Progeny of mothers drinking corticosterone during lactation has lower stress-induced corticosterone secretion and better cognitive performance

Catalani, A.; Marinelli, Michela; Scaccianoce, Sergio; Nicolai, Raffaella; Muscolo, Luisa A.A.; Porcu, Alessandra; Korányi, L.; Piazza, Pier Vincenzo; Angelucci, L.

doi:10.1016/0006-8993(93)90079-3

Cited by 126 publications

(100 citation statements)

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“…Handling involves separating the pups from the mother for 10 min per day for the first 2 weeks of neonatal life, and the licking of the pup by the mother appears to be an important determinant of the postnatal handling effect (74). At the same time, increasing corticosterone levels in the mother's milk mimic some of the effects of neonatal handling (21), and thyroid hormone elevations have been suggested as a possible mediator of the neonatal handling effect, particularly regarding the elevated expression of glucocorticoid receptors in the hippocampus (97).…”

Section: The Problems and Opportunities Of Studying Individual Differmentioning

confidence: 99%

Section: The Problems and Opportunities Of Studying Individual Differmentioning

confidence: 99%

“…Rats with increased HPA reactivity show early decline of cognitive functions associated with the hippocampus (28) as well as increased propensity to self-administer drugs such as amphetamine and cocaine (30,113). In contrast, rats with a lower HPA reactivity as a result of neonatal handling have a slower rate of cognitive aging and a reduced loss of hippocampal function (21,98).Is there a human counterpart to the story of individual differences in rat HPA activity and hippocampal aging? We simply cannot say at this moment, but individual differences in human brain aging that are correlated with cortisol levels have been recognized in otherwise healthy individuals that are followed over a number of years (78,79,131).…”

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Stress and the Aging Hippocampus

McEwen

1999

Frontiers in Neuroendocrinology

208

101

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The ''glucocorticoid cascade hypothesis'' of hippocampal aging has stimulated a great deal of research into the neuroendocrine aspects of aging and the role of glucocorticoids, in particular. Besides strengthening the methods for investigating the aging brain, this research has revealed that the interactions between glucocorticoids and hippocampal neurons are far more complicated than originally envisioned and involve the participation of neurotransmitter systems, particularly the excitatory amino acids, as well as calcium ions and neurotrophins. New information has provided insights into the role of early experience in determining individual differences in brain and body aging by setting the reactivity of the hypothalamopituitary-adrenal axis and the autonomic nervous system. As a result of this research and advances in neuroscience and the study of aging, we now have a far more sophisticated view of the interactions among genes, early development, and environmental influences, as well as a greater appreciation of events at the cellular and molecular levels which protect neurons, and a greater appreciation of pathways of neuronal damage and destruction. While documenting the ultimate vulnerability of the brain to stressful challenges and to the aging process, the net result of this research has highlighted the resilience of the brain and offered new hope for treatment strategies for promoting the health of the aging brain. KEY WORDS: stress; hippocampal aging; glucocorticoid cascade hypothesis. 1999 Academic Press INTRODUCTIONThe hippocampus is a particularly vulnerable and sensitive region of the brain that is also very important for declarative and spatial learning and memory (36). Hippocampal neurons are vulnerable to seizures, strokes, and head trauma, as well as responding to stressful experiences (27,92,130). At the same time they show remarkable plasticity, involving long-term synaptic potentiation and depression, dendritic remodeling, synaptic turnover, and neurogenesis in the case of the dentate gyrus (Fig 1) (17,27,92).The work of aus der Muhlen and Ockenfels (3) first drew attention to potentially toxic actions of adrenal steroids. The reported darkly stained neurons in the hippocampus of guinea pigs exposed to high levels of glucocorticoids, an observation that has been confirmed and extended to repeated stress in subsequent studies (41,100), although there are still some doubts as to whether ''dark neurons'' may be artifacts of tissue trauma (18). In 1968, we discovered receptors for adrenal steroids in hippocampus (95), and it is now known that two types of adrenal steroid receptors exist in the hippocampus and other brain regions and mediate a variety of adrenal steroid effects on excitability, neurochemistry, and structure (27). Landfield (68) and then Sapolsky (127,128) provided evidence for a role of adrenal steroids in neuronal aging in the hippocampus, leading to the formulation of the ''glucocorticoid cascade hypothesis '' (130). This hypothesis states that glucocorticoids participate in a ...

