Prenatal stress and increased susceptibility to anxiety-like behaviors: role of neuroinflammation and balance between GABAergic and glutamatergic transmission

References

• Ackermann, T. F., Hörtnagl, H., Wolfer, D. P., Colacicco, G., Sohr, R., Lang, F., Hellweg, R., & Lang, U. E. (2008). Phosphatidylinositide dependent kinase deficiency increases anxiety and decreases GABA and serotonin abundance in the amygdala. Cellular Physiology and Biochemistry: 22(5–6), 735–744. https://doi.org/10.1159/000185557.
   PubMed Web of Science ®Google Scholar
• Adrover, E., Pallarés, M. E., Baier, C. J., Monteleone, M. C., Giuliani, F. A., Waagepetersen, H. S., Brocco, M. A., Cabrera, R., Sonnewald, U., Schousboe, A., & Antonelli, M. C. (2015). Glutamate neurotransmission is affected in prenatally stressed offspring. Neurochemistry International, 88, 73–87. https://doi.org/10.1016/j.neuint.2015.05.005.
   PubMed Web of Science ®Google Scholar
• Ahmadzadeh, R., Saboory, E., Roshan-Milani, S., & Pilehvarian, A. A. (2011). Predator and restraint stress during gestation facilitates pilocarpine-induced seizures in prepubertal rats. Developmental Psychobiology, 53(8), 806–812. https://doi.org/10.1002/dev.20555.
   PubMed Web of Science ®Google Scholar
• Akatsu, S., Ishikawa, C., Takemura, K., Ohtani, A., & Shiga, T. (2015). Effects of prenatal stress and neonatal handling on anxiety, spatial learning and serotonergic system of male offspring mice. Neuroscience Research, 101, 15–23. https://doi.org/10.1016/j.neures.2015.07.002.
   PubMed Web of Science ®Google Scholar
• Azizi, N., Roshan-Milani, S., MahmoodKhani, M., Saboory, E., Gholinejad, Z., Abdollahzadeh, N., Sayyadi, H., & Chodari, L. (2019). Parental pre-conception stress status and risk for anxiety in rat offspring: Specific and sex-dependent maternal and paternal effects. Stress, 22(5), 619–631. https://doi.org/10.1080/10253890.2019.1619075.
   PubMed Web of Science ®Google Scholar
• Baek, H., Yi, M. H., Pandit, S., Park, J. B., Kwon, H. H., Zhang, E., Kim, S., Shin, N., Kim, E., Lee, Y. H., Kim, Y., Kim, D. W., & Kang, J. W. (2016). Altered expression of KCC2 in GABAergic interneuron contributes prenatal stress-induced epileptic spasms in infant rat. Neurochemistry International, 97, 57–64. https://doi.org/10.1016/j.neuint.2016.05.006.
   PubMed Web of Science ®Google Scholar
• Bagheri, M., Saboory, E., Nejatbakhsh, M., Roshan-Milani, S., Derafshpour, L., Sayyadi, H., & Rasmi, Y. (2020). Prenatal stress increased γ2 GABAA receptor subunit gene expression in hippocampus and potentiated pentylenetetrazol-induced seizure in rats. Iranian Journal of Basic Medical Sciences, 23, 1–6.
   PubMed Web of Science ®Google Scholar
• Bangasser, D. A., Zhang, X., Garachh, V., Hanhauser, E., & Valentino, R. J. (2011). Sexual dimorphism in locus coeruleus dendritic morphology: A structural basis for sex differences in emotional arousal. Physiology & Behavior, 103(3–4), 342–351. https://doi.org/10.1016/j.physbeh.2011.02.037.
   PubMed Web of Science ®Google Scholar
• Ben-Ari, Y., Khalilov, I., Kahle, K. T., & Cherubini, E. (2012). The GABA excitatory/inhibitory shift in brain maturation and neurological disorders. The Neuroscientist: A Review Journal Bringing Neurobiology, Neurology and Psychiatry, 18(5), 467–486. https://doi.org/10.1177/1073858412438697.
   PubMed Web of Science ®Google Scholar
• Bennett, G. A., Palliser, H. K., Shaw, J. C., Palazzi, K. L., Walker, D. W., & Hirst, J. J. (2017). Maternal stress in pregnancy affects myelination and neurosteroid regulatory pathways in the guinea pig cerebellum. Stress, 20(6), 580–588. https://doi.org/10.1080/10253890.2017.1378637
   PubMed Web of Science ®Google Scholar
• Berger, M. A., Barros, V. G., Sarchi, M. I., Tarazi, F. I., & Antonelli, M. C. (2002). Long-term effects of prenatal stress on dopamine and glutamate receptors in adult rat brain. Neurochemical Research, 27(11), 1525–1533. https://doi.org/10.1023/A:1021656607278
   PubMed Web of Science ®Google Scholar
• Biala, Y. N., Bogoch, Y., Bejar, C., Linial, M., & Weinstock, M. (2011). Prenatal stress diminishes gender differences in behavior and in expression of hippocampal synaptic genes and proteins in rats. Hippocampus, 21(10), 1114–1125. https://doi.org/10.1002/hipo.20825.
   PubMed Web of Science ®Google Scholar
• Boersma, G. J., & Tamashiro, K. L. (2015). Individual differences in the effects of prenatal stress exposure in rodents. Neurobiology of Stress, 1, 100–108. https://doi.org/10.1016/j.ynstr.2014.10.006.
   PubMed Web of Science ®Google Scholar
• Bronson, S. L., & Bale, T. L. (2014). Prenatal stress-induced increases in placental inflammation and offspring hyperactivity are male-specific and ameliorated by maternal antiinflammatory treatment. Endocrinology, 155(7), 2635–2646. https://doi.org/10.1210/en.2014-1040
   PubMed Web of Science ®Google Scholar
• Brunton, P. J., & Russell, J. A. (2010). Prenatal social stress in the rat programmes neuroendocrine and behavioural responses to stress in the adult offspring: Sex-specific effects. Journal of Neuroendocrinology, 22(4), 258–271. https://doi.org/10.1111/j.1365-2826.2010.01969.x.
