maternal separation. Int J Obes (Lond) 32(9): 1355-1362
166. Ryu V, Yoo SB, Kang DW, Lee JH, Jahng JW (2009) Post-weaning isolation promotes food intake and body weight gain in rats that experienced neonatal maternal separation. Brain Res 1295: 127-134
167. Sánchez MM, Ladd CO, Plotsky PM (2001) Early adverse experience as a developmental risk factor for later psychopathology: evidence from rodent and primate models. Dev Psychopathol 13(3): 419-449
168. Sapolsky RM, Meaney MJ (1986) Maturation of the adrenocortical stress response: neuroendocrine control mechanisms and the stress hyporesponsive period. Brain Res 396(1): 64-76
169. Schmidt MV, Sterlemann V, Ganea K, Liebl C, Alam S, Harbich D et al (2007) Persistent neuroendocrine and behavioral effects of a novel, etiologically relevant mouse paradigm for chronic social stress during adolescence. Psychoneuroendocrinology 32: 417-429
170. Schmidt MV, Czisch M, Sterlemann V, Reinel C, Samann P, Muller MB (2009) Chronic social stress during adolescence in mice alters fat distributionin late life: prevention by antidepressant treatment. Stress 12: 89-94
171. Schulz KM, Molenda-Figueira HA, Sisk CL (2009) Back to the future: the organizational-activational hypothesis adapted to puberty and adolescence. Horm Behav 55: 597-604
172. Schwartz NB (2000) Neuroendocrine regulation of reproductive cyclicity. In: Conn PM, Freeman ME (eds) Neuroendocrinology in physiology and medicine. Humana Press, Clifton, pp 135-146
173. Severino GS, Fossati IA, Padoin MJ, Gomes CM, Trevizan L, Sanvitto GL, Franci CR, Anselmo-Franci JA, Lucion AB (2004) Effects of neonatal handling on the behavior and prolactin stress response in male and female rats at various ages and estrous cycle phases of females. Physiol Behav 81(3): 489-4 98
174. Shea A, Walsh C, Macmillan H, Steiner M (2005) Child maltreatment and HPA axis dysregulation: relationship to major depressive disorder and post traumatic stress disorder in females. Psychoneuroendocrinology 30: 162-178
175. Sheriff MJ, Krebs CJ, Boonstra R (2010) The ghosts of predators past: population cycles and the role of maternal programming under fluctuating predation risk. Ecology 91(10): 2983-2994
176. Sieck G, Ramaley JA (1975) Effects of early handling upon puberty: correlations with adrenal stress responsiveness. Physiol Behav 15: 487-489
177. Silveira PP, Portella AK, Clemente Z, Bassani E, Tabajara AS, Gamaro GD, Dantas G, Torres IL, Lucion AB, Dalmaz C (2004) Neonatal handling alters feeding behavior of adult rats. Physiol Behav 80(5): 739-745
178. Silveira PP, Portella AK, Clemente Z, Gamaro GD, Dalmaz C (2005) The effect of neonatal handling on adult feeding behavior is not an anxiety-like behavior. Int J Dev Neurosci 23(1): 93-99
179. Silveira PP, da Silva Benetti C, Ayres C, Pederiva FQ, Portella AK, Lucion AB, Dalmaz C (2006) Satiety assessment in neonatally handled rats. Behav Brain Res 173(2): 205-210
180. Silveira PP, Portella AK, Assis SA, Nieto FB, Diehl LA, Crema LM, Peres W, Costa G, Scorza C, Quillfeldt JA, Lucion AB, Dalmaz C (2010) Early life experience alters behavioral responses to sweet food and accumbal dopamine metabolism. Int J Dev Neurosci 28(1): 111-118
181. Sisk CL, Foster DL (2004) The neural basis of puberty and adolescence. Nat Neurosci 7: 1040-1047
182. Siviy SM, Harrison KA (2008) Effects of neonatal handling on play behavior and fear towards a predator odor in juvenile rats (Rattus norvegicus) J Comp Psychol 122: 1-8
183. Slotten HA, Kalinichev M, Hagan JJ, Marsden CA, Fone KC (2006) Long-lasting changes in behavioural and neuroendocrine indices in the rat following neonatal maternal separation: gender-dependent effects. Brain Res 1097(1): 123-132
184. Spear LP (2000) The adolescent brain and age-related behavioral manifestations Neurosci Biobehav Rev 24: 417-463
185. Stevenson CW, Meredith JP, Spicer CH, Mason R, Marsden CA (2009) Early life programming of innate fear and fear learning in adult female rats. Behav Brain Res 198(1): 51-57
186. Suomi SJ, Harlow HF, Domek CJ (1971) Effects of repetitive infant-infant separation of young monkeys. J Abnormal Psychol 76: 161-172
187. Thomas KM, Drevets WC, Dahl RE, Ryan ND, Birmaher B, Eccard CH, Casey BJ (2001) Amygdala response to fearful faces in anxious and depressed children. Arch Gen Psychiatry 58: 1057-1063
188. Todeschin AS, Winkelmann-Duarte EC, Jacob MHV, Aranda BCC, Jacobs S, Fernandes MC, Ribeiro MFM, Sanvitto GL, Lucion AB (2009) Effects of neonatal handling on social memory, social interaction, and number of oxytocin and vasopressin neurons in rats. Horm Behav 56: 93-100
