Weinstock M. The long-term behavioural consequences of prenatal stress. Neurosci Biobehav Rev. 2008;32:1073–86.
Karnwal R, Sharmila K. Perspective view of stress, anxiety, and depression among pregnant women: a review. JEOH. 2024;24:7–19.
Weinstock M. Prenatal stressors in rodents: effects on behavior. Neurobiol Stress. 2017;6:3–13.
Ross LE, McLean LM. Anxiety disorders during pregnancy and the postpartum period: a systematic review. J Clin Psychiatry. 2006;67:1285–98.
Lebel C, MacKinnon A, Bagshawe M, Tomfohr-Madsen L, Giesbrecht G. Elevated depression and anxiety symptoms among pregnant individuals during the COVID-19 pandemic. J Affect Disord. 2020;277:5–13.
Luo Y, Zhang K, Huang M, Qiu C. Risk factors for depression and anxiety in pregnant women during the COVID-19 pandemic: evidence from meta-analysis. PLoS One. 2022;17:e0265021.
Fisher J, Cabral de Mello M, Patel V, Rahman A, Tran T, Holton S, et al. Prevalence and determinants of common perinatal mental disorders in women in low- and lower-middle-income countries: a systematic review. Bull World Health Organ. 2012;90:139G–149G.
Woody CA, Ferrari AJ, Siskind DJ, Whiteford HA, Harris MG. A systematic review and meta-regression of the prevalence and incidence of perinatal depression. J Affect Disord. 2017;219:86–92.
Benoit JD, Rakic P, Frick KM. Prenatal stress induces spatial memory deficits and epigenetic changes in the hippocampus indicative of heterochromatin formation and reduced gene expression. Behav Brain Res. 2015;281:1–8.
Markham JA, Taylor AR, Taylor SB, Bell DB, Koenig JI. Characterization of the cognitive impairments induced by prenatal exposure to stress in the rat. Front Behav Neurosci. 2010;4:173.
Yang J, Han H, Cao J, Li L, Xu L. Prenatal stress modifies hippocampal synaptic plasticity and spatial learning in young rat offspring. Hippocampus. 2006;16:431–6.
Matrisciano F, Tueting P, Dalal I, Kadriu B, Grayson DR, Davis JM, et al. Epigenetic modifications of GABAergic interneurons are associated with the schizophrenia-like phenotype induced by prenatal stress in mice. Neuropharmacology. 2013;68:184–94.
Brachetta V, Schleich CE, Cutrera AP, Merlo JL, Kittlein MJ, Zenuto RR. Prenatal predatory stress in a wild species of subterranean rodent: do ecological stressors always have a negative effect on the offspring? Dev Psychobiol. 2018;60:567–81.
Holson RR, Gough B, Sullivan P, Badger T, Sheehan DM. Prenatal dexamethasone or stress but not ACTH or corticosterone alter sexual behavior in male rats. Neurotoxicol Teratol. 1995;17:393–401.
Merlot E, Couret D, Otten W. Prenatal stress, fetal imprinting and immunity. Brain Behav Immun. 2008;22:42–51.
St-Pierre J, Laurent L, King S, Vaillancourt C. Effects of prenatal maternal stress on serotonin and fetal development. Placenta. 2016;48:S66–S71.
Mueller BR, Bale TL. Sex-specific programming of offspring emotionality after stress early in pregnancy. J Neurosci. 2008;28:9055–65.
Dong E, Guidotti A, Zhang H, Pandey SC. Prenatal stress leads to chromatin and synaptic remodeling and excessive alcohol intake comorbid with anxiety-like behaviors in adult offspring. Neuropharmacology. 2018;140:76–85.
Matrisciano F, Dong E, Nicoletti F, Guidotti A. Epigenetic alterations in prenatal stress mice as an endophenotype model for schizophrenia: role of metabotropic glutamate 2/3 receptors. Front Mol Neurosci. 2018;11:423.
Sheriff MJ, Bell A, Boonstra R, Dantzer B, Lavergne SG, McGhee KE, et al. Integrating ecological and evolutionary context in the study of maternal stress. Integr Comp Biol. 2017;57:437–49.
Verdolin JL. Meta-analysis of foraging and predation risk trade-offs in terrestrial systems. Behav Ecol Sociobiol. 2006;60:457–64.
St-Cyr S, McGowan PO. Programming of stress-related behavior and epigenetic neural gene regulation in mice offspring through maternal exposure to predator odor. Front Behav Neurosci. 2015;9:145.
