Stress during development alters anxiety-like behavior and hippocampal neurotransmission in male and female rats

Neuropharmacology

Volumn 62, Issue 1, 2012, Pages 518-526

  Barbosa Neto, Jair B ^a   Tiba, Paula A ^a,b   Faturi, Claudia B ^c   De Castro Neto, Eduardo F ^a   Da Graa Naffah Mazacoratti, Maria ^a   De Jesus Mari, Jair ^a   De Mello, Marcelo F ^a   Suchecki, Deborah ^a  

^a FEDERAL UNIVERSITY OF SÃO PAULO   (Brazil)

^b UNIVERSIDADE FEDERAL DO ABC   (Brazil)

^c UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

Anxiety like behavior; GABA; Hippocampus; HPLC; Maternal deprivation; Stress; Taurine

Indexed keywords

4 AMINOBUTYRIC ACID; AMINO ACID; ASPARTIC ACID; CORTICOSTERONE; GLUTAMIC ACID; MONOAMINE; NEUROTRANSMITTER; NORADRENALIN; TAURINE;

AMINO ACID BRAIN LEVEL; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANXIETY; BEHAVIOR CHANGE; BRAIN LEVEL; CONFERENCE PAPER; CONTROLLED STUDY; CORTICOSTERONE BLOOD LEVEL; CORTICOSTERONE RELEASE; DEVELOPMENTAL STAGE; EMOTION; FEMALE; HIPPOCAMPUS; MALE; MATERNAL DEPRIVATION; MAZE TEST; NEUROTRANSMISSION; NONHUMAN; PERINATAL PERIOD; PRIORITY JOURNAL; PROTEIN DETERMINATION; RAT; RISK ASSESSMENT; SEX DIFFERENCE; STRESS;

AGE FACTORS; ANIMALS; ANIMALS, NEWBORN; ANXIETY; BIOGENIC MONOAMINES; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; CORTICOSTERONE; DISEASE MODELS, ANIMAL; ELECTROCHEMISTRY; FEMALE; HIPPOCAMPUS; MALE; MATERNAL DEPRIVATION; MAZE LEARNING; NEUROTRANSMITTER AGENTS; RATS; RATS, WISTAR; SEX FACTORS; STATISTICS, NONPARAMETRIC; STRESS, PSYCHOLOGICAL; SYNAPTIC TRANSMISSION;

EID: 80054101845     PISSN: 00283908     EISSN: 18737064     Source Type: Journal    
DOI: 10.1016/j.neuropharm.2011.09.011     Document Type: Conference Paper

References (107)

