Prenatal stressors in rodents: Effects on behavior

Neurobiology of Stress

Volumn 6, Issue , 2017, Pages 3-13

  Weinstock, Marta ^a  

^a HADASSAH HEBREW UNIVERSITY MEDICAL CENTER   (Israel)

Author keywords

Anxiety and depressive like behavior; BDNF; Epigenetic mechanisms; Glutamate receptors; Memory; Social interaction

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; GLUTAMATE RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2B; SEROTONIN;

ANXIETY; CORTICOSTERONE BLOOD LEVEL; DEPRESSION; ELEVATED PLUS MAZE TEST; EPIGENETICS; FORCED SWIM TEST; HUMAN; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; LEARNING DISORDER; MATERNAL STRESS; MORRIS WATER MAZE TEST; NEUROCHEMISTRY; NONHUMAN; OPEN FIELD TEST; PRENATAL STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; RECOGNITION; REVIEW; RODENT; SCHIZOPHRENIA; SOCIAL INTERACTION; SPATIAL LEARNING; SPATIAL MEMORY; SUCROSE PREFERENCE TEST;

EID: 85009160421     PISSN: None     EISSN: 23522895     Source Type: Journal    
DOI: 10.1016/j.ynstr.2016.08.004     Document Type: Review

References (170)

1. Abe, H., Hidaka, N., Kawagoe, C., Odagiri, K., Watanabe, Y., et al. Prenatal psychological stress causes higher emotionality, depression-like behavior, and elevated activity in the hypothalamo-pituitary-adrenal axis. Neurosci. Res. 59 (2007), 145–151.
2. Akatsu, S., Ishikawa, C., Takemura, K., Ohtani, A., Shiga, T., Effects of prenatal stress and neonatal handling on anxiety, spatial learning and serotonergic system of male offspring mice. Neurosci. Res. 101 (2015), 15–23.
3. Asztely, F., Gustafsson, B., Ionotropic glutamate receptors. Their possible role in the expression of hippocampal synaptic plasticity. Mol. Neurobiol. 12 (1996), 1–11.
4. Austin, K.B., Bronzino, J., Morgane, P.J., Prenatal protein malnutrition affects synaptic potentiation in the dentate gyrus of rats in adulthood. Brain Res. 394 (1986), 267–273.
5. Autry, A.E., Monteggia, L.M., Brain-derived neurotrophic factor and neuropsychiatric disorders. Pharmacol. Rev. 64 (2012), 238–258.
6. Azmitia, E.C., Segal, M., An autoradiographic analysis of the differential ascending projections of the dorsal and median raphe nuclei in the rat. J. Comp. Neurol. 179 (1978), 641–667.
7. Baker, S., Chebli, M., Rees, S., Lemarec, N., Godbout, R., et al. Effects of gestational stress: 1. Evaluation of maternal and juvenile offspring behavior. Brain Res. 1213 (2008), 98–110.
8. Baker, S., Rees, S., Chebli, M., Lemarec, N., Godbout, R., et al. Effects of gestational stress: 2. Evaluation of male and female adult offspring. Brain Res. 1302 (2009), 194–204.
9. Barbazanges, A., Piazza, P.V., Le Moal, M., Maccari, S., Maternal glucocorticoid secretion mediates long-term effects of prenatal stress. J. Neurosci. 16 (1996), 3943–3949.
10. Barros, V.G., Rodriguez, P., Martijena, I.D., Perez, A., Molina, V.A., et al. Prenatal stress and early adoption effects on benzodiazepine receptors and anxiogenic behavior in the adult rat brain. Synapse 60 (2006), 609–618.
11. Barzegar, M., Sajjadi, F.S., Talaei, S.A., Hamidi, G., Salami, M., Prenatal exposure to noise stress: anxiety, impaired spatial memory, and deteriorated hippocampal plasticity in postnatal life. Hippocampus 25 (2015), 187–196.
12. Bauer, E.P., Schafe, G.E., LeDoux, J.E., NMDA receptors and L-type voltage-gated calcium channels contribute to long-term potentiation and different components of fear memory formation in the lateral amygdala. J. Neurosci. 22 (2002), 5239–5249.
13. Bayer, S.A., Altman, J., Russo, R.J., Zhang, X., Timetables of neurogenesis in the human brain based on experimentally determined patterns in the rat. Neurotoxicology 14 (1993), 83–144.
14. Benoit, J.D., Rakic, P., Frick, K.M., Prenatal stress induces spatial memory deficits and epigenetic changes in the hippocampus indicative of heterochromatin formation and reduced gene expression. Behav. Brain Res. 281 (2015), 1–8.
15. Berridge, C.W., Waterhouse, B.D., The locus coeruleus-noradrenergic system: modulation of behavioral state and state-dependent cognitive processes. Brain Res. Brain Res. Rev. 42 (2003), 33–84.
16. Biala, Y.N., Bogoch, Y., Bejar, C., Linial, M., Weinstock, M., Prenatal stress diminishes gender differences in behavior and in expression of hippocampal synaptic genes and proteins in rats. Hippocampus 21 (2011), 1114–1125.
