Role of adrenal steroid mineralocorticoid and glucocorticoid receptors in long-term potentiation in the CA1 field of hippocampal slices

Pavlides, Constantine; Ogawa, Sonoko; Kimura, Akihisa; McEwen, Bruce S.

doi:10.1016/s0006-8993(96)00776-7

Cited by 217 publications

(115 citation statements)

References 36 publications

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“…Sidak post hoc comparison revealed that compared with VEH conditions, the percentage increase in fEPSP after tetanic stimulation was reduced in slices from high LG offspring pretreated with high CORT ( p Ͻ 0.01). This is in agreement with previous studies using a similar dose of CORT using rats with unknown history of maternal care (Diamond et al, 1992;Pavlides et al, 1996;Wiegert et al, 2005;Joels and Krugers, 2007) (Fig. 5A).…”

Section: Corticosterone Modulation Of Ltp Is Altered By History Of Masupporting

confidence: 93%

“…CORT exerts its action via binding to MR and/or GR, which are both abundantly expressed in CA1 pyramidal neurons (de Kloet et al, 1998). Although GR activation mediates the inhibitory effects of high CORT on LTP, conditions of predominant MR activation (resting state) are associated with efficient induction of LTP (Diamond et al, 1992;Pavlides et al, 1996;Joels and Krugers, 2007). Differences in MR and GR protein levels between low and high LG offspring may thus affect LTP, both under resting and stresslike conditions.…”

Section: Corticosteroid Receptor Protein Levels Are Altered By Maternmentioning

confidence: 99%

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

Champagne¹,

Bagot²,

Hasselt³

et al. 2008

Journal of Neuroscience

594

478

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Maternal licking and grooming (LG) in infancy influences stress responsiveness and cognitive performance in the offspring. We examined the effects of variation in the frequency of pup LG on morphological, electrophysiological, and behavioral aspects of hippocampal synaptic plasticity under basal and stress-like conditions. We found shorter dendritic branch length and lower spine density in CA1 cells from the adult offspring of low compared with high LG offspring. We also observed dramatic effects on long-term potentiation (LTP) depending on corticosterone treatment. Low LG offspring, in contrast to those of high LG mothers, displayed significantly impaired LTP under basal conditions but surprisingly a significantly enhanced LTP in response to high corticosterone in vitro. This enhanced plasticity under conditions that mimic those of a stressful event was apparent in vivo. Adult low LG offspring displayed enhanced memory relative to high LG offspring when tested in a hippocampal-dependent, contextual fear-conditioning paradigm. Hippocampal levels of glucocorticoid and mineralocorticoid receptors were reduced in low compared with high LG offspring. Such effects, as well as the differences in dendritic morphology, likely contribute to LTP differences under resting conditions, as well as to the maternal effects on synaptic plasticity and behavior in response to elevated corticosterone levels. These results suggest that maternal effects may modulate optimal cognitive functioning in environments varying in demand in later life, with offspring of high and low LG mothers showing enhanced learning under contexts of low and high stress, respectively.

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Section: Corticosterone Modulation Of Ltp Is Altered By History Of Masupporting

confidence: 93%

Section: Corticosteroid Receptor Protein Levels Are Altered By Maternmentioning

confidence: 99%

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

Champagne¹,

Bagot²,

Hasselt³

et al. 2008

Journal of Neuroscience

594

478

View full text Add to dashboard Cite

show abstract

“…Therefore, possible involvement of effects on peripheral receptors cannot be ruled out. However, to the extent that similar findings were obtained in the in vitro preparations in which the blockers were obtained directly in the hippocampus (Pavlides et al, 1996), it is likely that the effects observed in the current study result from direct blockade of hippocampal MRs or GRs.…”

Section: Discussionsupporting

confidence: 78%

“…In contrast, elevated levels of corticosteroid hormones (presumably occupying both GRs and MRs) or exposure to stress have been reported to impair LTP and to facilitate long-term depression (LTD) in the hippocampus (Diamond et al, 1992;Pavlides et al, 1995Pavlides et al, , 1996Pavlides and McEwen, 1999;Alfarez et al, 2002;Krugers et al, 2005). Little is known about the mechanism through which these stress-induced changes exert their effects, although NMDA receptors seem to be involved (Kim et al, 1996).…”

Section: Introductionmentioning

confidence: 99%

Contrasting Roles of Corticosteroid Receptors in Hippocampal Plasticity

Avital

Segal²,

Richter‐Levin³

2006

J. Neurosci.

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Elevated levels of corticosteroid hormones, presumably occupying both mineralocorticoid receptors (MRs) and glucocorticoid receptors (GRs), have been reported to impair synaptic plasticity in the hippocampus as well as the acquisition of hippocampus-dependent memories. In contrast, recent evidence suggests that activation of MRs enhance cognitive functions. To clarify the roles of different steroid receptors in hippocampal plasticity, young adult rats were injected with the GR antagonist RU38486 (mifepristone) or the MR antagonist Spironolactone before the exposure to an acute swim stress. Hippocampal responses to perforant path stimulation were then recorded in anesthetized rats. Stress combined with RU38486 produced a striking facilitation of LTP. Spironolactone enabled only short-term potentiation that reversed to long-term depression (LTD) in the stressed animals. Finally, the blockade of both MRs and GRs led to impairment of long-term potentiation. These findings indicate that MRs and GRs assume opposite roles in regulation of synaptic plasticity after acute exposure to stressors.

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“…Adrenal steroids, which have a bad reputation as concerns their role in exacerbating these forms of damage (126), are also involved in three types of adaptive plasticity in the hippocampal formation. First, they reversibly and biphasically modulate the excitability of hippocampal neurons and influence the magnitude of long-term potentiation, as well as producing long-term depression (27,63,(109)(110)(111)(112). These effects may be involved in biphasic effects of adrenal secretion on excitability and cognitive 53 STRESS AND THE AGING HIPPOCAMPUS function and memory during the diurnal rhythm and after stress (8,24,31,34).…”

Section: There Are Multiple Mechanisms Of Plasticitymentioning

confidence: 99%

Stress and the Aging Hippocampus

McEwen

1999

Frontiers in Neuroendocrinology

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205

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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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Role of adrenal steroid mineralocorticoid and glucocorticoid receptors in long-term potentiation in the CA1 field of hippocampal slices

Cited by 217 publications

References 36 publications

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

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

Contrasting Roles of Corticosteroid Receptors in Hippocampal Plasticity

Stress and the Aging Hippocampus

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