1. O. Agid, B. Shapira, J. Zislin, M. Ritsner, B. Hanin, H. Murad, T. Troudart, M. Bloch, U. Heresco-Levy, and B. Lerer Environment and vulnerability to major psychiatric illness: a case control study of early parental loss in major depression, bipolar disorder and schizophrenia Mol. Psychiatry 4 1999 163 172 (Pubitemid 29163979)
2. J. Albrecht, and A. Schousboe Taurine interaction with neurotransmitter receptors in the CNS: an update Neurochem. Res. 30 2005 1615 1621 (Pubitemid 41813726)
3. A.M. Aloisi, H.L. Steenbergen, N.E. van de Poll, and F. Farabollini Sex-dependent effects of restraint on nociception and pituitary-adrenal hormones in the rat Physiol. Behav. 55 1994 789 793 (Pubitemid 24133790)
4. S.L. Andersen, and M.H. Teicher Stress, sensitive periods and maturational events in adolescent depression Trends Neurosci. 31 2008 183 191
5. S.L. Andersen, A. Tomada, E.S. Vincow, E. Valente, A. Polcari, and M.H. Teicher Preliminary evidence for sensitive periods in the effect of childhood sexual abuse on regional brain development J. Neuropsychiatry Clin. Neurosci. 20 2008 292 301
6. S. Avishai-Eliner, E.E. Gilles, M. Eghbal-Ahmadi, Y. Bar-El, and T.Z. Baram Altered regulation of gene and protein expression of hypothalamic- pituitary-adrenal axis components in an immature rat model of chronic stress J. Neuroendocrinol. 13 2001 799 807 (Pubitemid 32894435)
7. D.M. Bannerman, J.N. Rawlins, S.B. McHugh, R.M. Deacon, B.K. Yee, T. Bast, W.N. Zhang, H.H. Pothuizen, and J. Feldon Regional dissociations within the hippocampus-memory and anxiety Neurosci. Biobehav. Rev. 28 2004 273 283 (Pubitemid 38844376)
8. I. Barna, E. Balint, J. Baranyi, N. Bakos, G.B. Makara, and J. Haller Gender-specific effect of maternal deprivation on anxiety and corticotropin-releasing hormone mRNA expression in rats Brain Res. Bull. 62 2003 85 91 (Pubitemid 37443653)
9. R.J. Blanchard, and D.C. Blanchard Attack and defense in rodents as ethoexperimental models for the study of emotion Prog. Neuropsychopharmacol. Biol. Psychiatry Suppl. 13 1989 S3 S14
10. M.C. Bohn Glucocorticoid induced teratologies of the nervous system J. Yanai, Neurobehavioral Teratology 1984 Elsevier Science Publishers B.V. Amsterdam 365 387
11. M.H. Bureau, and R.W. Olsen Taurine acts on a subclass of GABAA receptors in mammalian brain in vitro Eur. J. Pharmacol. 207 1991 9 16
12. C. Caldji, D. Francis, S. Sharma, P.M. Plotsky, and M.J. Meaney 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 2000 219 229 (Pubitemid 30089532)
13. E.A. Cavalheiro, M.J. Fernandes, L. Turski, and M.G. Naffah-Mazzacoratti Spontaneous recurrent seizures in rats: amino acid and monoamine determination in the hippocampus Epilepsia 35 1994 1 11 (Pubitemid 24074459)
14. S.W. Chen, W.X. Kong, Y.J. Zhang, Y.L. Li, X.J. Mi, and X.S. Mu Possible anxiolytic effects of taurine in the mouse elevated plus-maze Life Sci. 75 2004 1503 1511 (Pubitemid 38887277)
15. F. Cirulli, D. Santucci, G. Laviola, E. Alleva, and S. Levine Behavioral and hormonal responses to stress in the newborn mouse: effects of maternal deprivation and chlordiazepoxide Dev. Psychobiol. 27 1994 301 316
16. R. Corbett, S. Fielding, M. Cornfeldt, and R.W. Dunn GABAmimetic agents display anxiolytic-like effects in the social interaction and elevated plus maze procedures Psychopharmacology (Berl) 104 1991 312 316
17. B.M. Cortese, T.R. Mitchell, M.P. Galloway, K.E. Prevost, J. Fang, G.J. Moore, and T.W. Uhde Region-specific alteration in brain glutamate: possible relationship to risk-taking behavior Physiol. Behav. 99 2010 445 450
18. A.P. Cruz, F. Frei, and F.G. Graeff Ethopharmacological analysis of rat behavior on the elevated plus-maze Pharmacol. Biochem. Behav. 49 1994 171 176 (Pubitemid 24297273)
19. E.R. de Kloet, M. Joels, M. Oitzl, and W. Sutanto Implication of brain corticosteroid receptor diversity for the adaptation syndrome concept Methods Achiev. Exp. Pathol. 14 1991 104 132