17. Bibel, M., Barde, Y.A., Neurotrophins: key regulators of cell fate and cell shape in the vertebrate nervous system. Genes Dev. 14 (2000), 2919–2937.
18. Bourke, C.H., Stowe, Z.N., Neigh, G.N., Olson, D.E., Owens, M.J., Prenatal exposure to escitalopram and/or stress in rats produces limited effects on endocrine, behavioral, or gene expression measures in adult male rats. Neurotoxicol. Teratol. 39 (2013), 100–109.
19. Bramham, C.R., Bacher-Svendsen, K., Sarvey, J.M., LTP in the lateral perforant path is beta-adrenergic receptor-dependent. Neuroreport 8 (1997), 719–724.
20. Brown, A.S., Susser, E.S., Butler, P.D., Richardson Andrews, R., Kaufmann, C.A., et al. Neurobiological plausibility of prenatal nutritional deprivation as a risk factor for schizophrenia. J. Nerv. Ment. Dis. 184 (1996), 71–85.
21. Brunton, P.J., Russell, J.A., Prenatal social stress in the rat programmes neuroendocrine and behavioural responses to stress in the adult offspring: sex-specific effects. J. Neuroendocrinol. 22 (2010), 258–271.
22. Butkevich, I., Mikhailenko, V., Vershinina, E., Semionov, P., Makukhina, G., et al. Maternal buspirone protects against the adverse effects of in utero stress on emotional and pain-related behaviors in offspring. Physiol. Behav. 102 (2011), 137–142.
23. Buynitsky, T., Mostofsky, D.I., Restraint stress in biobehavioral research: recent developments. Neurosci. Biobehav. Rev. 33 (2009), 1089–1098.
24. Caldji, C., Tannenbaum, B., Sharma, S., Francis, D., Plotsky, P.M., Meaney, M.J., 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 (1998), 5335–5340.
25. Carini, L.M., Nephew, B.C., Effects of early life social stress on endocrinology, maternal behavior, and lactation in rats. Horm. Behav. 64 (2013), 634–641.
26. Charil, A., Laplante, D.P., Vaillancourt, C., King, S., Prenatal stress and brain development. Brain Res. Rev. 65 (2010), 56–79.
27. Choe, H.K., Son, G.H., Chung, S., Kim, M., Sun, W., et al. Maternal stress retards fetal development in mice with transcriptome-wide impact on gene expression profiles of the limb. Stress Int. J. Biol. Stress 14 (2011), 194–204.
28. Crosio, C., Heitz, E., Allis, C.D., Borrelli, E., Sassone-Corsi, P., Chromatin remodeling and neuronal response: multiple signaling pathways induce specific histone H3 modifications and early gene expression in hippocampal neurons. J. Cell Sci. 116 (2003), 4905–4914.
29. Davis, E.P., Pfaff, D., Sexually dimorphic responses to early adversity: implications for affective problems and autism spectrum disorder. Psychoneuroendocrinology 49 (2014), 11–25.
30. Davis, E.P., Sandman, C.A., Prenatal psychobiological predictors of anxiety risk in preadolescent children. Psychoneuroendocrinology 37 (2012), 1224–1233.
31. de Souza, M.A., Centenaro, L.A., Menegotto, P.R., Henriques, T.P., Bonini, J., et al. Prenatal stress produces social behavior deficits and alters the number of oxytocin and vasopressin neurons in adult rats. Neurochem. Res. 38 (2013), 1479–1489.
32. Debanne, D., Daoudal, G., Sourdet, V., Russier, M., Brain plasticity and ion channels. J. Physiol. Paris 97 (2003), 403–414.
33. Dhabhar, F.S., McEwen, B.S., Spencer, R.L., Adaptation to prolonged or repeated stress–comparison between rat strains showing intrinsic differences in reactivity to acute stress. Neuroendocrinology 65 (1997), 360–368.
34. Dong, E., Dzitoyeva, S.G., Matrisciano, F., Tueting, P., Grayson, D.R., et al. Brain-derived neurotrophic factor epigenetic modifications associated with schizophrenia-like phenotype induced by prenatal stress in mice. Biol. Psychiatry 77 (2015), 589–596.
35. Drevets, W.C., Thase, M.E., Moses-Kolko, E.L., Price, J., Frank, E., Kupfer, D.J., et al. Serotonin-1A receptor imaging in recurrent depression: replication and literature review. Nucl. Med. Biol. 34 (2007), 865–877.
36. Ehrlich, D.E., Rainnie, D.G., Prenatal stress alters the development of socioemotional behavior and amygdala neuron excitability in rats. Neuropsychopharmacology 40 (2015), 2135–2145.
37. Ennaceur, A., Delacour, J., A new one-trial test for neurobiological studies of memory in rats. 1: behavioral data. Behav. Brain Res. 31 (1988), 47–59.
38. Ennaceur, A., Michalikova, S., Bradford, A., Ahmed, S., Detailed analysis of the behavior of Lister and Wistar rats in anxiety, object recognition and object location tasks. Behav. Brain Res. 159 (2005), 247–266.