   PubMed Web of Science ®Google Scholar
• Bueno, C. H., Zangrossi, H., Jr,., & Viana, M. B. (2005). The inactivation of the basolateral nucleus of the rat amygdala has an anxiolytic effect in the elevated T-maze and light/dark transition tests. Revista Brasileira de Pesquisas Medicas e Biologicas [Brazilian Journal of Medical and Biological Research], 38(11), 1697–1701. https://doi.org/10.1590/s0100-879x2005001100019
   Google Scholar
• Burt, M. A., Tse, Y. C., Boksa, P., & Wong, T. P. (2013). Prenatal immune activation interacts with stress and corticosterone exposure later in life to modulate N-methyl-d-aspartate receptor synaptic function and plasticity. International Journal of Neuropsychopharmacology, 16(8):1835–1848. https://doi.org/10.1017/S1461145713000229
   PubMed Web of Science ®Google Scholar
• Calcia, M. A., Bonsall, D. R., Bloomfield, P. S., Selvaraj, S., Barichello, T., & Howes, O. D. (2016). Stress and neuroinflammation: A systematic review of the effects of stress on microglia and the implications for mental illness. Psychopharmacology, 233(9), 1637–1650. https://doi.org/10.1007/s00213-016-4218-9.
   PubMed Web of Science ®Google Scholar
• Cartwright-Hatton, S. (2006). Anxiety of childhood and adolescence: Challenges and opportunities. Clinical Psychology Review, 26(7), 813–816. https://doi.org/10.1016/j.cpr.2005.12.001.
   PubMed Web of Science ®Google Scholar
• Charil, A., Laplante, D. P., Vaillancourt, C., & King, S. (2010). Prenatal stress and brain development. Brain Research Reviews, 65(1), 56–79. https://doi.org/10.1016/j.brainresrev.2010.06.002.
   PubMedGoogle Scholar
• Chen, M.-X., Liu, Q., Cheng, S., Lei, L., Lin, A.-J., Wei, R., K Hui, T. C., Li, Q., Ao, L.-J., & Sham, P. C. (2020). Interleukin-18 levels in the hippocampus and behavior of adult rat offspring exposed to prenatal restraint stress during early and late pregnancy. Neural Regeneration Research, 15(9), 1748–1756. https://doi.org/10.4103/1673-5374.276358
   PubMed Web of Science ®Google Scholar
• Coe, C. L., Kramer, M., Czéh, B., Gould, E., Reeves, A. J., Kirschbaum, C., & Fuchs, E. (2003). Prenatal stress diminishes neurogenesis in the dentate gyrus of juvenile Rhesus monkeys. Biological Psychiatry, 54(10), 1025–1034. https://doi.org/10.1016/S0006-3223(03)00698-X.
   PubMed Web of Science ®Google Scholar
• Darnaudéry, M., & Maccari, S. (2008). Epigenetic programming of the stress response in male and female rats by prenatal restraint stress. Brain Research Reviews, 57(2), 571–585. https://doi.org/10.1016/j.brainresrev.2007.11.004.
   PubMed Web of Science ®Google Scholar
• Davis, E. P., & Sandman, C. A. (2012). Prenatal psychobiological predictors of anxiety risk in preadolescent children. Psychoneuroendocrinology, 37(8), 1224–1233. https://doi.org/10.1016/j.psyneuen.2011.12.016.
   PubMed Web of Science ®Google Scholar
• Del Giudice, M. (2016). Differential susceptibility to the environment: Are developmental models compatible with the evidence from twin studies? Developmental Psychology, 52(8), 1330–1339. https://doi.org/10.1037/dev0000153.
   PubMed Web of Science ®Google Scholar
• Di Giorgi Gerevini, V. D., Caruso, A., Cappuccio, I., Ricci Vitiani, L., Romeo, S., Della Rocca, C., Gradini, R., Melchiorri, D., & Nicoletti, F. (2004). The mGlu5 metabotropic glutamate receptor is expressed in zones of active neurogenesis of the embryonic and postnatal brain. Brain Research. Developmental Brain Research, 150(1), 17–22. https://doi.org/10.1016/j.devbrainres.2004.02.003.
   PubMedGoogle Scholar
• Di Giorgi-Gerevini, V., Melchiorri, D., Battaglia, G., Ricci-Vitiani, L., Ciceroni, C., Busceti, C. L., Biagioni, F., Iacovelli, L., Canudas, A. M., Parati, E., De Maria, R., & Nicoletti, F. (2005). Endogenous activation of metabotropic glutamate receptors supports the proliferation and survival of neural progenitor cells. Cell Death and Differentiation, 12(8), 1124–1133. https://doi.org/10.1038/sj.cdd.4401639.
   PubMed Web of Science ®Google Scholar
• Dipietro, J. (2004). The role of prenatal maternal stress in child development. Current Directions in Psychological Science, 13(2), 71–74. https://doi.org/10.1111/j.0963-7214.2004.00277.x
   Web of Science ®Google Scholar
• Diz-Chaves, Y., Astiz, M., Bellini, M. J., & Garcia-Segura, L. M. (2013). Prenatal stress increases the expression of proinflammatory cytokines and exacerbates the inflammatory response to LPS in the hippocampal formation of adult male mice. Brain, Behavior, and Immunity, 28, 196–206. https://doi.org/10.1016/j.bbi.2012.11.013.
   PubMed Web of Science ®Google Scholar
• Diz-Chaves, Y., Pernía, O., Carrero, P., & Garcia-Segura, L. M. (2012). Prenatal stress causes alterations in the morphology of microglia and the inflammatory response of the hippocampus of adult female mice. Journal of Neuroinflammation, 9, 71. https://doi.org/10.1186/1742-2094-9-71.
