Neonatal Novelty-Induced Persistent Enhancement in Offspring Spatial Memory and the Modulatory Role of Maternal Self-Stress Regulation

Tang, Akaysha C.; Reeb‐Sutherland, Bethany C.; Yang, Zhen; Romeo, Russell D.; McEwen, Bruce S.

doi:10.1523/jneurosci.6808-10.2011

Cited by 22 publications

(16 citation statements)

References 44 publications

(73 reference statements)

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“…Instead, it is the case that mothers with good selfstress regulation will enable the pups to respond positively to novelty exposure. This sensitivity of the novelty exposure effect to the context of maternal self-stress regulation supports an important notion that the mother can function as both a binary "switch," setting the direction of the novelty exposure influence on her offspring (14), and a "dial" to set continuous and finer control of the magnitude of this novelty effect (17,18).…”

Section: Resultssupporting

confidence: 63%

“…Recently, we reported for the same group of rats that neonatal novelty exposure and maternal self-stress regulation also similarly interact to influence offspring cognitive development (17). Therefore, we speculated that the early growth measure may be associated with early cognitive development.…”

Section: Resultsmentioning

confidence: 90%

“…More recently, the maternal modulation hypothesis has been tested for long-range and continuous (as opposed binary) modulation across the offspring's life span. Family-to-family variations in both maternal-care reliability and maternal selfstress regulation have been shown to account for variations in the effects of neonatal novelty exposure on adult offspring behavior and HPA function (15-18), pointing out an obvious (when thinking human development) (19), yet easily missed possibility (when thinking animal models), that the maternal context itself is multidimensional, including not only her care-giving behaviors (15, 16) but also the mother's self-stress regulation (17,18).This notion of multiple maternal influences beyond maternalcare quantity is compatible with a large body of rodent literature. First, differences in offspring's HPA and behavioral functions can be created by prenatal (20) and postnatal (6, 7) manipulation of the mother's stress-response system, including directly adding corticosterone (CORT) to her drinking water (6) and injection of CORT into key brain structures (14).…”

mentioning

confidence: 99%

mentioning

confidence: 99%

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Maternal modulation of novelty effects on physical development

Tang

Yang²,

Reeb‐Sutherland³

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

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Familiarity to the mother and the novelty afforded by the postnatal environment are two contrasting sources of neonatal influence. One hypothesis regarding their relationship is the maternal modulation hypothesis, which predicts that the same neonatal stimulation may have different effects depending on the maternal context. Here we tested this hypothesis using physical development, indexed by body weight, as an endpoint and found that, among offspring of mothers with a high initial swim-stress-induced corticosterone (CORT) response, neonatal novelty exposure induced an enhancement in early growth, and among offspring with mothers of a low initial CORT response, the same neonatal stimulation induced an impairment. At an older age, a novelty-induced increase in body weight was also found among offspring of mothers with high postnatal care reliability and a novelty-induced reduction found among offspring of mothers with low care reliability. These results support a maternal modulation of early stimulation effects on physical development and demonstrate that the maternal influence originates from multiple instead of any singular sources. These results (i) significantly extend the findings of maternal modulation from the domain of cognitive development to the domain of physical development; (ii) offer a unifying explanation for a previously inconsistent literature regarding early stimulation effects on body weight; and (iii) highlight the notion that the early experience effect involves no causal primacy but higher order interactions among the initial triggering events and subsequent events involving a multitude of maternal and nonmaternal influences.maternal stress | maternal care | maternal mediation | developmental plasticity | growth enhancement I t seems self-evident that, for a developing infant, both the maternal and nonmaternal environment affects his or her development. Over the past century, ample evidence from both human and animal early-experience studies has confirmed this intuition (1-3). What remains challenging is how these two environmental sources interact to jointly influence offspring development (4-7). Emerging from the rodent developmental literature are two alternative views regarding the relation between maternal and nonmaternal influences. The "maternal mediation view" assumes that nonmaternal environment exerts its effect indirectly through its effect on the mother, who in turn affects the offspring (e.g., see refs. 8 and 9). When taken to the extreme, this view would directly contradict the stress-activation hypothesis (10, 11), which states that the nonmaternal environment has a direct effect on the offspring by activating some aspects of the offspring's hypothalamic-pituitary-adrenal (HPA) function. In contrast, the "maternal modulation view" incorporates the stressactivation hypothesis and assumes that the nonmaternal environment first activates aspects of the HPA axis, and the mother then modulates this effect (12). According to the latter view, the individual mother sets distinct conte...

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Section: Resultssupporting

confidence: 63%

Section: Resultsmentioning

confidence: 90%

mentioning

confidence: 99%

mentioning

confidence: 99%

See 2 more Smart Citations

Maternal modulation of novelty effects on physical development

Tang

Yang²,

Reeb‐Sutherland³

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

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“…An exception to the classical ERs is the GPER1 (111,208), which associates with PSD-95 in the dendritic spine and appears to couple estrogen action to membrane progestin receptors, 5HT 1A receptors, and corticotrophin releasing hormone (CRH1) receptors (35). Finally, it should be noted that rapid, nongenomic actions are recognized along with classical cell nuclear actions for all classes of steroid hormones: progestins (142,230), androgens (209), glucocorticoids (210,211), mineralocorticoids (98), and vitamin D (86).…”

Section: A Rapid Nongenomic Actions Of Estrogens and Other Steroid Hmentioning

confidence: 99%

Estrogen Effects on Cognitive and Synaptic Health Over the Lifecourse

Hara

Waters

McEwen

et al. 2015

Physiological Reviews

334

249

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Estrogen facilitates higher cognitive functions by exerting effects on brain regions such as the prefrontal cortex and hippocampus. Estrogen induces spinogenesis and synaptogenesis in these two brain regions and also initiates a complex set of signal transduction pathways via estrogen receptors (ERs). Along with the classical genomic effects mediated by activation of ER α and ER β, there are membrane-bound ER α, ER β, and G protein-coupled estrogen receptor 1 (GPER1) that can mediate rapid nongenomic effects. All key ERs present throughout the body are also present in synapses of the hippocampus and prefrontal cortex. This review summarizes estrogen actions in the brain from the standpoint of their effects on synapse structure and function, noting also the synergistic role of progesterone. We first begin with a review of ER subtypes in the brain and how their abundance and distributions are altered with aging and estrogen loss (e.g., ovariectomy or menopause) in the rodent, monkey, and human brain. As there is much evidence that estrogen loss induced by menopause can exacerbate the effects of aging on cognitive functions, we then review the clinical trials of hormone replacement therapies and their effectiveness on cognitive symptoms experienced by women. Finally, we summarize studies carried out in nonhuman primate models of age- and menopause-related cognitive decline that are highly relevant for developing effective interventions for menopausal women. Together, we highlight a new understanding of how estrogen affects higher cognitive functions and synaptic health that go well beyond its effects on reproduction.

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Adaptive Regulations in Developing Rodents Following Neonatal Challenges

Coutellier

2012

Adaptive and Maladaptive Aspects of Developmental Stress

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Neonatal Novelty-Induced Persistent Enhancement in Offspring Spatial Memory and the Modulatory Role of Maternal Self-Stress Regulation

Cited by 22 publications

References 44 publications

Maternal modulation of novelty effects on physical development

Maternal modulation of novelty effects on physical development

Estrogen Effects on Cognitive and Synaptic Health Over the Lifecourse

Adaptive Regulations in Developing Rodents Following Neonatal Challenges

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