39. Erdtsieck-Ernste, E.B., Feenstra, M.G., Botterblom, M.H., Boer, G.J., Developmental changes in rat brain monoamine metabolism and beta-adrenoceptor subtypes after chronic prenatal exposure to propranolol. Neurochem. Int. 22 (1993), 589–598.
40. Felten, D.L., Hallman, H., Jonsson, G., Evidence for a neurotropic role of noradrenaline neurons in the postnatal development of rat cerebral cortex. J. Neurocytol. 11 (1982), 119–135.
41. Fineberg, A.M., Ellman, L.M., Schaefer, C.A., Maxwell, S.D., Shen, L., et al. Fetal exposure to maternal stress and risk for schizophrenia spectrum disorders among offspring: differential influences of fetal sex. Psychiatry Res. 236 (2016), 91–97.
42. Flores, O., Perez, H., Valladares, L., Morgan, C., Gatica, A., et al. Hidden prenatal malnutrition in the rat: role of beta(1)-adrenoceptors on synaptic plasticity in the frontal cortex. J. Neurochem. 119 (2011), 314–323.
43. Fride, E., Dan, Y., Feldon, J., Halevy, G., Weinstock, M., Effects of prenatal stress on vulnerability to stress in prepubertal and adult-rats. Physiol. Behav. 37 (1986), 681–687.
44. Fride, E., Weinstock, M., The effects of prenatal exposure to predictable or unpredictable stress on early development in the rat. Dev. Psychobiol. 17 (1984), 651–660.
45. Fride, E., Weinstock, M., Prenatal stress increases anxiety related behavior and alters cerebral lateralization of dopamine activity. Life Sci. 42 (1988), 1059–1065.
46. Fujioka, T., Sakata, Y., Yamaguchi, K., Shibasaki, T., Kato, H., et al. The effects of prenatal stress on the development of hypothalamic paraventricular neurons in fetal rats. Neuroscience 92 (1999), 1079–1088.
47. Fujita, S., Ueki, S., Miyoshi, M., Watanabe, T., “Green odor” inhalation by stressed rat dams reduces behavioral and neuroendocrine signs of prenatal stress in the offspring. Horm. Behav. 58 (2010), 264–272.
48. Garber, J., Weersing, V.R., Comorbidity of anxiety and depression in youth: implications for treatment and prevention. Clin. Psychol. N.Y. 17 (2010), 293–306.
49. Gerardin, D.C.C., Pereira, O.C.M., Kempinas, W.G., Florio, J.C., Moreira, E.G., et al. Sexual behavior, neuroendocrine, and neurochemical aspects in male rats exposed prenatally to stress. Physiol. Behav. 84 (2005), 97–104.
50. Glombik, K., Stachowicz, A., Slusarczyk, J., Trojan, E., Budziszewska, B., et al. Maternal stress predicts altered biogenesis and the profile of mitochondrial proteins in the frontal cortex and hippocampus of adult offspring rats. Psychoneuroendocrinology 60 (2015), 151–162.
51. Goelman, G., Ilinca, R., Zohar, I., Weinstock, M., Functional connectivity in prenatally stressed rats with and without maternal treatment with ladostigil, a brain-selective monoamine oxidase inhibitor. Eur. J. Neurosci. 40 (2014), 2734–2743.
52. Golub, Y., Fabio, C., Funke, R., Frey, S., Distler, J., et al. Effects of in-utero environment and maternal behaviour on neuroendocrine and behavioural alterations in a mouse model of prenatal trauma. Dev Neurobiol., 2016.
53. Graignic-Philippe, R., Dayan, J., Chokron, S., Jacquet, A.Y., Tordjman, S., Effects of prenatal stress on fetal and child development: a critical literature review. Neurosci. Biobehav. Rev. 43 (2014), 137–162.
54. Grayson, D.R., Guidotti, A., The dynamics of DNA methylation in schizophrenia and related psychiatric disorders. Neuropsychopharmacology 38 (2013), 138–166.
55. Grigoryan, G., Segal, M., Prenatal stress alters noradrenergic modulation of LTP in hippocampal slices. J. Neurophysiol. 110 (2013), 279–285.
56. Grizenko, N., Fortier, M.E., Zadorozny, C., Thakur, G., Schmitz, N., et al. Maternal stress during pregnancy, ADHD symptomatology in children and genotype: gene-environment interaction. J. Can. Acad. Child. Adolesc. Psychiatry 21 (2012), 9–15.
57. Guan, L., Jia, N., Zhao, X., Zhang, X., Tang, G., et al. The involvement of ERK/CREB/Bcl-2 in depression-like behavior in prenatally stressed offspring rats. Brain Res. Bull. 99 (2013), 1–8.
58. Handley, S.L., Mithani, S., Effects of alpha-adrenoceptor agonists and antagonists in a maze-exploration model of ‘fear'-motivated behaviour. Naunyn Schmiedeb. Arch. Pharmacol. 327 (1984), 1–5.
59. Harrison, P.J., The hippocampus in schizophrenia: a review of the neuropathological evidence and its pathophysiological implications. Psychopharmacol. Berl. 174 (2004), 151–162.
