Pre-reproductive maternal enrichment influences rat maternal care and offspring developmental trajectories: behavioral performances and neuroplasticity correlates

Abstract

Environmental enrichment (EE) is a widely used paradigm for investigating the influence of complex stimulations on brain and behavior. Here we examined whether pre-reproductive exposure to EE of female rats may influence their maternal care and offspring cognitive performances. To this aim, from weaning to breeding age enriched females (EF) were reared in enriched environments. Females reared in standard conditions were used as controls. At 2.5 months of age all females were mated and reared in standard conditions with their offspring. Maternal care behaviors and nesting activity were assessed in lactating dams. Their male pups were also behaviorally evaluated at different post-natal days (pnd). Brain BDNF, reelin and adult hippocampal neurogenesis levels were measured as biochemical correlates of neuroplasticity. EF showed more complex maternal care than controls due to their higher levels of licking, crouching and nest building activities. Moreover, their offspring showed higher discriminative (maternal odor preference T-maze, pnd 10) and spatial (Morris Water Maze, pnd 45; Open Field with objects, pnd 55) performances, with no differences in social abilities (Sociability test, pnd 35), in comparison to controls. BDNF levels were increased in EF frontal cortex at pups' weaning and in their offspring hippocampus at pnd 21 and 55. No differences in offspring reelin and adult hippocampal neurogenesis levels were found. In conclusion, our study indicates that pre-reproductive maternal enrichment positively influences female rats' maternal care and cognitive development of their offspring, demonstrating thus a transgenerational transmission of EE benefits linked to enhanced BDNF-induced neuroplasticity.

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

“…Some studies investigating the effects of EE on maternal behaviour, showed a reduction in the time/frequency of nursing [20,23,46,51,52] and this is consistent with our results. L/G behaviour was increased with our protocol but only in the first two days of lactation; some studies show no differences [46,52], others a reduced [20,53] or an increased L/G and ABN behaviour [23,45,51].…”

“…L/G behaviour was increased with our protocol but only in the first two days of lactation; some studies show no differences [46,52], others a reduced [20,53] or an increased L/G and ABN behaviour [23,45,51]. Probably these contrasting data may be ascribed to the different EE protocols utilised or the timing of exposure.…”

“…We observed a gender effect also in spatial learning where only female offspring showed a better performance. Female offspring of EE mothers were never investigated in spatial learning, while it is reported that males improve spatial ability when maternal enrichment is performed during pregnancy [19] or in the prereproductive phase [23]. Again, in our study anxiety was affected in a sex specific way, showing an increase in male offspring but not in females in the EPM.…”

“…We can agree that our rats living in a complex environment with social and physical stimulation, had received a chronic mild physiological stress [10,71], which presumably caused an intermittent release of moderate amounts of corticosterone [72]. The hormone could have acted directly on the mother"s germ-line cells before pregnancy; in fact the progeny of mothers exposed to EE only in the pre-reproductive period shows an early development of complex motor skills associated with an increase of brain BDNF [22] and modifications of different behavioural parameters in adulthood [23,24]. We can also hypothesize that maternal corticosterone influenced the foetus during gestation crossing the placenta.…”

The BDNF Val66Met Polymorphism Interacts with Maternal Parenting Influencing Adolescent Depressive Symptoms: Evidence of Differential Susceptibility Model

“…Specifically, the Val66Met polymorphism has been shown to reduce intracellular trafficking and activity-dependent secretion of BDNF (Chen et al 2006;Egan et al 2003;Kuczewski et al 2009). Rodent studies indicate that maternal behavior including postnatal maternal separation (negative) and higher quality maternal care (positive) can influence offspring's BDNF expression in brain (Bath et al 2013;Cutuli et al 2015;Mashoodh et al 2012). Noteworthy, too, is accumulating evidence of the diverse role of BDNF on depression in different brain regions (Yu and Chen 2011), such that in the hippocampus BNDF inhibits depression (Duman and Monteggia 2006) whereas in the nucleus accumbens (NAc) it facilitates depression (Groves 2007;Martinowich et al 2007).…”