   PubMed Web of Science ®Google Scholar
• Duan, Z., Zhang, X., Zhu, G. X., Gao, Y., & Xue, X. (2013). Activation of mGluR4 promotes proliferation of rat neural progenitor cells while mediating activation of ERK1/2 signaling pathway. Cell Mol Biol, 59, OL1809–1817.
   PubMed Web of Science ®Google Scholar
• Edwards, H. E., Dortok, D., Tam, J., Won, D., & Burnham, W. M. I. (2002). Prenatal stress alters seizure thresholds and the development of kindled seizures in infant and adult rats. Hormones and Behavior, 42(4), 437–447. https://doi.org/10.1006/hbeh.2002.1839.
   PubMed Web of Science ®Google Scholar
• Ehrlich, D. E., Neigh, G. N., Bourke, C. H., Nemeth, C. L., Hazra, R., Ryan, S. J., Rowson, S., Jairam, N., Sholar, C. A., Rainnie, D. G., Stowe, Z. N., & Owens, M. J. (2015). Prenatal stress, regardless of concurrent escitalopram treatment, alters behavior and amygdala gene expression of adolescent female rats. Neuropharmacology, 97, 251–258. https://doi.org/10.1016/j.neuropharm.2015.05.012.
   PubMed Web of Science ®Google Scholar
• El-Ansary, A., & Al-Ayadhi, L. (2014). GABAergic/glutamatergic imbalance relative to excessive neuroinflammation in autism spectrum disorders. Journal of Neuroinflammation, 11, 189. https://doi.org/10.1186/s12974-014-0189-0
   PubMed Web of Science ®Google Scholar
• Ensminger, D. C., Langkilde, T., Owen, D. A. S., MacLeod, K. J., & Sheriff, M. J. (2018). Maternal stress alters the phenotype of the mother, her eggs and her offspring in a wild-caught lizard. Journal of Animal Ecology, 87(6), 1685–1697. https://doi.org/10.1111/1365-2656.12891.
   PubMed Web of Science ®Google Scholar
• Entringer, S., Buss, C., & Wadhwa, P. D. (2012). Prenatal stress, telomere biology, and fetal programming of health and disease risk. Science Signaling, 5(248), pt12. https://doi.org/10.1126/scisignal.2003580.
   PubMed Web of Science ®Google Scholar
• Evanson, N. K., & Herman, J. P. (2015). Role of paraventricular nucleus glutamate signaling in regulation of HPA axis stress responses. Interdisciplinary Information Sciences, 21(3), 253–260. https://doi.org/10.4036/iis.2015.b.10.
   PubMedGoogle Scholar
• Finnell, J. E., Lombard, C. M., Padi, A. R., Moffitt, C. M., Wilson, L. B., Wood, C. S., & Wood, S. K. (2017). Physical versus psychological social stress in male rats reveals distinct cardiovascular, inflammatory and behavioral consequences. PLoS One, 12(2), e0172868. https://doi.org/10.1371/journal.pone.0172868.
   PubMed Web of Science ®Google Scholar
• Fride, E., & Weinstock, M. (1988). Prenatal stress increase anxiety related behavior and alters cerebral lateralization of dopamine activity. Life Sciences, 42(10), 1059–1065. https://doi.org/10.1016/0024-3205(88)90561-9.
   PubMed Web of Science ®Google Scholar
• French, N. P., Hagan, R., Evans, S. F., Mullan, A., & Newnham, J. P. (2004). Repeated antenatal corticosteroids: Effects on cerebral palsy and childhood behavior. American Journal of Obstetrics and Gynecology, 190(3), 588–595. https://doi.org/10.1016/j.ajog.2003.12.016
   PubMed Web of Science ®Google Scholar
• Frick, L. R., Williams, K., & Pittenger, C. (2013). Microglial dysregulation in psychiatric disease. Clinical & Developmental Immunology, 2013, 608654. https://doi.org/10.1155/2013/608654.
   PubMedGoogle Scholar
• Fumagalli, F., Pasini, M., Frasca, A., Drago, F., Racagni, G., & Riva, M. A. (2009). Prenatal stress alters glutamatergic system responsiveness in adult rat prefrontal cortex. Journal of Neurochemistry, 109(6), 1733–1744. https://doi.org/10.1111/j.1471-4159.2009.06088.x
   PubMed Web of Science ®Google Scholar
• Gholami, M., & Saboory, E. (2013). Morphine exposure induces age-dependent alterations in pentylenetetrazole-induced epileptic behaviors in prepubertal rats. Developmental Psychobiology, 55(8), 881–887. https://doi.org/10.1002/dev.21080
   PubMed Web of Science ®Google Scholar
• Gholipoor, P., Saboory, E., Ghazavi, A., Kiyani, A., Roshan-Milani, S., Mohammadi, S., Javanmardi, E., & Rasmi, Y. (2017). Prenatal stress potentiates febrile seizure and leads to long-lasting increase in cortisol blood levels in children under 2 years old. Epilepsy & Behavior, 72, 22–27. https://doi.org/10.1016/j.yebeh.2017.04.021.
   PubMed Web of Science ®Google Scholar
• Glover, V. (2011). Annual research review: Prenatal stress and the origins of psychopathology: An evolutionary perspective. Journal of Child Psychology and Psychiatry, and Allied Disciplines, 52(4), 356–367. https://doi.org/10.1111/j.1469-7610.2011.02371.x
   PubMed Web of Science ®Google Scholar
• Götz, A. A., & Stefanski, V. (2007). Psychosocial maternal stress during pregnancy affects serum corticosterone, blood immune parameters and anxiety behaviour in adult male rat offspring. Physiology & Behavior, 90(1), 108–115. https://doi.org/10.1016/j.physbeh.2006.09.014
   PubMed Web of Science ®Google Scholar
• Gumusoglu, S. B., Fine, R. S., Murray, S. J., Bittle, J. L., & Stevens, H. E. (2017). The role of IL-6 in neurodevelopment after prenatal stress. Brain, Behavior, and Immunity, 65, 274–283. https://doi.org/10.1016/j.bbi.2017.05.015.