60. Heckers, S., Konradi, C., Hippocampal pathology in schizophrenia. Curr. Top. Behav. Neurosci. 4 (2010), 529–553.
61. Henry, C., Kabbaj, M., Simon, H., Le Moal, M., Maccari, S., Prenatal stress increases the hypothalamo-pituitary-adrenal axis response in young and adult rats. J. Neuroendocrinol. 6 (1994), 341–345.
62. Hogg, S., A review of the validity and variability of the elevated plus-maze as an animal model of anxiety. Pharmacol. Biochem. Behav. 54 (1996), 21–30.
63. Huizink, A.C., Mulder, E.J., Buitelaar, J.K., Prenatal stress and risk for psychopathology: specific effects or induction of general susceptibility?. Psychol. Bull. 130 (2004), 115–142.
64. Ikegame, T., Bundo, M., Murata, Y., Kasai, K., Kato, T., et al. DNA methylation of the BDNF gene and its relevance to psychiatric disorders. J. Hum. Genet. 58 (2013), 434–438.
65. Imhof, J.T., Coelho, Z.M., Schmitt, M.L., Morato, G.S., Carobrez, A.P., Influence of gender and age on performance of rats in the elevated plus maze apparatus. Behav. Brain Res. 56 (1993), 177–180.
66. Jenkins, J.A., Williams, P., Kramer, G.L., Davis, L.L., Petty, F., The influence of gender and the estrous cycle on learned helplessness in the rat. Biol. Psychol. 58 (2001), 147–158.
67. Jia, N., Li, Q., Sun, H., Song, Q., Tang, G., et al. Alterations of group I mGluRs and BDNF associated with behavioral abnormity in prenatally stressed offspring rats. Neurochem. Res. 40 (2015), 1074–1082.
68. Khashan, A.S., Abel, K.M., McNamee, R., Pedersen, M.G., Webb, R.T., et al. Higher risk of offspring schizophrenia following antenatal maternal exposure to severe adverse life events. Arch. Gen. Psychiatry 65 (2008), 146–152.
69. Kinney, D.K., Munir, K.M., Crowley, D.J., Miller, A.M., Prenatal stress and risk for autism. Neurosci. Biobehav. Rev. 32 (2008), 1519–1532.
70. Kinsley, C., Svare, B., Prenatal stress effects: are they mediated by reductions in maternal food and water intake and body weight gain?. Physiol. Behav. 37 (1986), 191–193.
71. Kirkpatrick, B., Fenton, W.S., Carpenter, W.T. Jr., Marder, S.R., The NIMH-MATRICS consensus statement on negative symptoms. Schizophr. Bull. 32 (2006), 214–219.
72. Kiryanova, V., Meunier, S.J., Vecchiarelli, H.A., Hill, M.N., Dyck, R.H., Effects of maternal stress and perinatal fluoxetine exposure on behavioral outcomes of adult male offspring. Neuroscience 320 (2016), 281–296.
73. Konradi, C., Heckers, S., Molecular aspects of glutamate dysregulation: implications for schizophrenia and its treatment. Pharmacol. Ther. 97 (2003), 153–179.
74. Laloux, C., Mairesse, J., Van Camp, G., Giovine, A., Branchi, I., Bouret, S., Morley-Fletcher, S., Bergonzelli, G., Malagodi, M., Gradini, R., Nicoletti, F., Darnaudery, M., Maccari, S., Anxiety-like behaviour and associated neurochemical and endocrinological alterations in male pups exposed to prenatal stress. Psychoneuroendocrinology 37:10 (2012), 1646–1658.
75. Laplante, D.P., Brunet, A., Schmitz, N., Ciampi, A., King, S., Project ice storm: prenatal maternal stress affects cognitive and linguistic functioning in 51/2-year-old children. J. Am. Acad. Child Adolesc. Psychiatry 47 (2008), 1063–1072.
76. Lee, P.R., Brady, D.L., Shapiro, R.A., Dorsa, D.M., Koenig, J.I., Prenatal stress generates deficits in rat social behavior: reversal by oxytocin. Brain Res. 1156 (2007), 152–167.
77. Lesage, J., Del-Favero, F., Leonhardt, M., Louvart, H., Maccari, S., et al. Prenatal stress induces intrauterine growth restriction and programmes glucose intolerance and feeding behaviour disturbances in the aged rat. J. Endocrinol. 181 (2004), 291–296.
78. Levenson, J.M., Sweatt, J.D., Epigenetic mechanisms in memory formation. Nat. Rev. Neurosci. 6 (2005), 108–118.
79. Levine, S.Z., Levav, I., Goldberg, Y., Pugachova, I., Becher, Y., et al. Exposure to genocide and the risk of schizophrenia: a population-based study. Psychol. Med. 46 (2016), 855–863.
80. Li, J., Olsen, J., Vestergaard, M., Obel, C., Attention-deficit/hyperactivity disorder in the offspring following prenatal maternal bereavement: a nationwide follow-up study in Denmark. Eur. Child. Adolesc. Psychiatry 19 (2010), 747–753.
81. Liu, F., Day, M., Muniz, L.C., Bitran, D., Arias, R., et al. Activation of estrogen receptor-beta regulates hippocampal synaptic plasticity and improves memory. Nat. Neurosci. 11 (2008), 334–343.