189. Tsoory M, Richter-Levin G (2005) Learning under stress in the adult rat is differentially affected by 'juvenile' or 'adolescent' stress. Int J Neuropsychopharmacol 8: 1-16
190. Tsoory M, Cohen H, Richter-Levin G (2007) Juvenile stress induces a predisposition to either anxiety or depressive-like symptoms following stress in adulthood. Eur Neuropsychopharmacol 17: 245-256
191. Tsuda MC, Yamaguchi N, Ogawa S (2011) Early life stress disrupts peripubertal development of aggression in male mice. Neuroreport 22: 259-263
192. Uys JDK, Marais L, Faure J, Prevoo D, Swart P, Mohammed AH et al (2006a) Developmental trauma is associated with behavioral hyperarousal, altered HPA axis activity, and decreased hippocampal neurotrophin expression in the adult rat. Ann N Y Acad Sci 1071: 542-546
193. Uys JDK, Muller CJF, Marais L, Harvey BH, Stein DJ, Daniels WMU (2006b) Early life trauma decreases glucocorticoid receptors in rat dentate gyrus upon adult re-stress: reversal by escitalopram. Neuroscience 137: 619-625
194. Vallée M, Mayo W, Dellu F, Le Moal M, Simon H, Maccari S (1997) Prenatal stress induces high anxiety and postnatal handling induces low anxiety in adult offspring: correlation with stressinduced corticosterone secretion. J Neurosci 17(7): 2626-2636
195. Van den Berg CL, Pijlman FT, Koning HA, Diergaarde L, Van Ree JM, Spruijt BM (1999) Isolation changes the incentive value of sucrose and social behaviour in juvenile and adult rats. Behav Brain Res 106: 133-142
196. Van den Berg CL, Van Ree JM, Spruijt BM (2000) Morphine attenuates the effects of juvenile isolation in rats. Neuropharmacology 39: 969-976
197. Van Eck M, Berkhof H, Nicolson N, Sulon J (1996) The effects of perceived stress, traits, mood states, and stressful daily events on salivary cortisol. Psychosom Med 58: 447-458
198. Veenema AH (2012) Toward understanding how early-life social experiences alter oxytocin-and vasopressin-regulated social behaviors. Horm Behav 61: 304-312
199. Veenema AH, Neumann ID (2008) Central vasopressin and oxytocin release: regulation of complex social behaviours. Progress Brain Res 170: 261-276
200. Veenema AH, Neumann ID (2009) Maternal separation enhances offensive play-fighting, basal corticosterone and hypothalamic vasopressin mRNA expression in juvenile male rats. Psychoneuroendocrinology 34: 463-467
201. Veenema AH, Blume A, Niederle D, Buwalda B, Neumann ID (2006) Effects of early lide stress on adult male aggression and hypothalamic vasopressin and serotonin. Euro J Neurosci 24: 1711-1720
202. Veenema AH, Bredewold R, Neumann ID (2007) Opposite effects of maternal separation on intermale and maternal aggression in C57BL/6 mice: link to hypothalamic vasopressin and oxytocin immunoreactivity. Psychoneuroendocrinology 32: 437-450
203. Wada H (2008) Glucocorticoids: mediators of vertebrate ontogenetic transitions. Gen Comp Endocrinol 156: 441-453
204. Weaver, IC (2007) Epigenetic programming by maternal behavior and pharmacological intervention. Nature versus nurture: let's call the whole thing off. Epigenetics 2(1): 22-28
205. Wei XY, Yang JY, Dong YX, Wu CF (2007) Anxiolytic-like effects of oleamide in grouphoused and socially isolated mice. Prog Neuropsychopharmacol Biol Psychiatry 31: 1189-1195
206. Weisstaub NV, Zhou M, Lira A, Lambe E, González-Maeso J, Hornung JP, Sibille E, Underwood M, Itohara S, Dauer WT, Ansorge MS (2006) Cortical 5-HT2A receptor signaling modulates anxiety-like behaviors in mice. Science 313(5786): 536-540
207. Weitzdorfer R, Hoger H, Shim KS, Cekici L, Pollak A, Lubec G (2008) Changes of hippocampal signaling protein levels during postnatal brain development in the rat. Hippocampus 18: 807-813
208. 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(2): 293-302
209. Winkelmann-Duarte EC, Todeschin AS, Fernandes MC, Bittencourt LC, Pereira GA, Samios VN, Schuh AF, Achaval ME, Xavier LL, Sanvitto GL, Mandarim-de-Lacerda CA, Lucion AB (2007) Plastic changes induced by neonatal handling in the hypothalamus of female rats. Brain Res 1170: 20-30
210. Yildirim M, Mapp OM, Janssen WGM, Yin WL, Morrison JH, Gore AC (2008) Postpubertal decrease in hippocampal dendritic spines of female rats. Exp Neuro 210: 339-348
211. Yoshimura S, Sakamoto S, Kudo H, Sassa S, Kumai A, Okamoto R (2003) Sex-differences in adrenocortical responsiveness during development in rats. Steroids 68: 439-445
212. Zimmerberg B, Sageser KA (2011) Comparison of two rodent models of maternal separation on juvenile social behavior. Front Psychiatry 2: 39