   PubMed Web of Science ®Google Scholar
• Gur, T. L., Shay, L., Palkar, A. V., Fisher, S., Varaljay, V. A., Dowd, S., & Bailey, M. T. (2017). Prenatal stress affects placental cytokines and neurotrophins, commensal microbes, and anxiety-like behavior in adult female offspring. Brain, Behavior, and Immunity, 64, 50–58. https://doi.org/10.1016/j.bbi.2016.12.021.
   PubMed Web of Science ®Google Scholar
• Hantsoo, L., Kornfield, S., Anguera, M. C., & Epperson, C. N. (2019). Inflammation: A proposed intermediary between maternal stress and offspring neuropsychiatric risk. Biological Psychiatry, 85(2), 97–106. https://doi.org/10.1016/j.biopsych.2018.08.018.
   PubMed Web of Science ®Google Scholar
• Haroon, E., Miller, A. H., & Sanacora, G. (2017). Inflammation, glutamate, and glia: A trio of trouble in mood disorders. Neuropsychopharmacology, 42(1), 193–215. https://doi.org/10.1038/npp.2016.199.
   PubMed Web of Science ®Google Scholar
• Hashemi, P., Ebrahimi, L., Saboory, E., & Roshan-Milani, S. (2013). Effect of restraint stress during gestation on pentylenetetrazol-induced epileptic behaviors in rat offspring. Iranian Journal of Basic Medical Sciences, 16(9), 979–984. https://doi.org/ijbms-16-979
   PubMed Web of Science ®Google Scholar
• Hashemi, P., Roshan-Milani, S., Saboory, E., Ebrahimi, L., & Soltanineghad, M. (2016). Interactive effects of prenatal exposure to restraint stress and alcohol on pentylenetetrazol-induced seizure behaviors in rat offspring. Alcohol, 56, 51–57. https://doi.org/10.1016/j.alcohol.2016.07.003
   PubMed Web of Science ®Google Scholar
• Hashimoto, T., Arion, D., Unger, T., Maldonado-Avilés, J. G., Morris, H. M., Volk, D. W., Mirnics, K., & Lewis, D. A. (2008). Alterations in GABA-related transcriptome in the dorsolateral prefrontal cortex of subjects with schizophrenia. Molecular Psychiatry, 13(2), 147–161. https://doi.org/10.1038/sj.mp.4002011.
   PubMed Web of Science ®Google Scholar
• Heshmatian, B., Roshan Milani, S. H., & Saboory, E. (2010). Prenatal acute stress attenuated epileptiform activities in neonate mice. Yakhteh, 12(1), 81–86.
   Google Scholar
• Heslin, K., & Coutellier, L. (2018). Npas4 deficiency and prenatal stress interact to affect social recognition in mice. Genes, Brain, and Behavior, 17(5), e12448. https://doi.org/10.1111/gbb.12448.
   PubMed Web of Science ®Google Scholar
• Hou, Q., Li, S., Jiang, C., Huang, Y., Huang, L., Ye, J., Pan, Z., Teng, T., Wang, Q., Jiang, Y., Zhang, H., Liu, C., Li, M., Mo, Z., & Yang, X. (2018). The associations between maternal lifestyles and antenatal stress and anxiety in Chinese pregnant women: A cross-sectional study. Scientific Reports, 8(1), 10771–10771. https://doi.org/10.1038/s41598-018-28974-x.
   PubMedGoogle Scholar
• Iturra-Mena, A. M., Arriagada-Solimano, M., Luttecke-Anders, A., & Dagnino-Subiabre, A. (2018). Effects of prenatal stress on anxiety- and depressive-like behaviours are sex-specific in prepubertal rats. Journal of Neuroendocrinology, 30(7), e12609. https://doi.org/10.1111/jne.12609.
   PubMed Web of Science ®Google Scholar
• Jafari, Z., Faraji, J., Mirza Agha, B., Metz, G. A. S., Kolb, B. E., & Mohajerani, M. H. (2017). The adverse effects of auditory stress on mouse uterus receptivity and behaviour. Scientific Reports, 7(1), 4720. https://doi.org/10.1038/s41598-017-04943-8.
   PubMedGoogle Scholar
• Jia, N., Li, Q., Sun, H., Song, Q., Tang, G., Sun, Q., Wang, W., Chen, R., Li, H., & Zhu, Z. (2015). Alterations of group I mGluRs and BDNF associated with behavioral abnormity in prenatally stressed offspring rats. Neurochemical Research, 40(5), 1074–1082. https://doi.org/10.1007/s11064-015-1565-6.
   PubMed Web of Science ®Google Scholar
• Joca, S. R. L., Ferreira, F. R., & Guimarães, F. S. (2007). Modulation of stress consequences by hippocampal monoaminergic, glutamatergic and nitrergic neurotransmitter systems. Stress, 10(3), 227–249. https://doi.org/10.1080/10253890701223130.
   PubMed Web of Science ®Google Scholar
• Kalueff, A. V., & Nutt, D. J. (2007). Role of GABA in anxiety and depression. Depression and Anxiety, 24(7), 495–517. https://doi.org/10.1002/da.20262
   PubMed Web of Science ®Google Scholar
• Kofman, O. (2002). The role of prenatal stress in the etiology of developmental behavioural disorders. Neuroscience and Biobehavioral Reviews, 26(4), 457–470. https://doi.org/10.1016/S0149-7634(02)00015-5.
   PubMed Web of Science ®Google Scholar
• Laloux, C., Mairesse, J., Van Camp, G., Giovine, A., Branchi, I., Bouret, S., Morley-Fletcher, S., Bergonzelli, G., Malagodi, M., Gradini, R., Nicoletti, F., Darnaudéry, M., & Maccari, S. (2012). Anxiety-like behaviour and associated neurochemical and endocrinological alterations in male pups exposed to prenatal stress. Psychoneuroendocrinology, 37(10), 1646–1658. https://doi.org/10.1016/j.psyneuen.2012.02.010.