82. Lui, C.C., Wang, J.Y., Tain, Y.L., Chen, Y.C., Chang, K.A., et al. Prenatal stress in rat causes long-term spatial memory deficit and hippocampus MRI abnormality: differential effects of postweaning enriched environment. Neurochem. Int. 58 (2011), 434–441.
83. Luoni, A., Berry, A., Calabrese, F., Capoccia, S., Bellisario, V., et al. Delayed BDNF alterations in the prefrontal cortex of rats exposed to prenatal stress: preventive effect of lurasidone treatment during adolescence. Eur. Neuropsychopharmacol. 24 (2014), 986–995.
84. Lynch, M.R., Schizophrenia and the D1 receptor: focus on negative symptoms. Prog. Neuropsychopharmacol. Biol. Psychiatry 16 (1992), 797–832.
85. Maccari, S., Piazza, P.V., Kabbaj, M., Barbazanges, A., Simon, H., et al. Adoption reverses the long-term impairment in glucocorticoid feedback induced by prenatal stress. J. Neurosci. 15 (1995), 110–116.
86. Maren, S., Tocco, G., Standley, S., Baudry, M., Thompson, R.F., Postsynaptic factors in the expression of long-term potentiation (LTP): increased glutamate receptor binding following LTP induction in vivo. Proc. Natl. Acad. Sci. U. S. A. 90 (1993), 9654–9658.
87. Markham, J.A., Taylor, A.R., Taylor, S.B., Bell, D.B., Koenig, J.I., Characterization of the cognitive impairments induced by prenatal exposure to stress in the rat. Front. Behav. Neurosci., 4, 2010, 173.
88. Martin, E.I., Ressler, K.J., Binder, E., Nemeroff, C.B., The neurobiology of anxiety disorders: brain imaging, genetics, and psychoneuroendocrinology. Psychiatr. Clin. North Am. 32 (2009), 549–575.
89. Martinowich, K., Manji, H., Lu, B., New insights into BDNF function in depression and anxiety. Nat. Neurosci. 10 (2007), 1089–1093.
90. Matrisciano, F., Panaccione, I., Grayson, D.R., Nicoletti, F., Guidotti, A., Metabotropic glutamate 2/3 Receptors and epigenetic modifications in psychotic disorders: a review. Curr. Neuropharmacol. 14 (2016), 41–47.
91. Matrisciano, F., Tueting, P., Dalal, I., Kadriu, B., Grayson, D.R., et al. Epigenetic modifications of GABAergic interneurons are associated with the schizophrenia-like phenotype induced by prenatal stress in mice. Neuropharmacology 68 (2013), 184–194.
92. McEwen, B.S., The neurobiology of stress: from serendipity to clinical relevance. Brain Res. 886 (2000), 172–189.
93. McGivern, R.F., Poland, R.E., Taylor, A.N., Branch, B.J., Raum, W.J., Prenatal stress feminizes adult male saccharin preference and maze learning: antagonism by propranolol. Monogr. Neural Sci. 12 (1986), 172–178.
94. Mednick, S.A., Huttunen, M.O., Machon, R.A., Prenatal influenza infections and adult schizophrenia. Schizophr. Bull. 20 (1994), 263–267.
95. Meek, L.R., Dittel, P.L., Sheehan, M.C., Chan, J.Y., Kjolhaug, S.R., Effects of stress during pregnancy on maternal behavior in mice. Physiol. Behav. 72 (2001), 473–479.
96. Melia, K.R., Ryabinin, A.E., Schroeder, R., Bloom, F.E., Wilson, M.C., Induction and habituation of immediate early gene expression in rat brain by acute and repeated restraint stress. J. Neurosci. 14 (1994), 5929–5938.
97. Melniczek, J.R., Ward, I.L., Patterns of ano-genital licking mother rats exhibit toward prenatally stressed neonates. Physiol. Behav. 56 (1994), 457–461.
98. Miyagawa, K., Tsuji, M., Fujimori, K., Saito, Y., Takeda, H., Prenatal stress induces anxiety-like behavior together with the disruption of central serotonin neurons in mice. Neurosci. Res. 70 (2011), 111–117.
99. Modir, F., Elahdadi Salmani, M., Goudarzi, I., Lashkarboluki, T., Abrari, K., Prenatal stress decreases spatial learning and memory retrieval of the adult male offspring of rats. Physiol. Behav. 129 (2014), 104–109.
100. Monyer, H., Burnashev, N., Laurie, D.J., Sakmann, B., Seeburg, P.H., Developmental and regional expression in the rat brain and functional properties of four NMDA receptors. Neuron 12 (1994), 529–540.
101. Moore, C.L., Power, K.L., Prenatal stress affects mother-infant interaction in Norway rats. Dev. Psychobiol. 19 (1986), 235–245.
102. Morato, S., Castrechini, P., Effects of floor surface and environmental illumination on exploratory activity in the elevated plus-maze. Braz. J. Med. Biol. Res. 22 (1989), 707–710.
103. Moreau, J.L., Simulating the anhedonia symptom of depression in animals. Dialogues Clin. Neurosci. 4 (2002), 351–360.
104. Morris, R., Developments of a water-maze procedure for studying spatial learning in the rat. J. Neurosci. Methods 11 (1984), 47–60.
