Maternal stress during pregnancy causes sex-specific alterations in offspring memory performance, social interactions, indices of anxiety

Department of Psychiatry, University of Colorado Denver, Aurora, CO 80045, USA.
Physiology & Behavior (Impact Factor: 2.98). 02/2011; 104(2):340-7. DOI: 10.1016/j.physbeh.2011.02.021
Source: PubMed


Prenatal stress (PS) impairs memory function; however, it is not clear whether PS-induced memory deficits are specific to spatial memory, or whether memory is more generally compromised by PS. Here we sought to distinguish between these possibilities by assessing spatial, recognition and contextual memory functions in PS and nonstressed (NS) rodents. We also measured anxiety-related and social behaviors to determine whether our unpredictable PS paradigm generates a behavioral phenotype comparable to previous studies. Female Sprague-Dawley rats were exposed to daily random stress during the last gestational week and behavior tested in adulthood. In males but not females, PS decreased memory for novel objects and novel spatial locations, and facilitated memory for novel object/context pairings. In the elevated zero maze, PS increased anxiety-related behavior only in females. Social behaviors also varied with sex and PS condition. Females showed more anogenital sniffing regardless of stress condition. In contrast, prenatal stress eliminated a male-biased sex difference in nonspecific bodily sniffing by decreasing sniffing in males, and increasing sniffing in females. Finally, PS males but not females gained significantly more weight across adulthood than did NS controls. In summary, these data indicate that PS differentially impacts males and females resulting in sex-specific adult behavioral and bodily phenotypes.

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Available from: Kalynn M Schulz, Oct 04, 2015
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    • "The consequences following prenatal stress exposure often di®er according to the stressor and its timing. For instance, if the stress is applied in the second half of pregnancy, impaired memory function (Markham et al., 2010; Modir et al., 2014), sexual and social abnormalities (Meisel et al., 1979; Schulz et al., 2011) may occur. Furthermore, early adverse life events are known to alter anxiety-like behavior in o®spring. "
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    ABSTRACT: We assess the anxiety-like behavior in the open field and elevated plus maze tests and measure the nociceptive response in the tail flick test following prenatal stress exposure in adult male and female Wistar rats. In both behavioral anxiety tests, prenatal stress increased the anxiety-like behavior in male PS rats, but not in females suggesting a strong sex-dependent anxiogenic effect. The tail flick results showed a hypersensitivity to pain in male and female PS rats with a subtle gender difference. These findings suggest that prenatal stress is an important risk factor for multiple mental disorders.
    Journal of Integrative Neuroscience 04/2015; 14(02):1-12. DOI:10.1142/S0219635215500107 · 0.94 Impact Factor
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    • "10 , Mychasiuk , Gibb , & Kolb , 2011 ; Weinstock , 2007 , 2011 ; Zohar & Wein - stock , 2011 ) . 1 For example , in a number of studies , pregnant rats were exposed to daily random stress during the last gesta - tional week , and behavior was tested in the adult offspring . Female , but not male , offspring showed anxiety - related be - haviors ( Schulz et al . , 2011 * ) ; reduced exploration of the open arms of an experimental maze , a marker for increased anxiety ( Zagron & Weinstock , 2006 ) ; and increased length of immobility in the forced swim test , a model of depression ( Frye & Wawrzycki , 2003 ) . Adrenalectomy of the rat mothers eliminated the effect of prenatal stress in female offspring"
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    ABSTRACT: Associations between low birth weight and prenatal anxiety and later psychopathology may arise from programming effects likely to be adaptive under some, but not other, environmental exposures and modified by sex differences. If physiological reactivity, which also confers vulnerability or resilience in an environment-dependent manner, is associated with birth weight and prenatal anxiety, it will be a candidate to mediate the links with psychopathology. From a general population sample of 1,233 first-time mothers recruited at 20 weeks gestation, a sample of 316 stratified by adversity was assessed at 32 weeks and when their infants were aged 29 weeks (N = 271). Prenatal anxiety was assessed by self-report, birth weight from medical records, and vagal reactivity from respiratory sinus arrhythmia during four nonstressful and one stressful (still-face) procedure. Lower birth weight for gestational age predicted higher vagal reactivity only in girls (interaction term, p = .016), and prenatal maternal anxiety predicted lower vagal reactivity only in boys (interaction term, p = .014). These findings are consistent with sex differences in fetal programming, whereby prenatal risks are associated with increased stress reactivity in females but decreased reactivity in males, with distinctive advantages and penalties for each sex.
    Development and Psychopathology 04/2014; 26(4):1-10. DOI:10.1017/S0954579414000194 · 4.89 Impact Factor
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    • "Maternal stress is associated with increased offspring anxiety and depressive-related behaviors in humans [1] and animals [2] [3] [4] [5] [6]. "
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    ABSTRACT: Brain cholinergic dysfunction is associated with neuropsychiatric illnesses such as depression, anxiety, and schizophrenia. Maternal stress exposure is associated with these same illnesses in adult offspring, yet the relationship between prenatal stress and brain cholinergic function is largely unexplored. Thus, using a rodent model, the current study implemented an intervention aimed at buffering the potential effects of prenatal stress on the developing brain cholinergic system. Specifically, control and stressed dams were fed choline-supplemented or control chow during pregnancy and lactation, and the anxiety-related behaviors of adult offspring were assessed in the open field, elevated zero maze and social interaction tests. In the open field test, choline supplementation significantly increased center investigation in both stressed and nonstressed female offspring, suggesting that choline-supplementation decreases female anxiety-related behavior irrespective of prenatal stress exposure. In the elevated zero maze, prenatal stress increased anxiety-related behaviors of female offspring fed a control diet (normal choline levels). However, prenatal stress failed to increase anxiety-related behaviors in female offspring receiving supplemental choline during gestation and lactation, suggesting that dietary choline supplementation ameliorated the effects of prenatal stress on anxiety-related behaviors. For male rats, neither prenatal stress nor diet impacted anxiety-related behaviors in the open field or elevated zero maze. In contrast, perinatal choline supplementation mitigated prenatal stress-induced social behavioral deficits in males, whereas neither prenatal stress nor choline supplementation influenced female social behaviors. Taken together, these data suggest that perinatal choline supplementation ameliorates the sex-specific effects of prenatal stress.
    Behavioural brain research 03/2014; 271. DOI:10.1016/j.bbr.2014.03.031 · 3.03 Impact Factor
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