Opposing roles of type I and type II adrenal steroid receptors in hippocampal long-term potentiation

Studies were performed in vivo on the dentate gyrus to investigate the possible involvement of Type I and Type II adrenal steroid receptors in the mediation of reported adrenal steroid effects on long-term potentiation, through the use of specific Type I and Type II receptor agonists and antagonists. In adrenalectomized rats, administration of aldosterone, a specific Type I agonist, produced a marked enhancement in long-term potentiation, in comparison to either the adrenalectomized or sham adrenalectomized controls. Administration of RU 28318, a Type I antagonist, which by itself had minimal effects, blocked the aldosterone enhancement. In contrast, administration of the specific Type II agonist, RU 28362, produced a marked decrement in the induction of long-term potentiation. The RU 28362 effect was blocked by a prior injection of the Type II antagonist, RU 38486. Neither adrenalectomy nor administration of any of the steroid agonists or antagonists had noticeable effects on neuronal excitability (as determined by the field potentials), nor on post-tetanic potentiation. These findings are consistent with other studies that have shown a biphasic effect of increasing levels of corticosterone on long-term or prime burst potentiation. Taken together, these studies suggest that Type I receptors, with a high affinity for corticosterone, and Type II receptors, having a lower affinity for corticosterone, form a two-level recognition system to modulate induced synaptic plasticity in opposite directions in the dentate gyrus and possibly also in Ammon's horn.

[1]  M. Joëls,et al.  Mineralocorticoid receptor-mediated changes in membrane properties of rat CA1 pyramidal neurons in vitro. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[2]  T. Bliss,et al.  Long‐lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path , 1973, The Journal of physiology.

[3]  Richard F. Thompson,et al.  Inescapable versus escapable shock modulates long-term potentiation in the rat hippocampus. , 1989, Science.

[4]  B. McEwen,et al.  Adrenal steroid receptors and actions in the nervous system. , 1986, Physiological reviews.

[5]  E. R. Kloet,et al.  Two receptor systems for corticosterone in rat brain: microdistribution and differential occupation. , 1985, Endocrinology.

[6]  E. R. Kloet,et al.  Anatomical resolution of two types of corticosterone receptor sites in rat brain with in vitro autoradiography and computerized image analysis. , 1986, Journal of steroid biochemistry.

[7]  Y Watanabe,et al.  Effects of glucocorticoids on hippocampal long‐term potentiation , 1993, Hippocampus.

[8]  D. Diamond,et al.  Serum corticosterone level predicts the magnitude of hippocampal primed burst potentiation and depression in urethane-anesthetized rats , 1991, Psychobiology.

[9]  D. Diamond,et al.  Adrenalectomy reduces the threshold for hippocampal primed burst potentiation in the anesthetized rat , 1989, Brain Research.

[10]  M. Joëls,et al.  Effects of glucocorticoids and norepinephrine on the excitability in the hippocampus. , 1989, Science.

[11]  B. McEwen,et al.  Rat Brain Binds Adrenal Steroid Hormone: Radioautography of Hippocampus with Corticosterone , 1972, Science.

[12]  P. Landfield,et al.  Corticosteroid modulation of hippocampal potentials: increased effect with aging. , 1989, Science.

[13]  Richard F. Thompson,et al.  Acute stress impairs (or induces) synaptic long‐term potentiation (LTP) but does not affect paired‐pulse facilitation in the stratum radiatum of rat hippocampus , 1992, Synapse.

[14]  S Levine,et al.  Behavioral stress impairs long-term potentiation in rodent hippocampus. , 1987, Behavioral and neural biology.

[15]  B. McEwen,et al.  Corticosterone regulation of Type I and Type II adrenal steroid receptors in brain, pituitary, and immune tissue , 1991, Brain Research.

[16]  W. Zieglgänsberger,et al.  Corticosterone Reduces Synaptic Inhibition in Rat Hippocampal and Neocortical Neurons in vitro , 1992, Journal of neuroendocrinology.

[17]  B. Dubrovsky,et al.  Effects of 5α-dihydrocorticosterone on evoked responses and long-term potentiation , 1987, Brain Research Bulletin.

[18]  B. Dubrovsky,et al.  Effects of adrenal steroids and their reduced metabolites on hippocampal long-term potentiation , 1991, The Journal of Steroid Biochemistry and Molecular Biology.

[19]  John A. Zelano,et al.  On-line acquisition, analysis and presentation of neurophysiological data based on a personal microcomputer system , 1990, Journal of Neuroscience Methods.

[20]  M. Joëls,et al.  Effect of corticosteroid hormones on electrical activity in rat hippocampus , 1991, The Journal of Steroid Biochemistry and Molecular Biology.

[21]  L. Swanson,et al.  The neuronal mineralocorticoid receptor as a mediator of glucocorticoid response. , 1988, Neuron.

[22]  Richard F. Thompson,et al.  Unpredictable and uncontrollable stress impairs neuronal plasticity in the rat hippocampus , 1990, Brain Research Bulletin.

[23]  E. Carlier,et al.  Corticosterone effects on long-term potentiation in mouse hippocampal slices. , 1994, Neuroendocrinology.

[24]  K. Fuxe,et al.  Mapping of glucocorticoid receptor immunoreactive neurons in the rat tel- and diencephalon using a monoclonal antibody against rat liver glucocorticoid receptor. , 1985, Endocrinology.

[25]  D. Diamond,et al.  Inverted‐U relationship between the level of peripheral corticosterone and the magnitude of hippocampal primed burst potentiation , 1992, Hippocampus.

[26]  D. Diamond,et al.  Exposure to a novel environment interferes with the induction of hippocampal primed burst potentiation in the behaving rat , 1990, Psychobiology.

[27]  M. Joëls,et al.  Control of neuronal excitability by corticosteroid hormones , 1992, Trends in Neurosciences.

[28]  O. Thibault,et al.  Hippocampal glucocorticoid receptor activation enhances voltage-dependent Ca2+ conductances: relevance to brain aging. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[29]  M. Ferrini,et al.  Corticosteroid receptors and glucocorticoid content in microdissected brain regions: correlative aspects. , 1989, Neuroendocrinology.

[30]  M. M. Bradford A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. , 1976, Analytical biochemistry.