20. E.R. De Kloet, G.L. Kovacs, G. Szabo, G. Telegdy, B. Bohus, and D.H. Versteeg Decreased serotonin turnover in the dorsal hippocampus of rat brain shortly after adrenalectomy: selective normalization after corticosterone substitution Brain Res. 239 1982 659 663 (Pubitemid 12116520)
21. M. De la Fuente, A. Hernanz, S. Medina, N. Guayerbas, B. Fernandez, and M.P. Viveros Characterization of monoaminergic systems in brain regions of prematurely ageing mice Neurochem. Int. 43 2003 165 172 (Pubitemid 36287335)
22. G. Dent, D.C. Choi, J.P. Herman, and S. Levine GABAergic circuits and the stress hyporesponsive period in the rat: ontogeny of glutamic acid decarboxylase (GAD) 67 mRNA expression in limbic-hypothalamic stress pathways Brain Res. 1138 2007 1 9 (Pubitemid 46281879)
23. B.A. Donzanti, and B.K. Yamamoto An improved and rapid HPLC-EC method for the isocratic separation of amino acid neurotransmitters from brain tissue and microdialysis perfusates Life Sci. 43 1988 913 922
24. B.A. Donzanti, and B.K. Yamamoto A rapid and simple HPLC microassay for biogenic amines in discrete brain regions Pharmacol. Biochem. Behav. 30 1988 795 799 (Pubitemid 19271171)
25. A. Duchesne, M.M. Dufresne, and R.M. Sullivan Sex differences in corticolimbic dopamine and serotonin systems in the rat and the effect of postnatal handling Prog. Neuropsychopharmacol. Biol. Psychiatry 33 2009 251 261
26. B.A. Ellenbroek, and A.R. Cools Early maternal deprivation and prepulse inhibition: the role of the postdeprivation environment Pharmacol. Biochem. Behav. 73 2002 177 184 (Pubitemid 34667030)
27. B.A. Ellenbroek, N. Derks, and H.J. Park Early maternal deprivation retards neurodevelopment in Wistar rats Stress 8 2005 247 257 (Pubitemid 43163257)
28. B.A. Ellenbroek, F. Sluyter, and A.R. Cools The role of genetic and early environmental factors in determining apomorphine susceptibility Psychopharmacology (Berl) 148 2000 124 131 (Pubitemid 30104133)
29. K. Fabricius, G. Wortwein, and B. Pakkenberg The impact of maternal separation on adult mouse behaviour and on the total neuron number in the mouse hippocampus Brain Struct. Funct. 212 2008 403 416 (Pubitemid 351161499)
30. Y. Fan, J. Zhang, X.L. Sun, L. Gao, X.N. Zeng, J.H. Ding, C. Cao, L. Niu, and G. Hu Sex- and region-specific alterations of basal amino acid and monoamine metabolism in the brain of aquaporin-4 knockout mice J. Neurosci. Res. 82 2005 458 464 (Pubitemid 41579345)
31. C.B. Faturi, P.A. Tiba, S.E. Kawakami, B. Catallani, M. Kerstens, and D. Suchecki Disruptions of the mother-infant relationship and stress-related behaviours: altered corticosterone secretion does not explain everything Neurosci. Biobehav. Rev. 34 2010 821 834
32. C.A. Frye, S.M. Petralia, and M.E. Rhodes Estrous cycle and sex differences in performance on anxiety tasks coincide with increases in hippocampal progesterone and 3alpha,5alpha-THP Pharmacol. Biochem. Behav. 67 2000 587 596 (Pubitemid 32103570)
33. G. Griebel, D.J. Sanger, and G. Perrault The use of the rat elevated plus-maze to discriminate between non-selective and BZ-1 (omega 1) selective, benzodiazepine receptor ligands Psychopharmacology (Berl) 124 1996 245 254
34. V. Gundersen Co-localization of excitatory and inhibitory transmitters in the brain Acta Neurol. Scand. Suppl. 188 2008 29 33 (Pubitemid 351595270)
35. D.J. Haleem, G.A. Kennett, and G. Curzon Hippocampal 5-hydroxytryptamine synthesis is greater in female rats than in males and more decreased by the 5-HT1A agonist 8-OH-DPAT J. Neural Transm. Gen. Sect. 79 1990 93 101 (Pubitemid 20002905)
36. S.L. Halligan, J. Herbert, I. Goodyer, and L. Murray Disturbances in morning cortisol secretion in association with maternal postnatal depression predict subsequent depressive symptomatology in adolescents Biol. Psychiatry 62 2007 40 46 (Pubitemid 46898229)