105. Mychasiuk, R., Schmold, N., Ilnytskyy, S., Kovalchuk, O., Kolb, B., et al. Prenatal bystander stress alters brain, behavior, and the epigenome of developing rat offspring. Dev. Neurosci. 33 (2011), 159–169.
106. Palacios-Garcia, I., Lara-Vasquez, A., Montiel, J.F., Diaz-Veliz, G.F., Sepulveda, H., et al. Prenatal stress down-regulates Reelin expression by methylation of its promoter and induces adult behavioral impairments in rats. PLoS One, 10, 2015, e0117680.
107. Paris, J.J., Frye, C.A., Gestational exposure to variable stressors produces decrements in cognitive and neural development of juvenile male and female rats. Curr. Top. Med. Chem. 11 (2011), 1706–1713.
108. Park, S., Cho, S.C., Kim, J.W., Shin, M.S., Yoo, H.J., et al. Differential perinatal risk factors in children with attention-deficit/hyperactivity disorder by subtype. Psychiatry Res. 219 (2014), 609–616.
109. Pellow, S., File, S.E., Anxiolytic and anxiogenic drug effects on exploratory activity in an elevated plus-maze: a novel test of anxiety in the rat. Pharmacol. Biochem. Behav. 24 (1986), 525–529.
110. Perez-Otano, I., Ehlers, M.D., Homeostatic plasticity and NMDA receptor trafficking. Trends Neurosci. 28 (2005), 229–238.
111. Pfister, H.P., Muir, J.L., Psychological stress and administered oxytocin during pregnancy: effect corticosterone and prolactin response in lactating rats. Int. J. Neurosci. 45 (1989), 91–99.
112. Ping, S.E., Trieu, J., Wlodek, M.E., Barrett, G.L., Effects of estrogen on basal forebrain cholinergic neurons and spatial learning. J. Neurosci. Res. 86 (2008), 1588–1598.
113. Poltyrev, T., Weinstock, M., Effect of gestational stress on maternal behavior in response to cage transfer and handling of pups in two strains of rat. Stress 3 (1999), 85–95.
114. Porsolt, R.D., Anton, G., Blavet, N., Jalfre, M., Behavioural despair in rats: a new model sensitive to antidepressant treatments. Eur. J. Pharmacol. 47 (1978), 379–391.
115. Power, K.L., Moore, C.L., Prenatal stress eliminates differential maternal attention to male offspring in Norway rats. Physiol. Behav. 38 (1986), 667–671.
116. Ratajczak, P., Kus, K., Murawiecka, P., Slodzinska, I., Giermaziak, W., et al. Biochemical and cognitive impairments observed in animal models of schizophrenia induced by prenatal stress paradigm or methylazoxymethanol acetate administration. Acta Neurobiol. Exp. (Wars) 75 (2015), 314–325.
117. Riedel, G., Platt, B., Micheau, J., Glutamate receptor function in learning and memory. Behav. Brain Res. 140 (2003), 1–47.
118. Rohde, W., Ohkawa, T., Dobashi, K., Arai, K., Okinaga, S., et al. Acute effects of maternal stress on fetal blood catecholamines and hypothalamic LH-RH content. Exp. Clin. Endocrinol. 82 (1983), 268–274.
119. Said, N., Lakehayli, S., El Khachibi, M., El Ouahli, M., Nadifi, S., et al. Effect of prenatal stress on memory, nicotine withdrawal and 5HT1A expression in raphe nuclei of adult rats. Int. J. Dev. Neurosci. 43 (2015), 92–98.
120. Salomon, S., Bejar, C., Schorer-Apelbaum, D., Weinstock, M., Corticosterone mediates some but not other behavioural changes induced by prenatal stress in rats. J. Neuroendocrinol. 23 (2011), 118–128.
121. Schroeder, M., Sultany, T., Weller, A., Prenatal stress effects on emotion regulation differ by genotype and sex in prepubertal rats. Dev. Psychobiol. 55 (2013), 176–192.
122. Schulz, K.M., Pearson, J.N., Neeley, E.W., Berger, R., Leonard, S., et al. Maternal stress during pregnancy causes sex-specific alterations in offspring memory performance, social interactions, indices of anxiety, and body mass. Physiol. Behav. 104 (2011), 340–347.
123. Selye, H., Stress and the general adaptation syndrome. Br. Med. J. 1 (1950), 1383–1392.
124. Sesack, S.R., Carr, D.B., Selective prefrontal cortex inputs to dopamine cells: implications for schizophrenia. Physiol. Behav. 77 (2002), 513–517.
125. Sickmann, H.M., Arentzen, T.S., Dyrby, T.B., Plath, N., Kristensen, M.P., Prenatal stress produces sex-specific changes in depression-like behavior in rats: implications for increased vulnerability in females. J. Dev. Orig. Health Dis. 6 (2015), 462–474.
126. Simonyi, A., Schachtman, T.R., Christoffersen, G.R., The role of metabotropic glutamate receptor 5 in learning and memory processes. Drug News Perspect. 18 (2005), 353–361.