   PubMed Web of Science ®Google Scholar
• Lemaire, V., Lamarque, S., Le Moal, M., Piazza, P. V., & Abrous, D. N. (2006). Postnatal stimulation of the pups counteracts prenatal stress-induced deficits in hippocampal neurogenesis. Biological Psychiatry, 59(9), 786–792. https://doi.org/10.1016/j.biopsych.2005.11.009.
   PubMed Web of Science ®Google Scholar
• Lopim, G. M., Gutierre, R. C., da Silva, E. A., & Arida, R. M. (2020). Physical exercise during pregnancy minimizes PTZ-induced behavioral manifestations in prenatally stressed offspring. Developmental Psychobiology, 62(2), 240–249. https://doi.org/10.1002/dev.21895.
   PubMed Web of Science ®Google Scholar
• Luo, L., Sun, T., Yang, L., Liu, A., Liu, Q. Q., Tian, Q. Q., Wang, Y., Zhao, M. G., & Yang, Q. (2020). Scopoletin ameliorates anxiety-like behaviors in complete Freund's adjuvant-induced mouse model. Molecular Brain, 13(1), 15. https://doi.org/10.1186/s13041-020-0560-2
   PubMed Web of Science ®Google Scholar
• Lussier, S. J., & Stevens, H. E. (2016). Delays in GABAergic interneuron development and behavioral inhibition after prenatal stress. Developmental Neurobiology, 76(10), 1078–1091. https://doi.org/10.1002/dneu.22376
   PubMed Web of Science ®Google Scholar
• Mahmoodkhani, M., Saboory, E., Roshan-Milani, S., Azizi, N., Karimipour, M., Rasmi, Y., & Gholinejad, Z. (2018). Pregestational stress attenuated fertility rate in dams and increased seizure susceptibility in offspring. Epilepsy & Behavior, 79, 174–179. https://doi.org/10.1016/j.yebeh.2017.12.016.
   PubMed Web of Science ®Google Scholar
• Mairesse, J., Gatta, E., Reynaert, M. L., Marrocco, J., Morley-Fletcher, S., Soichot, M., Deruyter, L., Camp, G. V., Bouwalerh, H., Fagioli, F., Pittaluga, A., Allorge, D., Nicoletti, F., & Maccari, S. (2015). Activation of presynaptic oxytocin receptors enhances glutamate release in the ventral hippocampus of prenatally restraint stressed rats. Psychoneuroendocrinology, 62, 36–46. https://doi.org/10.1016/j.psyneuen.2015.07.005
   PubMed Web of Science ®Google Scholar
• Markham, J. A., Taylor, A. R., Taylor, S. B., Bell, D. B., & Koenig, J. I. (2010). Characterization of the cognitive impairments induced by prenatal exposure to stress in the rat. Frontiers in Behavioral Neuroscience, 4, 173. https://doi.org/10.3389/fnbeh.2010.00173.
   PubMed Web of Science ®Google Scholar
• Marrocco, J., Mairesse, J., Ngomba, R. T., Silletti, V., Van Camp, G., Bouwalerh, H., Summa, M., Pittaluga, A., Nicoletti, F., Maccari, S., & Morley-Fletcher, S. (2012). Anxiety-like behavior of prenatally stressed rats is associated with a selective reduction of glutamate release in the ventral hippocampus. Journal of Neuroscience, 32(48), 17143–17154. https://doi.org/10.1523/JNEUROSCI.1040-12.2012.
   PubMed Web of Science ®Google Scholar
• Matrisciano, F., Tueting, P., Dalal, I., Kadriu, B., Grayson, D. R., Davis, J. M., Nicoletti, F., & Guidotti, A. (2013). Epigenetic modifications of GABAergic interneurons are associated with the schizophrenia-like phenotype induced by prenatal stress in mice. Neuropharmacology, 68, 184–194. https://doi.org/10.1016/j.neuropharm.2012.04.013.
   PubMed Web of Science ®Google Scholar
• McCarthy, M. M. (2016). Sex differences in the developing brain as a source of inherent risk. Dialogues in Clinical Neuroscience, 18(4), 361–372. https://doi.org/10.31887/DCNS.2016.18.4/mmccarthy
   PubMed Web of Science ®Google Scholar
• McLean, M. A., Cobham, V. E., & Simcock, G. (2018). Prenatal maternal distress: A risk factor for child anxiety? Clinical Child and Family Psychology Review, 21(2), 203–223. https://doi.org/10.1007/s10567-017-0251-4
   PubMed Web of Science ®Google Scholar
• Monk, C., Lugo-Candelas, C., & Trumpff, C. (2019). Prenatal developmental origins of future psychopathology: Mechanisms and pathways. Annual Review of Clinical Psychology, 15, 317–344. https://doi.org/10.1146/annurev-clinpsy-050718-095539
   PubMed Web of Science ®Google Scholar
• Morley-Fletcher, S., Mairesse, J., Soumier, A., Banasr, M., Fagioli, F., Gabriel, C., Mocaer, E., Daszuta, A., McEwen, B., Nicoletti, F., & Maccari, S. (2011). Chronic agomelatine treatment corrects behavioral, cellular, and biochemical abnormalities induced by prenatal stress in rats. Psychopharmacology, 217(3), 301–313. https://doi.org/10.1007/s00213-011-2280-x
   PubMed Web of Science ®Google Scholar
• Mueller, B. R., & Bale, T. L. (2008). Sex-specific programming of offspring emotionality after stress early in pregnancy. The Journal of Neuroscience, 28(36), 9055–9065. https://doi.org/10.1523/JNEUROSCI.1424-08.2008
   PubMed Web of Science ®Google Scholar
• Nakhjiri, E., Saboory, E., Roshan-Milani, S., Rasmi, Y., & Khalafkhani, D. (2017). Effect of prenatal restraint stress and morphine co-administration on plasma vasopressin concentration and anxiety behaviors in adult rat offspring. Stress, 20(2), 205–211. https://doi.org/10.1080/10253890.2017.1306053.