37. S.L. Halligan, L. Murray, C. Martins, and P.J. Cooper Maternal depression and psychiatric outcomes in adolescent offspring: a 13-year longitudinal study J. Affect Disord. 97 2007 145 154 (Pubitemid 44940819)
38. J.P. Herman, H. Figueiredo, N.K. Mueller, Y. Ulrich-Lai, M.M. Ostrander, D.C. Choi, and W.E. Cullinan Central mechanisms of stress integration: hierarchical circuitry controlling hypothalamo-pituitary-adrenocortical responsiveness Front. Neuroendocrinol. 24 2003 151 180 (Pubitemid 37336539)
39. J.P. Herman, N.K. Mueller, and H. Figueiredo Role of GABA and glutamate circuitry in hypothalamo-pituitary-adrenocortical stress integration Ann. N. Y. Acad. Sci. 1018 2004 35 45 (Pubitemid 38951388)
40. R.L. Huot, P.M. Plotsky, R.H. Lenox, and R.K. McNamara Neonatal maternal separation reduces hippocampal mossy fiber density in adult Long Evans rats Brain Res. 950 2002 52 63 (Pubitemid 35256148)
41. R.L. Huot, K.V. Thrivikraman, M.J. Meaney, and P.M. Plotsky 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 2001 366 373 (Pubitemid 33141312)
42. H. Husum, E. Termeer, A.A. Mathe, T.G. Bolwig, and B.A. Ellenbroek Early maternal deprivation alters hippocampal levels of neuropeptide Y and calcitonin-gene related peptide in adult rats Neuropharmacology 42 2002 798 806 (Pubitemid 34518280)
43. A. Iwasaki-Sekino, A. Mano-Otagiri, H. Ohata, N. Yamauchi, and T. Shibasaki Gender differences in corticotropin and corticosterone secretion and corticotropin-releasing factor mRNA expression in the paraventricular nucleus of the hypothalamus and the central nucleus of the amygdala in response to footshock stress or psychological stress in rats Psychoneuroendocrinology 34 2009 226 237
44. D.C. Javitt Glutamate as a therapeutic target in psychiatric disorders Mol. Psychiatry 9 2004 984 997 979 (Pubitemid 39524288)
45. M. Kalinichev, K.W. Easterling, P.M. Plotsky, and S.G. Holtzman Long-lasting changes in stress-induced corticosterone response and anxiety-like behaviors as a consequence of neonatal maternal separation in Long-Evans rats Pharmacol. Biochem. Behav. 73 2002 131 140 (Pubitemid 34667025)
46. S.F. Kash, L.H. Tecott, C. Hodge, and S. Baekkeskov Increased anxiety and altered responses to anxiolytics in mice deficient in the 65-kDa isoform of glutamic acid decarboxylase Proc. Natl. Acad. Sci. U. S. A. 96 1999 1698 1703 (Pubitemid 29098514)
47. K.S. Kendler, K. Sheth, C.O. Gardner, and C.A. Prescott Childhood parental loss and risk for first-onset of major depression and alcohol dependence: the time-decay of risk and sex differences Psychol. Med. 32 2002 1187 1194 (Pubitemid 35243976)
48. R.C. Kessler, C.G. Davis, and K.S. Kendler Childhood adversity and adult psychiatric disorder in the US National Comorbidity Survey Psychol. Med. 27 1997 1101 1119 (Pubitemid 27401833)
49. R.C. Kessler, and W.J. Magee Childhood adversities and adult depression: basic patterns of association in a US national survey Psychol. Med. 23 1993 679 690 (Pubitemid 23268086)
50. W.X. Kong, S.W. Chen, Y.L. Li, Y.J. Zhang, R. Wang, L. Min, and X. Mi Effects of taurine on rat behaviors in three anxiety models Pharmacol. Biochem. Behav. 83 2006 271 276
51. K.M. Landman-Peeters, J. Ormel, E.L. Van Sonderen, J.A. Den Boer, R.B. Minderaa, and C.A. Hartman Risk of emotional disorder in offspring of depressed parents: gender differences in the effect of a second emotionally affected parent Depress Anxiety 25 2008 653 660
52. M.L. Leret, M. Lecumberri, M. Garcia-Montojo, and J.C. Gonzalez Role of maternal corticosterone in the development and maturation of the aminoacidergic systems of the rat brain Int. J. Dev. Neurosci. 25 2007 465 471 (Pubitemid 350086843)
53. S. Levine Primary social relationships influence the development of the hypothalamic-pituitary-adrenal axis in the rat Physiol. Behav. 73 2001 255 260 (Pubitemid 32595698)
