Neuroplasticity of the Hypothalamic–Pituitary–Adrenal Axis Early in Life Requires Recurrent Recruitment of Stress-Regulating Brain Regions

Fenoglio, Kristina A.; Chen, Yuncai; Baram, Tallie Z.

doi:10.1523/jneurosci.4080-05.2006

Cited by 110 publications

(166 citation statements)

References 75 publications

(71 reference statements)

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“…Indeed, a general divergence of pCREB and Fos expression in response to sensory stimulation ('experience') in the immature rodent has recently been described. 82 At both ages, blocking CRH receptors within the hippocampus, and without interference with systemic glucocorticoid release, abrogated the ability of the 'psychological' stress to activate hippocampal neurons. This, supported by the fact that many of the activated neurons in the hippocampal formation expressed the CRF 1 receptor, points to a substantial role of CRH receptor activation in the transduction of stress signals within the hippocampus.…”

Section: Discussionmentioning

confidence: 99%

Cellular and molecular mechanisms of hippocampal activation by acute stress are age-dependent

et al. 2006

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The effects of stress, including their putative contribution to pathological psychiatric conditions, are crucially governed by the age at which the stress takes place. However, the cellular and molecular foundations for the impact of stress on neuronal function, and their change with age, are unknown. For example, it is not known whether 'psychological' stress signals are perceived by similar neuronal populations at different ages, and whether they activate similar or age-specific signaling pathways that might then mediate the spectrum of stress-evoked neuronal changes. We employed restraint and restraint/noise stress to address these issues in juvenile (postnatal day 18, [P18]) and adult rats, and used phosphorylation of the transcription factor CREB (pCREB) and induction of c-fos as markers of hippocampal neuronal responses. Stress-activated neuronal populations were identified both anatomically and biochemically, and selective blockers of the stress-activated hippocampal peptide, corticotropin-releasing hormone (CRH) were used to probe the role of this molecule in stressinduced hippocampal cell activation. Stress evoked strikingly different neuronal response patterns in immature vs adult hippocampus. Expression of pCREB appeared within minutes in hippocampal CA3 pyramidal cells of P18 rats, followed by delayed induction of Fos protein in the same cell population. In contrast, basal pCREB levels were high in adult hippocampus and were not altered at 10-120 min by stress. Whereas Fos induction was elicited by stress in the adult, it was essentially confined to area CA1, with little induction in CA3. At both age groups, central pretreatment with either a nonselective blocker of CRH receptors or the CRF 1 -selective antagonist, NBI 30775, abolished stress-evoked neuronal activation. In conclusion, hippocampal neuronal responses to psychological stress are generally more rapid and robust in juvenile rats, compared to fully mature adults, and at both ages, CRH plays a key role in this process. Enhanced hippocampal response to stress during development, and particularly the activation of the transcription factor CREB, may contribute to the enduring effects of stress during this period on hippocampal function.

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Section: Discussionmentioning

confidence: 99%

Cellular and molecular mechanisms of hippocampal activation by acute stress are age-dependent

et al. 2006

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“…Maternal separation during postnatal life in mice or rats for instance, can increase stress reactivity, induce behavioural despair and alter cognitive functions in some models 1,7,8,[33][34][35][36] but can have opposite effects in other models 37,38 . Although paradoxical at first sight, these findings indicate that the impact of early stress can vary, probably due to differences in experimental paradigms or in the sensitivity of the models.…”

Section: Discussionmentioning

confidence: 99%

Early life stress in fathers improves behavioural flexibility in their offspring

et al. 2014

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Traumatic experiences in childhood can alter behavioural responses and increase the risk for psychopathologies across life, not only in the exposed individuals but also in their progeny. In some conditions, such experiences can however be beneficial and facilitate the appraisal of adverse environments later in life. Here we expose newborn mice to unpredictable maternal separation combined with unpredictable maternal stress (MSUS) for 2 weeks and assess the impact on behaviour in the offspring when adult. We show that MSUS in male mice favours goal-directed behaviours and behavioural flexibility in the adult offspring. This effect is accompanied by epigenetic changes involving histone post-translational modifications at the mineralocorticoid receptor (MR) gene and decreased MR expression in the hippocampus. Mimicking these changes pharmacologically in vivo reproduces the behavioural phenotype. These findings highlight the beneficial impact that early adverse experiences can have in adulthood, and the implication of epigenetic modes of gene regulation.

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“…For example, Avishai-Eliner and collaborators have shown that the permanent down-regulation of hypothalamic CRH-mRNA levels observed in rats handled daily from postnatal days 3 to 14 was evident by postnatal day 9 and was sustained through postnatal days 23 and 45, i.e., beyond puberty (Avishai-Eliner et al, 2001;Fenoglio et al, 2006). These animals exhibit a behavioral profile of decreased anxiety and HPA responses in adulthood.…”

Section: Discussionmentioning

confidence: 99%

Brain corticotropin-releasing hormone (CRH) circuits in the developing rat: Effect of maternal deprivation

et al. 2006

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Early in life, there is a delicate and critical balance aimed to maintain low hormone responses derived from the stress responsive hypothalamic-pituitary-adrenal axis (HPA). However, in the infant rat hypothalamic corticotrophin-releasing hormone (CRH) stress responses to environmental events are clearly seen even though other elements of the HPA axis may have limited responses. In view of the role of CRH in mediating behavior associated with stress and anxiety, we considered the ontogeny and the effects of prolonged maternal deprivation (DEP) in brain areas that express CRH-related molecules outside the hypothalamus. We hypothesized that DEP would alter the ontogeny of CRH, CRH binding protein and CRH receptor 1 in prefrontal cortex, amygdala, septum and hippocampus, areas that are part of the CRH extra hypothalamic system, and that a differential modulation would be observed in response to restraint. We compared non-deprived animals to animals subjected to 24 h of DEP at 6, 12 and 18 days of life. We found (1) developmental patterns, which were idiosyncratic to the anatomical area examined, and (2) a temporal response of mRNA levels which was also site specific. The genomic changes are not always related to maternal deprivation status, in fact DEP enhanced, suppressed or had no consequence on the underlying ontogenic progression and restraint response of these CRH-related molecules. We conclude that the extra hypothalamic CRH system is a dynamic system responding to developmental and environmental demands challenging the basic assumption of stress hypo responsiveness in the infant rat. This modulation may have important repercussions on morphological organization and events leading to neuroprotection.

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Neuroplasticity of the Hypothalamic–Pituitary–Adrenal Axis Early in Life Requires Recurrent Recruitment of Stress-Regulating Brain Regions

Cited by 110 publications

References 75 publications

Cellular and molecular mechanisms of hippocampal activation by acute stress are age-dependent

Cellular and molecular mechanisms of hippocampal activation by acute stress are age-dependent

Early life stress in fathers improves behavioural flexibility in their offspring

Brain corticotropin-releasing hormone (CRH) circuits in the developing rat: Effect of maternal deprivation

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