St-Cyr S, Abuaish S, Spinieli RL, McGowan PO. Maternal predator odor exposure in mice programs adult offspring social behavior and increases stress-induced behaviors in semi-naturalistic and commonly-used laboratory tasks. Front Behav Neurosci. 2018;12:136.
St-Cyr S, Abuaish S, Sivanathan S, McGowan PO. Maternal programming of sex-specific responses to predator odor stress in adult rats. Horm Behav. 2017;94:1–12.
Wu Y, Bian J, Liu J. Effects of predator-induced maternal stress on offspring’s locomotor activity and exploring behavior in root voles. Acta Theriol Sin. 2006;26:235–40.
Chen G, Shi D. Study on reproductive behavior of different social hierarchy of Brandt’s voles (Lasiopodomys Brandtii). Acta Theriol Sin. 2003;23:220–4.
Liu Z, Sun R. Study on physiological age structure of Brandt’s voles (Microtus brandti). Acta Theriol Sin. 1993;13:50–60.
Yu X, Sun R, Fang J. Effect of kinship on social behaviors in Brandt’s voles (Microtus brandti). J Ethol. 2004;22:17–22.
Liu XH, Yue LF, Wang DW, Li N, Cong L. Inbreeding avoidance drives consistent variation of fine-scale genetic structure caused by dispersal in the seasonal mating system of Brandt’s voles. PloS one. 2013;8:e58101.
Wu R, Jiang X, Wu X, Pang J, Tang Y, Ren Z, et al. Interspecific differences in sociability, social novelty preference, anxiety- and depression-like behaviors between Brandt’s voles and C57BL/6J mice. Behav Processes. 2022;197:104624.
Hegab IM, Wang A, Yin B, Yang S, Wei W. Behavioral and neuroendocrine response of Brandt’s voles, Lasiopodomys brandtii, to odors of different species. Eur J Wildlife Res. 2014;60:331–40.
Hegab IM, Shang G, Ye M, Jin Y, Wang A, Yin B, et al. Defensive responses of Brandt’s voles (Lasiopodomys brandtii) to chronic predatory stress. Physiol Behav. 2014;126:1–7.
Peng Y, Wu Y, Gu C, Yang S, Yin B, Wei W. Effects of repeated exposure to cat odor on anti-predator and anxiety-like behaviors of juvenile Brandt’s voles (Lasiopodomys brandtii). Acta Theriol Sin. 2021;41:451–8.
Gu C, Wang W, Ding X, Yang S, Wang A, Yin B, et al. Effects of maternal stress induced by predator odors during gestation on behavioral and physiological responses of offspring in Brandt’s vole (Lasiopodomys brandtii). Integr Zool. 2018;13:723–34.
Gu C, Xu Z, Chen L, Gu M, Yang S, Wang A, et al. Effects of maternal stress on the behavioral and HPA responses of offspring exposed to the predator or non-predator odor in Brandt’s voles. Pakistan J Zool. 2023;55:2151–61.
Pang J, Li S, Liu Y, Yang S, Wu R, Wei W. Adolescent predatory risk alters the antipredator behavior and basal HPA axis activity of future offspring in Brandt’s voles. Acta Theriol Sin. 2022;42:177–88.
Wu R, Li S, Huang Y, Pang J, Cai Y, Zhang X, et al. Postpartum maternal exposure to predator odor alters offspring antipredator behavior, basal HPA axis activity and immunoglobulin levels in adult Brandt’s voles. Behav Brain Res. 2022;416:113532.
Wu R, Wang W, Zheng Y, Li S, Zhang L, Pang J, et al. Maternal predation risk during pregnancy alters various social behaviors in the offspring of Brandt’s voles. Behav Ecol Sociobiol. 2023;77:121.
Anacker C, Luna VM, Stevens GS, Millette A, Shores R, Jimenez JC, et al. Hippocampal neurogenesis confers stress resilience by inhibiting the ventral dentate gyrus. Nature. 2018;559:98–102.
Yagi S, Galea LAM. Sex differences in hippocampal cognition and neurogenesis. Neuropsychopharmacology. 2019;44:200–13.
Liu MY, Wei LL, Zhu XH, Ding HC, Liu XH, Li H, et al. Prenatal stress modulates HPA axis homeostasis of offspring through dentate TERT independently of glucocorticoids receptor. Mol Psychiatry. 2023;28:1383–95.
