Stress-induced changes in corticosteroid receptor expression in primate hippocampus and prefrontal cortex

Patel, Paresh D.; Katz, Maor; Karssen, Adriaan M.; Lyons, David M.

doi:10.1016/j.psyneuen.2007.12.003

Cited by 92 publications

(81 citation statements)

References 53 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…GQ845040). Riboprobe synthesis and in situ hybridization histochemistry were carried out as previously described (52). Hybridized tissue sections were dehydrated, air-dried, and exposed to Biomax MR film for 3 d with [ 14 C]-radiolabeled standards to assure that specific hybridization signal did not exceed the linear range of the film.…”

Section: Methodsmentioning

confidence: 99%

Stress coping stimulates hippocampal neurogenesis in adult monkeys

Lyons¹,

Buckmaster

Lee³

et al. 2010

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

Self Cite

View full text Add to dashboard Cite

Coping with intermittent social stress is an essential aspect of living in complex social environments. Coping tends to counteract the deleterious effects of stress and is thought to induce neuroadaptations in corticolimbic brain systems. Here we test this hypothesis in adult squirrel monkey males exposed to intermittent social separations and new pair formations. These manipulations simulate conditions that typically occur in male social associations because of competition for limited access to residency in mixed-sex groups. As evidence of coping, we previously confirmed that cortisol levels initially increase and then are restored to prestress levels within several days of each separation and new pair formation. Follow-up studies with exogenous cortisol further established that feedback regulation of the hypothalamic-pituitary-adrenal axis is not impaired. Now we report that exposure to intermittent social separations and new pair formations increased hippocampal neurogenesis in squirrel monkey males. Hippocampal neurogenesis in rodents contributes to spatial learning performance, and in monkeys we found that spatial learning was enhanced in conditions that increased hippocampal neurogenesis. Corresponding changes were discerned in the expression of genes involved in survival and integration of adult-born granule cells into hippocampal neural circuits. These findings support recent indications that stress coping stimulates hippocampal neurogenesis in adult rodents. Psychotherapies designed to promote stress coping potentially have similar effects in humans with major depression.gene expression | learning | neuroplasticity | resilience | hippocampus A lthough stress generally inhibits proliferation of new cells (1, 2) and thereby decreases neurogenesis in the hippocampus (3-5), recent studies of rodents suggest that coping with mild intermittent stress increases adult neurogenesis in the hippocampal dentate gyrus (6). Psychotherapies designed to promote coping in humans with depressive disorders may potentially have similar effects (7,8), but the neurogenic potential of stress coping has not been examined in human or nonhuman primates. Studies of primates are important for understanding neurogenesis in adult brain systems with established neural circuits and life spans that differ significantly from rodents (9).For most adult human and nonhuman primates, coping with stressful psychosocial demands spontaneously occurs in the absence of therapeutic interventions or guidance (10, 11). Male squirrel monkeys, for example, travel alone, in pairs, or in all-male groups that undergo stressful changes in membership. Changing male social associations occur in free ranging naturalistic conditions because of competition for limited access to residency in mixed-sex groups (12, 13). As evidence of coping, we and other investigators determined that plasma levels of cortisol initially increase and then are restored to prestress levels during intermittent social separations and new pair formations (14-16). Follow-up studies wit...

show abstract

Section: Methodsmentioning

confidence: 99%

Stress coping stimulates hippocampal neurogenesis in adult monkeys

Lyons¹,

Buckmaster

Lee³

et al. 2010

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

Self Cite

View full text Add to dashboard Cite

show abstract

“…Highest expression of MR was found in the limbic structures, notably, the hippocampus of rats, mice, hamsters, birds and primates that was previously found to retain 3 H-corticosterone (Rhees et al 1972, Gerlach et al 1976, Sutanto & de Kloet 1987, Patel et al 2008. The naming of the receptor was ambivalent though as the soluble brain MR did bind aldosterone as well as the naturally occurring glucocorticoids and even progesterone, hence, its promiscuous nature (Funder 2016).…”