   PubMed Web of Science ®Google Scholar
• Owens, D. F., & Kriegstein, A. R. (2002). Is there more to GABA than synaptic inhibition? Nature Reviews. Neuroscience, 3(9), 715–727. https://doi.org/10.1038/nrn919
   PubMed Web of Science ®Google Scholar
• Pribiag, H., & Stellwagen, D. (2013). TNF-α downregulates inhibitory neurotransmission through protein phosphatase 1-dependent trafficking of GABA(A) receptors. Journal of Neuroscience, 33(40), 15879–15893. https://doi.org/10.1523/jneurosci.0530-13.2013.
   PubMed Web of Science ®Google Scholar
• Réus, G. Z., Fries, G. R., Stertz, L., Badawy, M., Passos, I. C., Barichello, T., Kapczinski, F., & Quevedo, J. (2015). The role of inflammation and microglial activation in the pathophysiology of psychiatric disorders. Neuroscience, 300, 141–154. https://doi.org/10.1016/j.neuroscience.2015.05.018.
   PubMed Web of Science ®Google Scholar
• Riaza Bermudo-Soriano, C., Perez-Rodriguez, M. M., Vaquero-Lorenzo, C., & Baca-Garcia, E. (2012). New perspectives in glutamate and anxiety. Pharmacology, Biochemistry, and Behavior, 100(4), 752–774. https://doi.org/10.1016/j.pbb.2011.04.010.
   PubMed Web of Science ®Google Scholar
• Richardson, H. N., Zorrilla, E. P., Mandyam, C. D., & Rivier, C. L. (2006). Exposure to repetitive versus varied stress during prenatal development generates two distinct anxiogenic and neuroendocrine profiles in adulthood. Endocrinology, 147(5), 2506–2517. https://doi.org/10.1210/en.2005-1054.
   PubMed Web of Science ®Google Scholar
• Saaltink, D. J., & Vreugdenhil, E. (2014). Stress, glucocorticoid receptors, and adult neurogenesis: A balance between excitation and inhibition? Cellular and Molecular Life Sciences, 71(13), 2499–2515. https://doi.org/10.1007/s00018-014-1568-5.
   PubMed Web of Science ®Google Scholar
• Saboory, E., Ebrahimi, L., Roshan-Milani, S., & Hashemi, P. (2015). Interaction of prenatal stress and morphine alters prolactin and seizure in rat pups. Physiology & Behavior, 149, 181–186. https://doi.org/10.1016/j.physbeh.2015.06.004
   PubMed Web of Science ®Google Scholar
• Saboory, E., Gholami, M., Zare, S., & Roshan-Milani, S. (2014). The long-term effects of neonatal morphine administration on the pentylenetetrazol seizure model in rats: The role of hippocampal cholinergic receptors in adulthood. Developmental Psychobiology, 56(3), 498–509. https://doi.org/10.1002/dev.21117.
   PubMed Web of Science ®Google Scholar
• Saboory, E., Mohammadi, S., Dindarian, S., & Mohammadi, H. (2019). Prenatal stress and elevated seizure susceptibility: Molecular inheritable changes. Epilepsy & Behavior, 96, 122–131. https://doi.org/10.1016/j.yebeh.2019.04.046
   PubMed Web of Science ®Google Scholar
• Said, N., Lakehayli, S., Battas, O., Hakkou, F., & Tazi, A. (2015). Effects of prenatal stress on anxiety-like behavior and nociceptive response in rats. Journal of Integrative Neuroscience, 14(2), 223–234. https://doi.org/10.1142/s0219635215500107.
   PubMed Web of Science ®Google Scholar
• Sanacora, G., & Banasr, M. (2013). From pathophysiology to novel antidepressant drugs: Glial contributions to the pathology and treatment of mood disorders. Biological Psychiatry, 73(12), 1172–1179. https://doi.org/10.1016/j.biopsych.2013.03.032.
   PubMed Web of Science ®Google Scholar
• Schulz, K. M., Pearson, J. N., Neeley, E. W., Berger, R., Leonard, S., Adams, C. E., & Stevens, K. E. (2011). Maternal stress during pregnancy causes sex-specific alterations in offspring memory performance, social interactions, indices of anxiety, and body mass. Physiology & Behavior, 104(2), 340–347. https://doi.org/10.1016/j.physbeh.2011.02.021.
   PubMed Web of Science ®Google Scholar
• Servatius, R. J., Salameh, G., Coyle, K. M., & Paré, W. P. (2007). Restraint stress. In G. Fink (Ed.), Encyclopedia of stress. Elsevier.
   Google Scholar
• Shim, H. S., Park, H. J., Woo, J., Lee, C. J., & Shim, I. (2019). Role of astrocytic GABAergic system on inflammatory cytokine-induced anxiety-like behavior. Neuropharmacology, 160, 107776. https://doi.org/10.1016/j.neuropharm.2019.107776.
   PubMed Web of Science ®Google Scholar
• Sierra, A., Gottfried-Blackmore, A., Milner, T. A., McEwen, B. S., & Bulloch, K. (2008). Steroid hormone receptor expression and function in microglia. Glia, 56(6), 659–674. https://doi.org/10.1002/glia.20644.
   PubMed Web of Science ®Google Scholar
• Ślusarczyk, J., Trojan, E., Głombik, K., Budziszewska, B., Kubera, M., Lasoń, W., Popiołek-Barczyk, K., Mika, J., Wędzony, K., & Basta-Kaim, A. (2015). Prenatal stress is a vulnerability factor for altered morphology and biological activity of microglia cells. Frontiers in Cellular Neuroscience, 9, 82. https://doi.org/10.3389/fncel.2015.00082.
