Maternal Programming of Defensive Responses Through Sustained Effects on Gene Expression

Journal of psychiatry & neuroscience: JPN (Impact Factor: 5.86). 07/2007; 32(4). DOI: 10.1093/acprof:oso/9780195306255.003.0007


There are profound maternal effects on individual differences in defensive responses in species ranging from plants to insects to birds. In this paper, we review data from the rat that suggest comparable forms of maternal effects on defensive responses to stress, which are mediated by the effects of variations in maternal behaviour on gene expression. Under conditions of environmental adversity, maternal effects enhance the capacity for defensive responses in the offspring. These effects appear to "program" emotional, cognitive and endocrine systems toward increased sensitivity to adversity. In environments with an increased level of adversity, such effects can be considered adaptive, enhancing the capacity for responses that have immediate adaptive value; the cost is an increased risk for multiple forms of pathology in later life.

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    • "64 A. Sequeira-Cordero et al. / Behavioural Brain Research 237 (2013) 63– 70 limbic regions such as the hippocampus (HPC), cortical structures such as the prefrontal cortex (PFC) and striatal subregions such as the nucleus accumbens (NAc) [13] [15] [16]. Differential maternal care investment has a profound impact on hippocampal function affecting the expression of hundreds of genes [11] [17]. One of these genes is the brain-derived neurotrophic factor (BDNF) [18] [19] [20]. "
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    ABSTRACT: Maternal care plays an important role as an early modeler of neurodevelopment and brain function, and its effects remain until adulthood. Such modeling or programming has shown to influence the stress response and represents a key susceptibility factor in the development of mood disorders. In order to characterize such process which is still not clear, male offspring were classified in animals with low, medium and high licking/grooming (LG) according to the maternal behavior. Juvenile animals were subjected to the open field test (OFT) and the forced swimming test (FST), and offspring of low and high LG mothers were compared. Seven days after the FST, neurochemical and gene expression analyses were carried out in order to identify possible changes on relevant targets. Maternal care did determine locomotor behaviors in the OFT, supporting an anxiogenic effect of low maternal investment. This effect seems to be associated with the serotonergic systems in both nucleus accumbens (NAc) and hippocampus (HPC), since offspring of low LG mothers showed decreased 5-HT neurotransmission in those brain regions compared with animals of high LG mothers. Furthermore, TrkB expression was higher in offspring of high LG compared to the group of low LG mothers, supporting its influence as a mechanistic intermediate of such effect, at least in the NAc. Taken together, these findings strongly support the influence of differential maternal care on the neurodevelopment and responsivity of juvenile rats.
    Full-text · Article · Sep 2012 · Behavioural brain research
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    • "These effects are essentially reversed with cross fostering, suggesting a direct effect of maternal care (Francis et al., 1999; Caldji et al., 2003). The maternal effects on behavioral and HPA responses to stress depend on, at least in part, epigenetic programming of gene expression (Meaney and Szyf, 2005; Diorio and Meaney, 2007). However, such effects, and especially those on hippocampaldependent forms of learning and memory, may also involve differences in synaptic plasticity. "
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    ABSTRACT: Maternal licking and grooming (LG) in infancy influences stress responsiveness and cognitive performance in the offspring. We examined the effects of variation in the frequency of pup LG on morphological, electrophysiological, and behavioral aspects of hippocampal synaptic plasticity under basal and stress-like conditions. We found shorter dendritic branch length and lower spine density in CA1 cells from the adult offspring of low compared with high LG offspring. We also observed dramatic effects on long-term potentiation (LTP) depending on corticosterone treatment. Low LG offspring, in contrast to those of high LG mothers, displayed significantly impaired LTP under basal conditions but surprisingly a significantly enhanced LTP in response to high corticosterone in vitro. This enhanced plasticity under conditions that mimic those of a stressful event was apparent in vivo. Adult low LG offspring displayed enhanced memory relative to high LG offspring when tested in a hippocampal-dependent, contextual fear-conditioning paradigm. Hippocampal levels of glucocorticoid and mineralocorticoid receptors were reduced in low compared with high LG offspring. Such effects, as well as the differences in dendritic morphology, likely contribute to LTP differences under resting conditions, as well as to the maternal effects on synaptic plasticity and behavior in response to elevated corticosterone levels. These results suggest that maternal effects may modulate optimal cognitive functioning in environments varying in demand in later life, with offspring of high and low LG mothers showing enhanced learning under contexts of low and high stress, respectively.
    Full-text · Article · Jun 2008 · The Journal of Neuroscience : The Official Journal of the Society for Neuroscience
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