54. S. Levine, D.M. Huchton, S.G. Wiener, and P. Rosenfeld Time course of the effect of maternal deprivation on the hypothalamic-pituitary-adrenal axis in the infant rat Dev. Psychobiol. 24 1991 547 558
55. R. Llorente, L. Arranz, E.M. Marco, E. Moreno, M. Puerto, C. Guaza, M. De la Fuente, and M.P. Viveros Early maternal deprivation and neonatal single administration with a cannabinoid agonist induce long-term sex-dependent psychoimmunoendocrine effects in adolescent rats Psychoneuroendocrinology 32 2007 636 650 (Pubitemid 47018322)
56. R. Llorente, E. O'Shea, M.D. Gutierrez-Lopez, A. Llorente-Berzal, M.I. Colado, and M.P. Viveros Sex-dependent maternal deprivation effects on brain monoamine content in adolescent rats Neurosci. Lett. 479 2010 112 117
57. A. Maercker, T. Michael, L. Fehm, E.S. Becker, and J. Margraf Age of traumatisation as a predictor of post-traumatic stress disorder or major depression in young women Br. J. Psychiatry 184 2004 482 487 (Pubitemid 38725707)
58. F.K. Marcondes, K.J. Miguel, L.L. Melo, and R.C. Spadari-Bratfisch Estrous cycle influences the response of female rats in the elevated plus-maze test Physiol. Behav. 74 2001 435 440 (Pubitemid 34076588)
59. B.S. McEwen, E.A. Gould, and R.R. Sakai The vulnerability of the hippocampus to protective and destructive effects of glucocorticoids in relation to stress Br. J. Psychiatry Suppl. 1992 18 23
60. J.H. Medina, and E. De Robertis Taurine modulation of the benzodiazepine-gamma-aminobutyric acid receptor complex in brain membranes J. Neurochem. 42 1984 1212 1217 (Pubitemid 14137599)
61. S.S. Oja, and P. Saransaari Modulation of taurine release by glutamate receptors and nitric oxide Prog. Neurobiol. 62 2000 407 425 (Pubitemid 30336475)
62. C.A. Oomen, C.E. Girardi, R. Cahyadi, E.C. Verbeek, H. Krugers, M. Joels, and P.J. Lucassen Opposite effects of early maternal deprivation on neurogenesis in male versus female rats PLoS One 4 2009 e3675
63. C.A. Oomen, H. Soeters, N. Audureau, L. Vermunt, F.N. van Hasselt, E.M. Manders, M. Joels, H. Krugers, and P.J. Lucassen Early maternal deprivation affects dentate gyrus structure and emotional learning in adult female rats Psychopharmacology (Berl) 214 2011 249 260
64. C.A. Oomen, H. Soeters, N. Audureau, L. Vermunt, F.N. van Hasselt, E.M. Manders, M. Joels, P.J. Lucassen, and H. Krugers Severe early life stress hampers spatial learning and neurogenesis, but improves hippocampal synaptic plasticity and emotional learning under high-stress conditions in adulthood J. Neurosci. 30 2010 6635 6645
65. Z. Penke, K. Felszeghy, B. Fernette, D. Sage, C. Nyakas, and A. Burlet Postnatal maternal deprivation produces long-lasting modifications of the stress response, feeding and stress-related behaviour in the rat Eur. J. Neurosci. 14 2001 747 755 (Pubitemid 34626001)
66. P.M. Plotsky, and M.J. Meaney 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 1993 195 200
67. S.L. Rees, M. Steiner, and A.S. Fleming Early deprivation, but not maternal separation, attenuates rise in corticosterone levels after exposure to a novel environment in both juvenile and adult female rats Behav. Brain Res. 175 2006 383 391 (Pubitemid 44750243)
68. G. Rentesi, K. Antoniou, M. Marselos, A. Fotopoulos, J. Alboycharali, and M. Konstandi Long-term consequences of early maternal deprivation in serotonergic activity and HPA function in adult rat Neurosci. Lett. 480 2010 7 11
69. M. Roceri, W. Hendriks, G. Racagni, B.A. Ellenbroek, and M.A. Riva Early maternal deprivation reduces the expression of BDNF and NMDA receptor subunits in rat hippocampus Mol. Psychiatry 7 2002 609 616
70. R.J. Rodgers, B.J. Cao, A. Dalvi, and A. Holmes Animal models of anxiety: an ethological perspective Braz. J. Med. Biol. Res. 30 1997 289 304 (Pubitemid 127521025)