Christie BR, Cameron HA. Neurogenesis in the adult hippocampus. Hippocampus. 2006;16:199–207.
Eriksson PS, Perfilieva E, Bjork-Eriksson T, Alborn AM, Nordborg C, Peterson DA, et al. Neurogenesis in the adult human hippocampus. Nat Med. 1998;4:1313–7.
McEwen BS. Redefining neuroendocrinology: epigenetics of brain-body communication over the life course. Front Neuroendocrinol. 2018;49:8–30.
Artola A, von Frijtag JC, Fermont PCJ, Gispen WH, Schrama LH, Kamal A, et al. Long-lasting modulation of the induction of LTD and LTP in rat hippocampal CA1 by behavioural stress and environmental enrichment. Eur J Neurosci. 2006;23:261–72.
Lemaire V, Koehl M, Le Moal M, Abrous DN. Prenatal stress produces learning deficits associated with an inhibition of neurogenesis in the hippocampus. Proc Natl Acad Sci USA. 2000;97:11032–7.
Belnoue L, Grosjean N, Ladeveze E, Abrous DN, Koehl M. Prenatal stress inhibits hippocampal neurogenesis but spares olfactory bulb neurogenesis. PLoS One. 2013;8:e72972.
Zheng X, Wang X, Wang T, Zhang H, Wu H, Zhang C, et al. Gestational exposure to particulate matter 2.5 (PM2.5) leads to spatial memory dysfunction and neurodevelopmental impairment in hippocampus of mice offspring. Front Neurosci. 2019;12:1000.
Bock J, Murmu MS, Biala Y, Weinstock M, Braun K. Prenatal stress and neonatal handling induce sex-specific changes in dendritic complexity and dendritic spine density in hippocampal subregions of prepubertal rats. Neuroscience. 2011;193:34–43.
Wu YP, Gao HY, Ouyang SH, Kurihara H, He RR, Li YF. Predator stress-induced depression is associated with inhibition of hippocampal neurogenesis in adult male mice. Neural Regen Res. 2019;14:298–305.
Cohen H, Matar MA, Todder D, Cohen C, Zohar J, Hawlena H, et al. Sounds of danger and post-traumatic stress responses in wild rodents: ecological validity of a translational model of post-traumatic stress disorder. Mol Psychiatry. 2023;28:4719–28.
Wu R, Huang Y, Liu Y, Shen Q, Han Y, Yang S, et al. Repeated predator odor exposure alters maternal behavior of postpartum Brandt’s voles and offspring’s locomotor activity. Behav Processes. 2020;177:104143.
Markus EJ, Zecevic M. Sex differences and estrous cycle changes in hippocampus-dependent fear conditioning. Psychobiology. 1997;25:246–52.
Paris JJ, Frye CA. Estrous cycle, pregnancy, and parity enhance performance of rats in object recognition or object placement tasks. Reproduction. 2008;136:105–15.
Wu R, Pang J, Xu Z, Wu X, Wang W, Zheng Y, et al. Adolescence predatory risk alters social behaviors and cognitive ability and central oxytocin and vasopressin expression in adult Brandt’s voles. Neuroendocrinology. 2023;113:519–34.
Pascual R, Valencia M, Bustamante C. Antenatal betamethasone produces protracted changes in anxiety-like behaviors and in the expression of microtubule-associated protein 2, brain-derived neurotrophic factor and the tyrosine kinase B receptor in the rat cerebellar cortex. Int J Dev Neurosci. 2015;43:78–85.
Kiryanova V, Meunier SJ, Dyck RH. Behavioural outcomes of adult female offspring following maternal stress and perinatal fluoxetine exposure. Behav Brain Res. 2017;331:84–91.
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. 2015;101:15–23.
Coe CL, Kramer M, Czeh B, Gould E, Reeves AJ, Kirschbaum C, et al. Prenatal stress diminishes neurogenesis in the dentate gyrus of juvenile rhesus monkeys. Biol Psychiatry. 2003;54:1025–34.
Willner P, Scheel-Kruger J, Belzung C. The neurobiology of depression and antidepressant action. Neurosci Biobehav Rev. 2013;37:2331–71.
Zoladz PR, Diamond DM. Predator-based psychosocial stress animal model of PTSD: preclinical assessment of traumatic stress at cognitive, hormonal, pharmacological, cardiovascular and epigenetic levels of analysis. Exp Neurol. 2016;284:211–9.