Section: Post-cloning Periodmentioning

confidence: 99%

30 YEARS OF THE MINERALOCORTICOID RECEPTOR: The brain mineralocorticoid receptor: a saga in three episodes

Joëls

Kloet

2017

Journal of Endocrinology

119

109

View full text Add to dashboard Cite

In 1968, Bruce McEwen discovered that 3 H-corticosterone administered to adrenalectomised rats is retained in neurons of hippocampus rather than those of hypothalamus. This discovery signalled the expansion of endocrinology into the science of higher brain regions. With this in mind, our contribution highlights the saga of the brain mineralocorticoid receptor (MR) in three episodes. First, the precloning era dominated by the conundrum of two types of corticosterone-binding receptors in the brain, which led to the identification of the high-affinity corticosterone receptor as the 'promiscuous' MR cloned in 1987 by Jeff Arriza and Ron Evans in addition to the classical glucocorticoid receptor (GR). Then, the post-cloning period aimed to disentangle the function of the brain MR from that of the closely related GR on different levels of biological complexity. Finally, the synthesis section that highlights the two faces of brain MR: Salt and Stress. 'Salt' refers to the regulation of salt appetite, and reciprocal arousal, motivation and reward, by a network of aldosterone-selective MR-expressing neurons projecting from nucleus tractus solitarii (NTS) and circumventricular organs. 'Stress' is about the limbic-forebrain nuclear and membrane MRs, which act as a switch in the selection of the best response to cope with a stressor. For this purpose, activation of the limbic MR promotes selective attention, memory retrieval and the appraisal process, while driving emotional expressions of fear and aggression. Subsequently, rising glucocorticoid concentrations activate GRs in limbic-forebrain circuitry underlying executive functions and memory storage, which contribute in balance with MR-mediated actions to homeostasis, excitability and behavioural adaptation.

show abstract

“…Seminal studies (Schulkin et al , 1994; McEwen & Sapolsky, 1995; Popoli et al , 2011) support this notion by documenting that corticosteroids released from the adrenals do not only produce feedback inhibition of hypothalamic and pituitary hormone secretion (Akana et al , 1992) but directly regulate limbic and reward circuits (Sapolsky, 2003) to gate coping and flexibility (e.g., “flight or fight” behaviors; Eriksen et al , 1999; McEwen et al , 2012), motivation (McEwen, 2005), memory (Roozendaal et al , 2009), and fear extinction (Korte, 2001; McEwen, 2005). The prefrontal cortex (PFC) has emerged as a central site to orchestrate coordinated responses to acute stress (McEwen, 2007) with glucocorticoid and mineralocorticoid receptors modulating its ability to integrate upstream emotional, sensory, cognitive, and spatial inputs (Patel et al , 2008; Gadek‐Michalska et al , 2013; Caudal et al , 2014). …”

Section: Introductionmentioning

confidence: 99%

Hypothalamic CNTF volume transmission shapes cortical noradrenergic excitability upon acute stress

et al. 2018

View full text Add to dashboard Cite

Stress‐induced cortical alertness is maintained by a heightened excitability of noradrenergic neurons innervating, notably, the prefrontal cortex. However, neither the signaling axis linking hypothalamic activation to delayed and lasting noradrenergic excitability nor the molecular cascade gating noradrenaline synthesis is defined. Here, we show that hypothalamic corticotropin‐releasing hormone‐releasing neurons innervate ependymal cells of the 3rd ventricle to induce ciliary neurotrophic factor (CNTF) release for transport through the brain's aqueductal system. CNTF binding to its cognate receptors on norepinephrinergic neurons in the locus coeruleus then initiates sequential phosphorylation of extracellular signal‐regulated kinase 1 and tyrosine hydroxylase with the Ca2+‐sensor secretagogin ensuring activity dependence in both rodent and human brains. Both CNTF and secretagogin ablation occlude stress‐induced cortical norepinephrine synthesis, ensuing neuronal excitation and behavioral stereotypes. Cumulatively, we identify a multimodal pathway that is rate‐limited by CNTF volume transmission and poised to directly convert hypothalamic activation into long‐lasting cortical excitability following acute stress.

show abstract

Stress-induced changes in corticosteroid receptor expression in primate hippocampus and prefrontal cortex

Cited by 92 publications

References 53 publications

Stress coping stimulates hippocampal neurogenesis in adult monkeys

Stress coping stimulates hippocampal neurogenesis in adult monkeys

30 YEARS OF THE MINERALOCORTICOID RECEPTOR: The brain mineralocorticoid receptor: a saga in three episodes

Hypothalamic CNTF volume transmission shapes cortical noradrenergic excitability upon acute stress

Contact Info

Product

Resources

About