71. R.J. Rodgers, and A. Dalvi Anxiety, defence and the elevated plus-maze Neurosci. Biobehav. Rev. 21 1997 801 810 (Pubitemid 27524775)
72. R.J. Rodgers, and N.J. Johnson Factor analysis of spatiotemporal and ethological measures in the murine elevated plus-maze test of anxiety Pharmacol. Biochem. Behav. 52 1995 297 303
73. P. Rosenfeld, J. Ekstrand, E. Olson, D. Suchecki, and S. Levine Maternal regulation of adrenocortical activity in the infant rat: effects of feeding Dev. Psychobiol. 26 1993 261 277
74. P. Rosenfeld, Y.A. Gutierrez, A.M. Martin, H.A. Mallett, E. Alleva, and S. Levine Maternal regulation of the adrenocortical response in preweanling rats Physiol. Behav. 50 1991 661 671
75. P. Rosenfeld, J.B. Wetmore, and S. Levine Effects of repeated maternal separations on the adrenocortical response to stress of preweanling rats Physiol. Behav. 52 1992 787 791
76. N.Y. Rots, J. de Jong, J.O. Workel, S. Levine, A.R. Cools, and E.R. De Kloet Neonatal maternally deprived rats have as adults elevated basal pituitary-adrenal activity and enhanced susceptibility to apomorphine J. Neuroendocrinol. 8 1996 501 506 (Pubitemid 26239717)
77. V. Roy, and P. Chapillon Further evidences that risk assessment and object exploration behaviours are useful to evaluate emotional reactivity in rodents Behav. Brain Res. 154 2004 439 448 (Pubitemid 39093994)
78. M. Schmidt, L. Enthoven, J.H. van Woezik, S. Levine, E.R. de Kloet, and M.S. Oitzl The dynamics of the hypothalamic-pituitary-adrenal axis during maternal deprivation J. Neuroendocrinol. 16 2004 52 57 (Pubitemid 38159393)
79. A. Schoedl, M.C.P. Costa, A.R. Tyrka, L.L. Carpenter, L.H. Price, J.J. Mar, and M.F. Mello The clinical correlates of reported childhood sexual abuse: an association between age at trauma onset and severity of depression and PTSD in adults J. Child Sex. Abuse Aceito 2008
80. J.V. Seale, S.A. Wood, H.C. Atkinson, E. Bate, S.L. Lightman, C.D. Ingram, D.S. Jessop, and M.S. Harbuz Gonadectomy reverses the sexually diergic patterns of circadian and stress-induced hypothalamic-pituitary-adrenal axis activity in male and female rats J. Neuroendocrinol. 16 2004 516 524 (Pubitemid 38878283)
81. J. Setem, A.P. Pinheiro, V.A. Motta, S. Morato, and A.P. Cruz Ethopharmacological analysis of 5-HT ligands on the rat elevated plus-maze Pharmacol. Biochem. Behav. 62 1999 515 521 (Pubitemid 29117195)
82. G.S. Severino, I.A. Fossati, M.J. Padoin, C.M. Gomes, L. Trevizan, G.L. Sanvitto, C.R. Franci, J.A. Anselmo-Franci, and A.B. Lucion 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 2004 489 498 (Pubitemid 38591538)
83. M.E. Stanton, and S. Levine Inhibition of infant glucocorticoid stress response: specific role of maternal cues Dev. Psychobiol. 23 1990 411 426 (Pubitemid 20368142)
84. T.L. Sterley, F.M. Howells, and V.A. Russell Effects of early life trauma are dependent on genetic predisposition: a rat study Behav. Brain Funct. 7 2011 11
85. O. Stork, F.Y. Ji, K. Kaneko, S. Stork, Y. Yoshinobu, T. Moriya, S. Shibata, and K. Obata Postnatal development of a GABA deficit and disturbance of neural functions in mice lacking GAD65 Brain Res. 865 2000 45 58 (Pubitemid 30256206)
86. D. Suchecki, B. Duarte Palma, and S. Tufik Pituitary-adrenal axis and behavioural responses of maternally deprived juvenile rats to the open field Behav. Brain Res. 111 2000 99 106 (Pubitemid 30326706)
87. D. Suchecki, D. Mozaffarian, G. Gross, P. Rosenfeld, and S. Levine Effects of maternal deprivation on the ACTH stress response in the infant rat Neuroendocrinology 57 1993 204 212 (Pubitemid 23147800)
88. D. Suchecki, D.Y. Nelson, H. Van Oers, and S. Levine Activation and inhibition of the hypothalamic-pituitary-adrenal axis of the neonatal rat: effects of maternal deprivation Psychoneuroendocrinology 20 1995 169 182 (Pubitemid 24366198)