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Section: The Problems and Opportunities Of Studying Individual Differmentioning

confidence: 99%

Section: The Problems and Opportunities Of Studying Individual Differmentioning

confidence: 99%

mentioning

confidence: 99%

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Stress and the Aging Hippocampus

McEwen

1999

Frontiers in Neuroendocrinology

208

101

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“…The development of spatial memory function is closely linked to the development of the hypothalamic-pituitary-adrenal (HPA) axis (Meaney et al, 1988;Catalani et al, 1993Catalani et al, , 2000. The hippocampus, a key brain structure underlying spatial learning (Morris et al, 1982;Sutherland et al, 1982), is both a major target of the stress hormone corticosterone (CORT), an end product of the HPA axis, and one of the major driving forces that provide input to the HPA axis (McEwen and Sapolsky, 1995;de Kloet et al, 1998).…”

Section: Introductionmentioning

confidence: 99%

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

Tang

Reeb‐Sutherland²,

Yang³

et al. 2011

J. Neurosci.

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Development of spatial memory in the rat is influenced by both maternal and nonmaternal aspects of the postnatal environment. Yet it remains poorly understood how these two aspects of the postnatal environment interact to program offspring cognitive development. By considering the joint influence of neonatal environmental novelty and maternal self-stress regulation on the development of spatial memory function in Long-Evans hooded rats, we show a persistent neonatal novelty-induced enhancement in spatial reference and working memory functions among the same individual offspring from juvenility to adulthood and a contrasting transient maternal modulatory influence on this novelty-related enhancement present during only juvenility. Specifically, at and only at juvenility, for mothers with good self-stress regulation as indexed by a low circulating basal corticosterone level, offspring showed a novelty-induced enhancement in spatial memory function, whereas for mothers with poor self-stress regulation, indexed by a high basal corticosterone level, offspring showed little enhancement or even small impairments. These findings indicate that maternal and nonmaternal postnatal environments exert separate but interacting influences on offspring cognitive development and support a maternal modulation model of cognitive development that considers maternal self-stress regulation as an important factor among the multitude of maternal influences.

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“…In rodents, offspring have been shown to be responsive to several factors that interact to affect the development of the postnatal brain. [32,34] and mice [33]. Interestingly, while low doses of neonatal corticosterone result in individual with an advantageous phenotype, high doses seem to lead to negative outcomes.…”

Section: Multiple Factors Interact To Mediate Environmental Effects Omentioning

confidence: 99%

Rodent models of early environment effects on offspring development and susceptibility to neurological diseases in adulthood

Coutellier

2012

Translational Neuroscience

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Rodent Models of eaRly envIRonMent effects on offspRIng developMent and susceptIbIlIty to neuRologIcal dIseases In adulthood abstractEvents early in life can program brain for a pattern of neuroendocrine and behavioral responses in later life. This mechanism is named "developmental phenotypic plasticity". Experimental evidences from rodents show that early experiences influence long-term development of behavioral, neuroendocrine and cognitive functions. While some neonatal conditions lead to positive outcomes, offspring might also display neurological dysfunctions in adulthood in case of adverse conditions during the early development. Different factors have been suggested to mediate the effects of neonatal conditions on offspring development but their exact contribution as well as their interaction still needs to be clarified. Studies based on rodents have been developed to model the longterm effects of early environmental conditions on the developing brain. These studies highlight importance of maternal behavior in mediating the effects of early environmental conditions on the offspring. However, other studies suggest that aside from the level of maternal care, other factors (gender, neonatal glucocorticoid levels) contribute to the adjustment of offspring phenotype to early environmental cues. Altogether, rodentsbased evidence suggests that developmental plasticity is a very complex phenomenon mediated by multiple factors that interact one to each other. Ultimately, the goal is to understand how early life events can lead to advantageous phenotype in adult life, or, on the contrary, can predispose individuals to psychopathologies such as depression or anxiety.

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Progeny of mothers drinking corticosterone during lactation has lower stress-induced corticosterone secretion and better cognitive performance

Cited by 126 publications

References 35 publications

Stress and the Aging Hippocampus

Stress and the Aging Hippocampus

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

Rodent models of early environment effects on offspring development and susceptibility to neurological diseases in adulthood

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