127. Son, G.H., Geum, D., Chung, S., Kim, E.J., Jo, J.H., et al. Maternal stress produces learning deficits associated with impairment of NMDA receptor-mediated synaptic plasticity. J. Neurosci. 26 (2006), 3309–3318.
128. Stefanis, N., Frangou, S., Yakeley, J., Sharma, T., O'Connell, P., et al. Hippocampal volume reduction in schizophrenia: effects of genetic risk and pregnancy and birth complications. Biol. Psychiatry 46 (1999), 697–702.
129. Sun, H., Jia, N., Guan, L., Su, Q., Wang, D., et al. Involvement of NR1, NR2A different expression in brain regions in anxiety-like behavior of prenatally stressed offspring. Behav. Brain Res. 257 (2013), 1–7.
130. Sutcliffe, J.S., Marshall, K.M., Neill, J.C., Influence of gender on working and spatial memory in the novel object recognition task in the rat. Behav. Brain Res. 177 (2007), 117–125.
131. Takahashi, L.K., Turner, J.G., Kalin, N.H., Prolonged stress-induced elevation in plasma corticosterone during pregnancy in the rat: implications for prenatal stress studies. Psychoneuroendocrinology 23 (1998), 571–581.
132. Thompson, W.R., Influence of prenatal maternal anxiety on emotionality in young rats. Science 125 (1957), 698–699.
133. Vallee, M., Mayo, W., Dellu, F., Le Moal, M., Simon, H., et al. Prenatal stress induces high anxiety and postnatal handling induces low anxiety in adult offspring: correlation with stress-induced corticosterone secretion. J. Neurosci. 17 (1997), 2626–2636.
134. Van den Bergh, B.R., Van Calster, B., Smits, T., Van Huffel, S., Lagae, L., Antenatal maternal anxiety is related to HPA-axis dysregulation and self-reported depressive symptoms in adolescence: a prospective study on the fetal origins of depressed mood. Neuropsychopharmacology 33 (2008), 536–545.
135. Van den Hove, D.L., Blanco, C.E., Aendekerk, B., Desbonnet, L., Bruschettini, M., et al. Prenatal restraint stress and long-term affective consequences. Dev. Neurosci. 27 (2005), 313–320.
136. Van den Hove, D.L., Leibold, N.K., Strackx, E., Martinez-Claros, M., Lesch, K.P., et al. Prenatal stress and subsequent exposure to chronic mild stress in rats; interdependent effects on emotional behavior and the serotonergic system. Eur. Neuropsychopharmacol. 24 (2014), 595–607.
137. Van Lieshout, R.J., Boylan, K., Increased depressive symptoms in female but not male adolescents born at low birth weight in the offspring of a national cohort. Can. J. Psychiatry 55 (2010), 422–430.
138. Voikar, V., Vasar, E., Rauvala, H., Behavioral alterations induced by repeated testing in C57BL/6J and 129S2/Sv mice: implications for phenotyping screens. Genes Brain Behav. 3 (2004), 27–38.
139. Volk, D.W., Lewis, D.A., Prefrontal cortical circuits in schizophrenia. Curr. Top. Behav. Neurosci. 4 (2010), 485–508.
140. Walder, D.J., Laplante, D.P., Sousa-Pires, A., Veru, F., Brunet, A., et al. Prenatal maternal stress predicts autism traits in 6(1/2) year-old children: project Ice Storm. Psychiatry Res. 219 (2014), 353–360.
141. Walf, A.A., Frye, C.A., Estradiol decreases anxiety behavior and enhances inhibitory avoidance and gestational stress produces opposite effects. Stress 10 (2007), 251–260.
142. Wang, Y., Ma, Y.C., Cheng, W.W., Jiang, H., Zhang, X.X., et al. Sexual differences in long-term effects of prenatal chronic mild stress on anxiety-like behavior and stress-induced regional glutamate receptor expression in rat offspring. Int. J. Dev. Neurosci. 41 (2015), 80–91.
143. Wang, Y., Ma, Y., Hu, J., Cheng, W., Jiang, H., et al. Prenatal chronic mild stress induces depression-like behavior and sex-specific changes in regional glutamate receptor expression patterns in adult rats. Neuroscience 301 (2015), 363–374.
144. Ward, I.L., Prenatal stress feminizes and demasculinizes the behavior of males. Science 175 (1972), 82–84.
145. Weickert, C.S., Hyde, T.M., Lipska, B.K., Herman, M.M., Weinberger, D.R., et al. Reduced brain-derived neurotrophic factor in prefrontal cortex of patients with schizophrenia. Mol. Psychiatry 8 (2003), 592–610.
146. Weiler, I.J., Greenough, W.T., Metabotropic glutamate receptors trigger postsynaptic protein synthesis. Proc. Natl. Acad. Sci. U. S. A. 90 (1993), 7168–7171.
147. Weinstock, M., The potential influence of maternal stress hormones on development and mental health of the offspring. Brain Behav. Immun. 19 (2005), 296–308.
148. Weinstock, M., Gender differences in the effects of prenatal stress on brain development and behaviour. Neurochem. Res. 32 (2007), 1730–1740.
149. Weinstock, M., The long-term behavioural consequences of prenatal stress. Neurosci. Biobehav. Rev. 32 (2008), 1073–1086.
