Maternal exposure to environmental enrichment before and during gestation influences behaviour of rat offspring in a sex-specific manner

Zuena, Anna Rita; Zinni, Manuela; Giuli, Chiara; Cinque, Carlo; Alemà, G; Giuliani, Alessandro; Catalani, A.; Casolini, Paola; Cozzolino, Roberto

doi:10.1016/j.physbeh.2016.05.010

Cited by 30 publications

(28 citation statements)

References 75 publications

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“…Thus, it has been shown that maternal exposure to environmental enrichment before and during gestation increased social play behaviour in male (but not female) rats (Zuena et al 2016). Similarly, post-weaning environmental enrichment was shown to counteract the deleterious effects of prenatal stress on play behaviour and corticosterone secretion in rats (Morley-Fletcher et al, 2003).…”

Section: Introductionmentioning

confidence: 99%

The neurobiology of social play and its rewarding value in rats

Vanderschuren

Achterberg

Trezza

2016

Neuroscience & Biobehavioral Reviews

238

183

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In the young of many mammalian species, including humans, a vigorous and highly rewarding social activity is abundantly expressed, known as social play behaviour. Social play is thought to be important for the development of social, cognitive and emotional processes and their neural underpinnings, and it is disrupted in pediatric psychiatric disorders. Here, we summarize recent progress in our understanding of the brain mechanisms of social play behaviour, with a focus on its rewarding properties. Opioid, endocannabinoid, dopamine and noradrenaline systems play a prominent role in the modulation of social play. Of these, dopamine is particularly important for the motivational properties of social play. The nucleus accumbens has been identified as a key site for opioid and dopamine modulation of social play. Endocannabinoid influences on social play rely on the basolateral amygdala, whereas noradrenaline modulates social play through the basolateral amygdala, habenula and prefrontal cortex. In sum, social play behaviour is the result of coordinated activity in a network of corticolimbic structures, and its monoamine, opioid and endocannabinoid innervation.

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Section: Introductionmentioning

confidence: 99%

The neurobiology of social play and its rewarding value in rats

Vanderschuren

Achterberg

Trezza

2016

Neuroscience & Biobehavioral Reviews

238

183

View full text Add to dashboard Cite

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“…Moreover, when EE protocol involves the transition from the enriched gestational environment to the standard environment, the increase in some pup-directed behaviors may be a substitute to object exploration activity, given the decreased space and stimuli ( Rosenfeld and Weller, 2012 ). A similar explanation can be valid also if females enriched in groups before and during gestation are individually housed in enriched cages near parturition ( Zuena et al, 2016 ).…”

Section: Impact Of Differently Timed Parental Enrichment On Maternal mentioning

confidence: 80%

“…Mother rats enriched before and during gestation show heightened LG behavior and reduced pup nursing ( Zuena et al, 2016 ).…”

Section: Impact Of Differently Timed Parental Enrichment On Maternal mentioning

confidence: 99%

Pre-reproductive Parental Enriching Experiences Influence Progeny’s Developmental Trajectories

Cutuli

Berretta

Laricchiuta

et al. 2018

Front. Behav. Neurosci.

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While the positive effects of environmental enrichment (EE) applied after weaning, in adulthood, during aging, or even in the presence of brain damage have been widely described, the transgenerational effects of pre-reproductive EE have been less examined. And yet, this issue is remarkable given that parental environmental experience may imprint offspring’s phenotype over generations through many epigenetic processes. Interactions between individual and environment take place lifelong even before conception. In fact, the environment pre-reproductively experienced by the mother and/or the father exerts a substantial impact on neural development and motor and cognitive performances of the offspring, even if not directly exposed to social, cognitive, physical and/or motor enrichment. Furthermore, pre-reproductive parental enrichment exerts a transgenerational impact on coping response to stress as well as on the social behavior of the offspring. Among the effects of pre-reproductive parental EE, a potentiation of the maternal care and a decrease in global methylation levels in the frontal cortex and hippocampus of the progeny have been described. Finally, pre-reproductive EE modifies different pathways of neuromodulation in the brain of the offspring (involving brain-derived neurotrophic factor, oxytocin and glucocorticoid receptors). The present review highlights the importance of pre-reproductive parental enrichment in altering the performances not only of animals directly experiencing it, but also of their progeny, thus opening the way to new hypotheses on the inheritance mechanisms of behavioral traits.

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“…Maternal exercise before and during pregnancy is necessary to confer maximal beneficial effects to offspring, and this timing address the likelihood of epigenetic changes represent the underlying mechanism by which maternal exercise improves offspring's metabolic health (Harris et al, 2018). Several data, including from our laboratory, indicates that maternal intervention during pregnancy affects differentially male and female littermates (Marcelino et al, 2016;Noschang et al, 2012;Eclarinal et al, 2016;Zuena et al, 2016). On reason of this, in the present study we analyzed female and male parameters separately.…”

Section: Discussionmentioning

confidence: 98%

Swimming exercise before and during pregnancy: Promising preventive approach to impact offspring's health

Klein

Hözer

Couto-Pereira

et al. 2018

Intl J of Devlp Neuroscience

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Several environmental factors affect child development, such as the intrauterine environment during the embryonic and fetal development and early postnatal environment provided by maternal behavior. Although mechanistic effects of maternal exercise on offspring health improvement are not yet completely understood, the number of reports published demonstrating the positive influence of maternal exercise have increase. Herein, we addressed issues related to early postnatal environment provided by maternal behavior and early developmental physical landmarks, sensorimotor reflexes, and motor movements ontogeny. In brief, adult female rats underwent involuntary swimming exercise, in a moderated intensity, one week before mating and throughout pregnancy, 30 min a day, 5 days a week. Maternal exercised dams have unchanged gestational outcomes compared to sedentary dams. We found no differences concerning the frequency of pup-directed behavior displayed by dams. However, sedentary dams displayed a poorer pattern of maternal care quality during dark cycle than exercised dams. Physical landmarks and sensorimotor reflexes development of female and male littermates did not differ between maternal groups. Developmental motor parameters such as immobility, lateral head movements, head elevation, pivoting, rearing with forelimb support and crawling frequencies did not differ between groups. Pups born to exercised dams presented higher frequency of walking and rearing on the hind legs. These data suggest that female and male littermates of exercised group present a high frequency of exploratory behavior over sedentary littermates. Taken together, the present findings reinforce that maternal exercise throughout pregnancy represent a window of opportunity to improve offspring's postnatal health.

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Maternal exposure to environmental enrichment before and during gestation influences behaviour of rat offspring in a sex-specific manner

Cited by 30 publications

References 75 publications

The neurobiology of social play and its rewarding value in rats

The neurobiology of social play and its rewarding value in rats

Pre-reproductive Parental Enriching Experiences Influence Progeny’s Developmental Trajectories

Swimming exercise before and during pregnancy: Promising preventive approach to impact offspring's health

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