Righetti-Veltema M, Conne-Perreard E, Bousquet A, Manzano J. Postpartum depression and mother-infant relationship at 3 months old. J Affect Disord. 2002;70:291–306.
Bauer CM, Hayes LD, Ebensperger LA, Ramirez-Estrada J, Leon C, Davis GT, et al. Maternal stress and plural breeding with communal care affect development of the endocrine stress response in a wild rodent. Horm Behav. 2015;75:18–24.
Mashoodh R, Sinal CJ, Perrot-Sinal TS. Predation threat exerts specific effects on rat maternal behaviour and anxiety-related behaviour of male and female offspring. Physiol Behav. 2009;96:693–702.
Bosch OJ, Pohl TT, Neumann ID, Young LJ. Abandoned prairie vole mothers show normal maternal care but altered emotionality: Potential influence of the brain corticotropin-releasing factor system. Behav Brain Res. 2018;341:114–21.
Alves RL, Portugal CC, Lopes IM, Oliveira P, Alves CJ, Barbosa F, et al. Maternal stress and vulnerability to depression: coping and maternal care strategies and its consequences on adolescent offspring. Transl Psychiatry. 2022;12:463.
Sullivan EL, Smith MS, Grove KL. Perinatal exposure to high-fat diet programs energy balance, metabolism and behavior in adulthood. Neuroendocrinology. 2011;93:1–8.
Cottrell EC, Holmes MC, Livingstone DE, Kenyon CJ, Seckl JR. Reconciling the nutritional and glucocorticoid hypotheses of fetal programming. FASEB J. 2012;26:1866–74.
Curley JP, Champagne FA. Influence of maternal care on the developing brain: Mechanisms, temporal dynamics and sensitive periods. Front Neuroendocrinol. 2016;40:52–66.
Moore CL, Morelli GA. Mother rats interact differently with male and female offspring. J Comp Physiol Psychol. 1979;93:677–84.
Hiroi R, Carbone DL, Zuloaga DG, Bimonte-Nelson HA, Handa RJ. Sex-dependent programming effects of prenatal glucocorticoid treatment on the developing serotonin system and stress-related behaviors in adulthood. Neuroscience. 2016;320:43–56.
Krusemark EA, Novak LR, Gitelman DR, Li W. When the sense of smell meets emotion: anxiety-state-dependent olfactory processing and neural circuitry adaptation. J Neurosci. 2013;33:15324–32.
Bontempi C, Jacquot L, Brand G. A study on the relationship between odor hedonic ratings and individual odor detection threshold. Sci Rep. 2022;12:18482.
Shah A, Oxley G, Lovic V, Fleming AS. Effects of preweaning exposure to novel maternal odors on maternal responsiveness and selectivity in adulthood. Dev Psychobiol. 2002;41:187–96.
Marr JN, Gardner Jr LE. Early olfactory experience and later social behavior in the rat: preference, sexual responsiveness, and care of young. J Genet Psychol. 1965;107:167–74.
Dias BG, Ressler KJ. Parental olfactory experience influences behavior and neural structure in subsequent generations. Nat Neurosci. 2014;17:89–96.
Abe H, Hidaka N, Kawagoe C, Odagiri K, Watanabe Y, Ikeda T, et al. Prenatal psychological stress causes higher emotionality, depression-like behavior, and elevated activity in the hypothalamo-pituitary-adrenal axis. Neurosci Res. 2007;59:145–51.
Jia N, Li Q, Sun H, Song Q, Tang G, Sun Q, et al. Alterations of group I mGluRs and BDNF associated with behavioral abnormity in prenatally stressed offspring rats. Neurochem Res. 2015;40:1074–82.
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. Psychopharmacology (Berl). 2015;232:1643–53.
Pawluski JL, Csaszar E, Savage E, Martinez-Claros M, Steinbusch HWM, van den Hove D. Effects of stress early in gestation on hippocampal neurogenesis and glucocorticoid receptor density in pregnant rats. Neuroscience. 2015;290:379–88.
Bock J, Wainstock T, Braun K, Segal M. Stress in utero: prenatal programming of brain plasticity and cognition. Biol Psychiatry. 2015;78:315–26.
Iribarne J, Brachetta V, Kittlein M, Schleich C, Zenuto R. Effects of acute maternal stress induced by predator cues on spatial learning and memory of offspring in the subterranean rodent Ctenomys talarum. Anim Cogn. 2023;26:1997–2008.