   PubMed Web of Science ®Google Scholar
• Son, G. H., Geum, D., Chung, S., Kim, E. J., Jo, J. H., Kim, C. M., Lee, K. H., Kim, H., Choi, S., Kim, H. T., Lee, C. J., & Kim, K. (2006). Maternal stress produces learning deficits associated with impairment of NMDA receptor-mediated synaptic plasticity. Journal of Neuroscience, 26(12), 3309–3318. https://doi.org/10.1523/JNEUROSCI.3850-05.2006
   PubMed Web of Science ®Google Scholar
• Sowa, J., Bobula, B., Glombik, K., Slusarczyk, J., Basta-Kaim, A., & Hess, G. (2015). Prenatal stress enhances excitatory synaptic transmission and impairs long-term potentiation in the frontal cortex of adult offspring rats. PLOS One, 10(3), e0119407. https://doi.org/10.1371/journal.pone.0119407
   PubMed Web of Science ®Google Scholar
• Stevens, H. E., Su, T., Yanagawa, Y., & Vaccarino, F. M. (2013). Prenatal stress delays inhibitory neuron progenitor migration in the developing neocortex. Psychoneuroendocrinology, 38(4), 509–521. https://doi.org/10.1016/j.psyneuen.2012.07.011.
   PubMed Web of Science ®Google Scholar
• Sun, H., Jia, N., Guan, L., Su, Q., Wang, D., Li, H., & Zhu, Z. (2013). Involvement of NR1, NR2A different expression in brain regions in anxiety-like behavior of prenatally stressed offspring. Behavioural Brain Research, 257, 1–7. https://doi.org/10.1016/j.bbr.2013.08.044.
   PubMed Web of Science ®Google Scholar
• Sutherland, S., & Brunwasser, S. M. (2018). Sex differences in vulnerability to prenatal stress: A review of the recent literature. Current Psychiatry Reports, 20(11), 102. https://doi.org/10.1007/s11920-018-0961-4[pii]10.1007/s11920-018-0961-4
   PubMed Web of Science ®Google Scholar
• Takahashi, L. K. (1992). Prenatal stress and the expression of stress-induced responses throughout the life span. Clinical Neuropharmacology., 15(154A), 153. https://doi.org/10.1097/00002826-199201001-00082
   Google Scholar
• Tavassoli, E., Saboory, E., Teshfam, M., Rasmi, Y., Roshan-Milani, S., Ilkhanizadeh, B., & Hesari, A. K. (2013). Effect of prenatal stress on density of NMDA receptors in rat brain. International Journal of Developmental Neuroscience, 31(8), 790–795. https://doi.org/10.1016/j.ijdevneu.2013.09.010.
   PubMed Web of Science ®Google Scholar
• Tollenaar, M. S., Beijers, R., Jansen, J., Riksen-Walraven, J. M. A., & De Weerth, C. (2011). Maternal prenatal stress and cortisol reactivity to stressors in human infants. Stress, 14(1), 53–65. https://doi.org/10.3109/10253890.2010.499485
   PubMed Web of Science ®Google Scholar
• Uchida, T., Furukawa, T., Iwata, S., Yanagawa, Y., & Fukuda, A. (2014). Selective loss of parvalbumin-positive GABAergic interneurons in the cerebral cortex of maternally stressed Gad1-heterozygous mouse offspring. Translational Psychiatry, 4(3), e371. https://doi.org/10.1038/tp.2014.13.
   PubMedGoogle Scholar
• 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 stress-induced corticosterone secretion. The Journal of Neuroscience, 17(7), 2626–2636. https://doi.org/10.1523/JNEUROSCI.17-07-02626.1997
   PubMed Web of Science ®Google Scholar
• van den Bergh, B. R. H., Dahnke, R., & Mennes, M. (2018). Prenatal stress and the developing brain: Risks for neurodevelopmental disorders. Development and Psychopathology, 30(3), 743–762. https://doi.org/10.1017/S0954579418000342
   PubMed Web of Science ®Google Scholar
• Van den Bergh, B. R. H., van den Heuvel, M. I., Lahti, M., Braeken, M., de Rooij, S. R., Entringer, S., Hoyer, D., Roseboom, T., Räikkönen, K., King, S., & Schwab, M. (2017). Prenatal developmental origins of behavior and mental health: The influence of maternal stress in pregnancy. Neuroscience & Biobehavioral Reviews, 117, 26–64. https://doi.org/S0149-7634(16)30734-5
   PubMedGoogle Scholar
• Van den Hove, D. L., Kenis, G., Brass, A., Opstelten, R., Rutten, B. P., Bruschettini, M., Blanco, C. E., Lesch, K. P., Steinbusch, H. W., & Prickaerts, J. (2013). Vulnerability versus resilience to prenatal stress in male and female rats; implications from gene expression profiles in the hippocampus and frontal cortex. European Neuropsychopharmacology, 23(10), 1226–1246. https://doi.org/10.1016/j.euroneuro.2012.09.011
   PubMed Web of Science ®Google Scholar
• Verstraeten, B. S. E., McCreary, J. K., Falkenberg, E. A., Fang, X., Weyers, S., Metz, G. A. S., & Olson, D. M. (2019). Multiple prenatal stresses increase sexual dimorphism in adult offspring behavior. Psychoneuroendocrinology, 107, 251–260. https://doi.org/10.1016/j.psyneuen.2019.05.003.
   PubMed Web of Science ®Google Scholar
• Viltart, O., Mairesse, J., Darnaudéry, M., Louvart, H., Vanbesien-Mailliot, C., Catalani, A., & Maccari, S. (2006). Prenatal stress alters Fos protein expression in hippocampus and locus coeruleus stress-related brain structures. Psychoneuroendocrinology, 31(6), 769–780. https://doi.org/10.1016/j.psyneuen.2006.02.007.