150. Weinstock, M., Sex-dependent changes induced by prenatal stress in cortical and hippocampal morphology and behaviour in rats: an update. Stress 14 (2011), 604–613.
151. Weinstock, M., Changes induced by prenatal stress in behavior and brain morphology: can they be prevented or reversed?. Adv. Neurobiol. 10 (2015), 3–25.
152. Weinstock, M., Fride, E., Hertzberg, R., Prenatal stress effects on functional development of the offspring. Prog. Brain Res. 73 (1988), 319–331.
153. Weinstock, M., Matlina, E., Maor, G.I., Rosen, H., McEwen, B.S., Prenatal stress selectively alters the reactivity of the hypothalamic-pituitary adrenal system in the female rat. Brain Res. 595 (1992), 195–200.
154. Williams, M.T., Davis, H.N., McCrea, A.E., Long, S.J., Hennessy, M.B., Changes in the hormonal concentrations of pregnant rats and their fetuses following multiple exposures to a stressor during the third trimester. Neurotoxicol. Teratol. 21 (1999), 403–414.
155. Wilson, C.A., Terry, A.V. Jr., Variable maternal stress in rats alters locomotor activity, social behavior, and recognition memory in the adult offspring. Pharmacol. Biochem. Behav. 104 (2013), 47–61.
156. Wilson, C.A., Vazdarjanova, A., Terry, A.V. Jr., Exposure to variable prenatal stress in rats: effects on anxiety-related behaviors, innate and contextual fear, and fear extinction. Behav. Brain Res. 238 (2013), 279–288.
157. Wood, M.A., Hawk, J.D., Abel, T., Combinatorial chromatin modifications and memory storage: a code for memory?. Learn Mem. 13 (2006), 241–244.
158. Xu, J., Yang, B., Yan, C., Hu, H., Cai, S., et al. Effects of duration and timing of prenatal stress on hippocampal myelination and synaptophysin expression. Brain Res. 1527 (2013), 57–66.
159. Yaka, R., Salomon, S., Matzner, H., Weinstock, M., Effect of varied gestational stress on acquisition of spatial memory, hippocampal LTP and synaptic proteins in juvenile male rats. Behav. Brain Res. 179 (2007), 126–132.
160. Yang, J., Han, H., Cao, J., Li, L., Xu, L., Prenatal stress modifies hippocampal synaptic plasticity and spatial learning in young rat offspring. Hippocampus 16 (2006), 431–436.
161. Yeh, C.M., Huang, C.C., Hsu, K.S., Prenatal stress alters hippocampal synaptic plasticity in young rat offspring through preventing the proteolytic conversion of pro-brain-derived neurotrophic factor (BDNF) to mature BDNF. J. Physiol. 590 (2012), 991–1010.
162. Zagron, G., Weinstock, M., Maternal adrenal hormone secretion mediates behavioural alterations induced by prenatal stress in male and female rats. Behav. Brain Res. 175 (2006), 323–328.
163. Zarrow, M.X., Philpott, J.E., Denenberg, V.H., Passage of 14C-4-corticosterone from the rat mother to the foetus and neonate. Nature 226 (1970), 1058–1059.
164. Zhang, X.H., Jia, N., Zhao, X.Y., Tang, G.K., Guan, L.X., Wang, D., Sun, H.L., Li, H., Zhu, Z.L., Involvement of pGluR1, EAAT2 and EAAT3 in offspring depression induced by prenatal stress. Neuroscience 250 (2013), 333–341.
165. Zhao, D., Liu, D., Chen, X., Wang, K., Zhang, A., et al. Prenatal stress disturbs hippocampal KIF17 and NR2B in spatial cognition in male offspring. J. Neurosci. Res. 91 (2013), 535–544.
166. Zhu, P., Hao, J.H., Tao, R.X., Huang, K., Jiang, X.M., et al. Sex-specific and time-dependent effects of prenatal stress on the early behavioral symptoms of ADHD: a longitudinal study in China. Eur. Child Adolesc. Psychiatry 24 (2015), 1139–1147.
167. Zohar, I., Dosoretz-Abittan, L., Shoham, S., Weinstock, M., Sex dependent reduction by prenatal stress of the expression of 5HT1A receptors in the prefrontal cortex and CRF type 2 receptors in the raphe nucleus in rats: reversal by citalopram. Psychopharmacol. Berl. 232 (2015), 1643–1653.
168. Zohar, I., Shoham, S., Weinstock, M., Perinatal citalopram does not prevent the effect of prenatal stress on anxiety, depressive-like behaviour and serotonergic transmission in adult rat offspring. Eur. J. Neurosci. 43 (2016), 590–600.
169. Zohar, I., Weinstock, M., Differential effect of prenatal stress on the expression of corticotrophin-releasing hormone and its receptors in the hypothalamus and amygdala in male and female rats. J. Neuroendocrinol. 23 (2011), 320–328.
170. Zuena, A.R., Mairesse, J., Casolini, P., Cinque, C., Alema, G.S., et al. Prenatal restraint stress generates two distinct behavioral and neurochemical profiles in male and female rats. PLoS One, 3, 2008, e2170.