Lian B, Gao J, Sui N, Feng T, Li M. Object, spatial and social recognition testing in a single test paradigm. Neurobiol Learn Mem. 2018;152:39–49.
Grundwald NJ, Benitez DP, Brunton PJ. Sex-dependent effects of prenatal stress on social memory in rats: a role for differential expression of central vasopressin-1a receptors. J Neuroendocrinol. 2016;28:n/a.
Lee PR, Brady DL, Shapiro RA, Dorsa DM, Koenig JI. Prenatal stress generates deficits in rat social behavior: reversal by oxytocin. Brain Res. 2007;1156:152–67.
Wilson CA, Terry Jr AV. Variable maternal stress in rats alters locomotor activity, social behavior, and recognition memory in the adult offspring. Pharmacol Biochem Behav. 2013;104:47–61.
Ehrlich DE, Rainnie DG. Prenatal stress alters the development of socioemotional behavior and amygdala neuron excitability in rats. Neuropsychopharmacology. 2015;40:2135–45.
Gur TL, Palkar AV, Rajasekera T, Allen J, Niraula A, Godbout J, et al. Prenatal stress disrupts social behavior, cortical neurobiology and commensal microbes in adult male offspring. Behav Brain Res. 2019;359:886–94.
Gur TL, Shay L, Palkar AV, Fisher S, Varaljay VA, Dowd S, et al. Prenatal stress affects placental cytokines and neurotrophins, commensal microbes, and anxiety-like behavior in adult female offspring. Brain Behav Immun. 2017;64:50–8.
Beery AK, Kaufer D. Stress, social behavior, and resilience: insights from rodents. Neurobiol Stress. 2015;1:116–27.
Sams-Dodd F. Phencyclidine in the social interaction test: an animal model of schizophrenia with face and predictive validity. Rev Neurosci. 1999;10:59–90.
Sapolsky RM. Is impaired neurogenesis relevant to the affective symptoms of depression? Biol Psychiatry. 2004;56:137–9.
Drew MR, Hen R. Adult hippocampal neurogenesis as target for the treatment of depression. CNS Neurol Disord Drug Targets. 2007;6:205–18.
Snyder JS, Soumier A, Brewer M, Pickel J, Cameron HA. Adult hippocampal neurogenesis buffers stress responses and depressive behaviour. Nature. 2011;476:458–61.
Sorra KE, Harris KM. Overview on the structure, composition, function, development, and plasticity of hippocampal dendritic spines. Hippocampus. 2000;10:501–11.
Koehl M, Lemaire V, Le Moal M, Abrous DN. Age-dependent effect of prenatal stress on hippocampal cell proliferation in female rats. Eur J Neurosci. 2009;29:635–40.
Lucassen PJ, Bosch OJ, Jousma E, Kromer SA, Andrew R, Seckl JR, et al. Prenatal stress reduces postnatal neurogenesis in rats selectively bred for high, but not low, anxiety: possible key role of placental 11beta-hydroxysteroid dehydrogenase type 2. Eur J Neurosci. 2009;29:97–103.
Paris JJ, Frye CA. Juvenile offspring of rats exposed to restraint stress in late gestation have impaired cognitive performance and dysregulated progestogen formation. Stress. 2011;14:23–32.
Hosseini-Sharifabad M, Hadinedoushan H. Prenatal stress induces learning deficits and is associated with a decrease in granules and CA3 cell dendritic tree size in rat hippocampus. Anat Sci Int. 2007;82:211–7.
Martinez-Tellez RI, Hernandez-Torres E, Gamboa C, Flores G. Prenatal stress alters spine density and dendritic length of nucleus accumbens and hippocampus neurons in rat offspring. Synapse. 2009;63:794–804.
Jia N, Yang K, Sun Q, Cai Q, Li H, Cheng D, et al. Prenatal stress causes dendritic atrophy of pyramidal neurons in hippocampal CA3 region by glutamate in offspring rats. Dev Neurobiol. 2010;70:114–25.
Bustamante C, Valencia M, Torres C, Gonzalez MJ, Carvajal C, Sandoval D, et al. Effects of a single course of prenatal betamethasone on dendritic development in dentate gyrus granular neurons and on spatial memory in rat offspring. Neuropediatrics. 2014;45:354–61.
Wu Y, De Asis-Cruz J, Limperopoulos C. Brain structural and functional outcomes in the offspring of women experiencing psychological distress during pregnancy. Mol Psychiatry. 2024;29:2223–40.