   PubMed Web of Science ®Google Scholar
• Wang, Y., Ma, Y., Cheng, W., Jiang, H., Zhang, X., Li, M., Ren, J., Zhang, X., & Li, X. (2015). 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. International Journal of Developmental Neuroscience, 41, 80–91. https://doi.org/10.1016/j.ijdevneu.2015.01.003
   PubMed Web of Science ®Google Scholar
• Weinstock, M. (2011). Sex-dependent changes induced by prenatal stress in cortical and hippocampal morphology and behaviour in rats: an update. Stress, 14(6), 604–613. https://doi.org/10.3109/10253890.2011.588294.
   PubMed Web of Science ®Google Scholar
• Weinstock, M. (2015). Changes induced by prenatal stress in behavior and brain morphology: Can they be prevented or reversed? Advances in Neurobiology, 10, 3–25. https://doi.org/10.1007/978-1-4939-1372-5_1
   PubMedGoogle Scholar
• Weinstock, M. (2017). Prenatal stressors in rodents: Effects on behavior. Neurobiology of Stress, 6, 3–13. https://doi.org/10.1016/j.ynstr.2016.08.004
   PubMed Web of Science ®Google Scholar
• Wohleb, E. S., Fenn, A. M., Pacenta, A. M., Powell, N. D., Sheridan, J. F., & Godbout, J. P. (2012). Peripheral innate immune challenge exaggerated microglia activation, increased the number of inflammatory CNS macrophages, and prolonged social withdrawal in socially defeated mice. Psychoneuroendocrinology, 37(9), 1491–1505. https://doi.org/10.1016/j.psyneuen.2012.02.003.
   PubMed Web of Science ®Google Scholar
• Wohleb, E. S., Hanke, M. L., Corona, A. W., Powell, N. D., Stiner, L. M., Bailey, M. T., Nelson, R. J., Godbout, J. P., & Sheridan, J. F. (2011). β-Adrenergic receptor antagonism prevents anxiety-like behavior and microglial reactivity induced by repeated social defeat. The Journal of Neuroscience, 31(17), 6277–6288. https://doi.org/10.1523/jneurosci.0450-11.2011
   PubMed Web of Science ®Google Scholar
• Won, E., & Kim, Y. K. (2020). Neuroinflammation-associated alterations of the brain as potential neural biomarkers in anxiety disorders. International Journal of Molecular Sciences, 21(18), 6546. https://doi.org/10.3390/ijms21186546
   Web of Science ®Google Scholar
• Wu, L. J., Kim, S. S., & Zhuo, M. (2008). Molecular targets of anxiety: From membrane to nucleus. Neurochemical Research, 33(10), 1925–1932. https://doi.org/10.1007/s11064-008-9679-8/
   PubMed Web of Science ®Google Scholar
• Xiao, X. L., Ma, D. L., Wu, J., & Tang, F. R. (2013). Metabotropic glutamate receptor 5 (mGluR5) regulates proliferation and differentiation of neuronal progenitors in the developmental hippocampus. Brain Research, 1493, 1–12. https://doi.org/10.1016/j.brainres.2012.11.015
   PubMed Web of Science ®Google Scholar
• Yaka, R., Salomon, S., Matzner, H., & Weinstock, M. (2007). Effect of varied gestational stress on acquisition of spatial memory, hippocampal LTP and synaptic proteins in juvenile male rats. Behavioural Brain Research, 179(1), 126–132. https://doi.org/10.1016/j.bbr.2007.01.018
   PubMed Web of Science ®Google Scholar
• Yip, J., Soghomonian, J.-J., & Blatt, G. J. (2008). Increased GAD67 mRNA expression in cerebellar interneurons in autism: Implications for Purkinje cell dysfunction. Journal of Neuroscience Research, 86(3), 525–530. https://doi.org/10.1002/jnr.21520.
   PubMed Web of Science ®Google Scholar
• Yoon, B. E., Woo, J., & Lee, C. J. (2012). Astrocytes as GABA-ergic and GABA-ceptive cells. Neurochemical Research, 37(11), 2474–2479. https://doi.org/10.1007/s11064-012-0808-z.
   PubMed Web of Science ®Google Scholar
• Zagron, G., & Weinstock, M. (2006). Maternal adrenal hormone secretion mediates behavioural alterations induced by prenatal stress in male and female rats. Behavioural Brain Research, 175(2), 323–328. https://doi.org/10.1016/j.bbr.2006.09.003
   PubMed Web of Science ®Google Scholar
• Zhang, X. H., Jia, N., Zhao, X. Y., Tang, G. K., Guan, L. X., Wang, D., Sun, H. L., Li, H., & Zhu, Z. L. (2013). Involvement of pGluR1, EAAT2 and EAAT3 in offspring depression induced by prenatal stress. Neuroscience, 250, 333–341. https://doi.org/10.1016/j.neuroscience.2013.04.031
   PubMed Web of Science ®Google Scholar
• Zhu, C., Liang, M., Li, Y., Feng, X., Hong, J., & Zhou, R. (2018). Involvement of epigenetic modifications of GABAergic interneurons in basolateral amygdala in anxiety-like phenotype of prenatally stressed mice. International Journal of Neuropsychopharmacology, 21(6), 570–581. https://doi.org/10.1093/ijnp/pyy006
   PubMed Web of Science ®Google Scholar
• Zimmerberg, B., & Blaskey, L. G. (1998). Prenatal stress effects are partially ameliorated by prenatal administration of the neurosteroid allopregnanolone. Pharmacology, Biochemistry, and Behavior, 59(4), 819–827. https://doi.org/10.1016/s0091-3057(97)00540-6
   PubMed Web of Science ®Google Scholar
• Zuena, A. R., Mairesse, J., Casolini, P., Cinque, C., Alemà, G. S., Morley-Fletcher, S., Chiodi, V., Spagnoli, L. G., Gradini, R., Catalani, A., Nicoletti, F., & Maccari, S. (2008). Prenatal restraint stress generates two distinct behavioral and neurochemical profiles in male and female rats. PLOS One, 3(5), e2170. https://doi.org/10.1371/journal.pone.0002170.
   PubMed Web of Science ®Google Scholar