89. D. Suchecki, P. Rosenfeld, and S. Levine Maternal regulation of the hypothalamic-pituitary-adrenal axis in the infant rat: the roles of feeding and stroking Brain Res. Dev. Brain Res. 75 1993 185 192 (Pubitemid 23293568)
90. D. Suchecki, P.A. Tiba, and S. Tufik Hormonal and behavioural responses of paradoxical sleep-deprived rats to the elevated plus maze J. Neuroendocrinol. 14 2002 549 554 (Pubitemid 34679217)
91. D. Suchecki, and S. Tufik Long-term effects of maternal deprivation on the corticosterone response to stress in rats Am. J. Physiol. 273 1997 R1332 R1338
92. M.H. Teicher, A. Tomoda, and S.L. Andersen Neurobiological consequences of early stress and childhood maltreatment: are results from human and animal studies comparable? Ann. N. Y. Acad. Sci. 1071 2006 313 323 (Pubitemid 44126738)
93. K.V. Thrivikraman, Y. Su, and P.M. Plotsky Patterns of Fos-immunoreactivity in the CNS induced by repeated hemorrhage in conscious rats: correlations with pituitary-adrenal axis activity Stress 2 1997 145 158 (Pubitemid 28140984)
94. H.J. van Oers, E.R. de Kloet, and S. Levine Early vs. late maternal deprivation differentially alters the endocrine and hypothalamic responses to stress Brain Res. Dev. Brain Res. 111 1998 245 252 (Pubitemid 28561730)
95. H.J. van Oers, E.R. de Kloet, T. Whelan, and S. Levine Maternal deprivation effect on the infant's neural stress markers is reversed by tactile stimulation and feeding but not by suppressing corticosterone J. Neurosci. 18 1998 10171 10179 (Pubitemid 28543790)
96. D.M. Vazquez, C. Bailey, G.W. Dent, D.K. Okimoto, A. Steffek, J.F. Lopez, and S. Levine Brain corticotropin-releasing hormone (CRH) circuits in the developing rat: effect of maternal deprivation Brain Res. 1121 2006 83 94 (Pubitemid 44708896)
97. P. Verma, K.G. Hellemans, F.Y. Choi, W. Yu, and J. Weinberg Circadian phase and sex effects on depressive/anxiety-like behaviors and HPA axis responses to acute stress Physiol. Behav. 99 2010 276 285
98. M. Vijayakumar, and B.L. Meti Alterations in the levels of monoamines in discrete brain regions of clomipramine-induced animal model of endogenous depression Neurochem. Res. 24 1999 345 349 (Pubitemid 29072042)
99. C.D. Walker, K.A. Scribner, C.S. Cascio, and M.F. Dallman The pituitary-adrenocortical system of neonatal rats is responsive to stress throughout development in a time-dependent and stressor-specific fashion Endocrinology 128 1991 1385 1395
100. S.M. Weiss, G. Wadsworth, A. Fletcher, and C.T. Dourish Utility of ethological analysis to overcome locomotor confounds in elevated maze models of anxiety Neurosci. Biobehav. Rev. 23 1998 265 271 (Pubitemid 29011628)
101. B.K. Whirley, and H. Einat Taurine trials in animal models offer no support for anxiolytic, antidepressant or stimulant effects Isr. J. Psychiatry Relat. Sci. 45 2008 11 18
102. C.P. Wiedenmayer Adaptations or pathologies? Long-term changes in brain and behavior after a single exposure to severe threat Neurosci. Biobehav. Rev. 28 2004 1 12 (Pubitemid 38224448)
103. L. Witek-Janusek Pituitary-adrenal response to bacterial endotoxin in developing rats Am. J. Physiol. 255 1988 E525 E530
104. R. Yehuda, A. Bell, L.M. Bierer, and J. Schmeidler Maternal, not paternal, PTSD is related to increased risk for PTSD in offspring of Holocaust survivors J. Psychiatr. Res. 42 2008 1104 1111
105. R. Yehuda, S.L. Halligan, and L.M. Bierer Relationship of parental trauma exposure and PTSD to PTSD, depressive and anxiety disorders in offspring J. Psychiatr. Res. 35 2001 261 270 (Pubitemid 32928427)
106. M.L.S. Zavaschi, F. Satler, D. Poester, C.F. Vargas, R. Piazenski, L.A.P. Rohde, and C.L. Eizirik Association between childhood loss trauma and depression in adulthood Rev. Bras. Psiquiatr. 24 2002 189 195
107. C.G. Zhang, and S.J. Kim Taurine induces anti-anxiety by activating strychnine-sensitive glycine receptor in vivo Ann. Nutr. Metab. 51 2007 379 386 (Pubitemid 47442981)