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Influence of Pre-reproductive Maternal Enrichment on Coping Response to Stress and Expression of c-Fos and Glucocorticoid Receptors in Adolescent Offspring.

ABSTRACT: Environmental enrichment (EE) is an experimental setting broadly used for investigating the effects of complex social, cognitive, and sensorimotor stimulations on brain structure and function. Recent studies point out that parental EE experience, even occurring in the pre-reproductive phase, affects neural development and behavioral trajectories of the offspring. In the present study we investigated the influences of pre-reproductive EE of female rats on maternal behavior and adolescent male offspring's coping response to an inescapable stressful situation after chronic social isolation. For this purpose female Wistar rats were housed from weaning to breeding age in enriched or standard environments. Subsequently, all females were mated and housed in standard conditions until offspring weaning. On the first post partum day (ppd 1), mother-pup interactions in undisturbed conditions were recorded. Further, after weaning the male pups were reared for 2 weeks under social isolation or in standard conditions, and then submitted or not to a single-session Forced Swim Test (FST). Offspring's neuronal activation and plastic changes were identified by immunohistochemistry for c-Fos and glucocorticoid receptors (GRs), and assessed by using stereological analysis. The biochemical correlates were measured in the hippocampus, amygdala and cingulate cortex, structures involved in hypothalamic-pituitary-adrenocortical axis regulation. Enriched dams exhibited increased Crouching levels in comparison to standard reared dams. In the offspring of both kinds of dams, social isolation reduced body weight, decreased Immobility, and increased Swimming during FST. Moreover, isolated offspring of enriched dams exhibited higher levels of Climbing in comparison to controls. Interestingly, in the amygdala of both isolated and control offspring of enriched dams we found a lower number of c-Fos immunopositive cells in response to FST and a higher number of GRs in comparison to the offspring of standard dams. These results highlight the profound influence of a stressful condition, such as the social isolation, on the brain of adolescent rats, and underline intergenerational effects of maternal experiences in regulating the offspring response to stress.

SUBMITTER: Cutuli D

PROVIDER: S-EPMC5422443 | biostudies-literature | 2017

REPOSITORIES: biostudies-literature

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Influence of Pre-reproductive Maternal Enrichment on Coping Response to Stress and Expression of c-Fos and Glucocorticoid Receptors in Adolescent Offspring.

Cutuli Debora D Berretta Erica E Pasqualini Greta G De Bartolo Paola P Caporali Paola P Laricchiuta Daniela D Sampedro-Piquero Patricia P Gelfo Francesca F Pesoli Matteo M Foti Francesca F Begega Azucena A Petrosini Laura L

Frontiers in behavioral neuroscience 20170509

Environmental enrichment (EE) is an experimental setting broadly used for investigating the effects of complex social, cognitive, and sensorimotor stimulations on brain structure and function. Recent studies point out that parental EE experience, even occurring in the pre-reproductive phase, affects neural development and behavioral trajectories of the offspring. In the present study we investigated the influences of pre-reproductive EE of female rats on maternal behavior and adolescent male off ...[more]

PMID: 28536510

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Project description:Pre-reproductive environmental enrichment of female rats influences sensorimotor development and spatial behavior of the offspring, possibly through the changed maternal nurturing. Nevertheless, maternal care could be not the solely responsible for changing offspring developmental trajectories. To disentangle the specific contribution to the transgenerational inheritance of pre- and post-natal factors, a cross-fostering study was performed. Female rats were reared in an enriched environment from weaning to sexual maturity, while control female rats were reared under standard conditions. Following mating with standard-reared males, all females were housed individually. Immediately after delivery, in- or cross-fostering manipulations were performed so that any foster dams received pups born to another dam of the same (in-fostering) or the opposite (cross-fostering) pre-reproductive rearing condition. In lactating dams maternal care and nesting activities were assessed, while in their male pups spatial abilities were assessed through Morris Water Maze (MWM) test at post-natal day 45. Moreover, the expression of Brain-Derived-Neurotrophic-Factor (BDNF) was evaluated in the hippocampus and frontal cortex of dams and pups at weaning. Pre-reproductive maternal environmental enrichment, followed by adoption procedures, loosened its potential in modifying maternal care and offspring developmental trajectories, as indicated by the lack of differences between in-fostered groups of dams and pups. In addition, enriched dams rearing standard pups showed the least complex maternal repertoire (the highest sniffing duration and the lowest nest quality), and their pups showed a reduced spatial learning in the MWM. Nevertheless, pre-reproductive maternal enrichment kept influencing neurotrophic pattern, with enriched dams expressing increased frontal BDNF levels (regardless of the kind of fostered pups), and their offspring expressing increased hippocampal BDNF levels. The present findings enlighten the crucial importance of the early mother-pups interactions in influencing maternal care and offspring phenotype, with the enriched dam-standard pups couple resulting in the most maladaptive encounter. Our study thus sustains that the bidirectional interactions between mother and pups are able to deeply shape offspring phenotype.

Project description:BackgroundResearch on parent-level factors linked to adolescent attachment security would inform interventions to prevent or reduce youth psychopathology and other negative outcomes. The current study examined one relevant parent-level variable: maternal interpersonal problems. Interpersonal problems, a key characteristic of personality pathology, are well described by the interpersonal circumplex (IPC) and have been shown to be associated with maladaptive adult attachment in close/romantic relationships; however, studies have not examined relationships with offspring attachment. Therefore, the first aim of the current study was to examine the relationship between maternal interpersonal problems and adolescent attachment insecurity. Based on previous evidence that parents' recalled bonding with caregivers is associated with the quality of bonding and attachment with offspring, the second aim was to examine whether mothers' recalled bonding with their own mothers partially explained this relationship.MethodsParticipants included 351 psychiatric inpatient adolescents (Mage = 15.26, 64.1% female) and their biological mothers. Logistic regressions tested whether maternal interpersonal problems were associated with Child Attachment Interview classifications (secure vs. insecure; secure vs. preoccupied vs. dismissing; not disorganized vs. disorganized). A mediation model (N = 210) tested whether the relationship between maternal interpersonal problems and adolescent attachment was mediated by the mother's recalled maternal bonding.ResultsMaternal interpersonal problems were associated with insecure (vs. secure), dismissing (vs. secure), and preoccupied (vs. secure) attachment. There was no significant relationship between maternal interpersonal problems and disorganized attachment. Mediation analyses showed that maternal interpersonal problems were indirectly related to adolescent attachment security via the mother's recalled maternal care, though only a small amount of variance (7%) in adolescent offspring attachment was accounted for by the model.ConclusionsResults provide the first evidence that maternal interpersonal problems are associated with higher likelihood of insecure attachment in adolescents. Therefore, researchers could consider drawing upon the IPC literature to further examine mechanisms of intergenerational risk and to tailor interventions aimed to improve parent-child relations and attachment. Additionally, findings highlight the mediating role of the mothers' recalled experiences with caregivers in the transmission of risk, suggesting attachment-based or mentalization-based interventions may be helpful for mothers with interpersonal problems and personality pathology.

Dataset Information

Influence of Pre-reproductive Maternal Enrichment on Coping Response to Stress and Expression of c-Fos and Glucocorticoid Receptors in Adolescent Offspring.

Publications

Influence of Pre-reproductive Maternal Enrichment on Coping Response to Stress and Expression of c-Fos and Glucocorticoid Receptors in Adolescent Offspring.

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