Importance of early lighting conditions in maternal care by dam as well as anxiety and memory later in life of offspring

Abstract

Rodent studies have revealed that the early rearing environment plays an important role in the development of stress vulnerability, memory and cognition. Although early lighting conditions (ELC) are involved in these neuronal developments through both maternal and offspring behavior, their influence has not been fully elucidated. Thus, by using Sprague-Dawley rats, we examined whether ELC affected maternal care by the dam and the subsequent neurodevelopment of the offspring. Prolonged dark phase conditions (PDC) (light/dark, 6/18 h) and prolonged light phase conditions (light/dark, 18/6 h) were administered from postnatal day 2 to postnatal day 14. Throughout this period, maternal care and the circadian rhythmicity of dams were investigated. In adolescence and adulthood of the offspring, we measured anxiety-like behavior, social interaction, object recognition memory, activity rhythm and corticosterone response to stress with hippocampal expression of N-methyl-D-aspartate and glucocorticoid receptor mRNAs. PDC altered maternal care and circadian rhythmicity in the dam compared with normal lighting conditions and prolonged light phase conditions. PDC markedly increased anxiety-like behavior, decreased social interaction and object recognition memory, and inhibited corticosterone feedback in offspring later in life. Furthermore, hippocampal levels of glucocorticoid receptor mRNA and N-methyl-D-aspartate receptor 2B mRNA in rats subjected to PDC were significantly lower than in animals subjected to normal lighting conditions. In the adult offspring, the circadian rhythm of locomotor activity was not affected. These findings suggested that ELC affect mother-infant interactions and subsequently at least partially alter the neurobehavioral development of offspring.

Maternal Care and Hippocampal Plasticity: Evidence for Experience-Dependent Structural Plasticity, Altered Synaptic Functioning, and Differential Responsiveness to Glucocorticoids and Stress

“…In the rat, naturally occurring variations in the frequency of pup licking and grooming (LG) provided by the dam during the first week of life are associated with individual differences in stress responsiveness, emotionality, and cognitive functioning in adult offspring. As adults, offspring of low compared with high LG mothers show increased hypothalamus-pituitary-adrenal (HPA) responses to stress (Liu et al, 1997;Weaver et al, 2004Weaver et al, , 2005, enhanced emotionality (Caldji et al, 1998;Menard and Hakvoort, 2007), and impaired performance in tests of spatial learning and object recognition (Liu et al, 2000;Bredy et al, 2003Bredy et al, , 2004Toki et al, 2007). These effects are essentially reversed with cross fostering, suggesting a direct effect of maternal care (Francis et al, 1999;Caldji et al, 2003).…”

“…However, such effects, and especially those on hippocampaldependent forms of learning and memory, may also involve differences in synaptic plasticity. Indeed, maternal care alters the expression of synaptophysin, growth factors, and selected glutamate receptor subunits (Liu et al, 2000;Bredy et al, 2003Bredy et al, , 2004Toki et al, 2007). However, potential effects on the structure and function of hippocampal neurons have not been examined and are of particular relevance in light of studies suggesting parental effects on hippocampal volume in humans (Vythilingam et al, 2002;Buss et al, 2007) and of consistent reports of decreased hippocampal volume in patients with mood disorders (Sheline et al, 1996;Bremner et al, 2000).…”

Environmental regulation of the neural epigenome

“…Variations in pup LG in the rat directly affect the development of behavioral and hypothalamic-pituitary-adrenal (HPA) responses to stress in adulthood [25][26][27][28][29][30][31][32][33]. Rat mothers exhibit considerable naturallyoccurring variations in the frequency of pup LG over the first week A schema outlining the function of the hypothalamic-pituitary-adrenal axis, the nexus of which are the corticotropin-releasing factor (CRF) neurons of the paraventricular nucleus of the hypothalamus.…”

“…Thus, maternal stress reduces the frequency of pup LG and decreases hippocampal GR expression in the offspring [23]; such effects are directly mediated by the decrease in postnatal pup LG. Manipulations, such as the brief handling of pups by the experimenter, that increase the frequency of pup LG by the mother increase hippocampal glucocorticoid receptor expression, decrease that of CRF in the hypothalamus and dampen HPA responses to stress [28,33,37]. Finally, the frequency of pup LG is also influenced by light cycles that mimic the daylight associated with seasonal change [33].…”

Maternal Care and DNA Methylation of a Glutamic Acid Decarboxylase 1 Promoter in Rat Hippocampus

“…One approach is that of examining maternal care in the rat, notably variations in pup licking/grooming (LG) (Liu et al, 1997;Francis et al, 1999;Weaver et al, 2004a,b). The adult offspring of mothers that naturally showing low levels of pup LG (i.e., low-LG mothers) show enhanced stress reactivity (Liu et al, 1997;Caldji et al, 1998;Francis et al, 1999;Weaver et al, 2004b;Toki et al, 2007), including increased dopamine stress responses in the medial prefrontal cortex (PFC) (Zhang et al, 2005). These animals also exhibit impaired sensorimotor gating as measured by prepulse inhibition (PPI) (Zhang et al, 2005).…”