Stress and cognition: are corticosteroids good or bad guys?

Corticosteroid hormones secreted by the adrenal cortex protect the brain against adverse events and are essential for cognitive performance. However, in recent literature, the central action of corticosteroids has mostly been portrayed as damaging and disruptive to memory formation. We argue that this paradox can be explained by appreciating the specific role of both mineralocorticoid and glucocorticoid receptors in the various stages of information processing. In addition, the context in which corticosteroid-receptor activation takes place is crucial in determining steroid-mediated effects. These effects generally favour adaptive behaviour that is most relevant to the situation. Corticosteroid effects on cognition can, however, turn from adaptive into maladaptive, when actions via the two corticosteroid-receptor types are imbalanced for a prolonged period of time.

[1]  T. Bliss,et al.  A synaptic model of memory: long-term potentiation in the hippocampus , 1993, Nature.

[2]  Carmen Sandi,et al.  Experience‐dependent Facilitating Effect of Corticosterone on Spatial Memory Formation in the Water Maze , 1997, The European journal of neuroscience.

[3]  Michael J. Rowan,et al.  Behavioural stress facilitates the induction of long-term depression in the hippocampus , 1997, Nature.

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

[5]  B. McEwen,et al.  Chronic stress impairs rat spatial memory on the Y maze, and this effect is blocked by tianeptine pretreatment. , 1996, Behavioral neuroscience.

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

[7]  O. Meijer,et al.  Penetration of dexamethasone into brain glucocorticoid targets is enhanced in mdr1A P-glycoprotein knockout mice. , 1998, Endocrinology.

[8]  M. Joëls,et al.  Hippocampal Cell Responses in Mice with a Targeted Glucocorticoid Receptor Gene Disruption , 1996, The Journal of Neuroscience.

[9]  F. Holsboer,et al.  Antidepressants and hypothalamic-pituitary-adrenocortical regulation. , 1996, Endocrine reviews.

[10]  M. Bear,et al.  Synaptic plasticity: LTP and LTD , 1994, Current Opinion in Neurobiology.

[11]  C. Pavlides,et al.  Hippocampal homosynaptic long-term depression/depotentiation induced by adrenal steroids , 1995, Neuroscience.

[12]  J. Herman,et al.  Stress regulation of mineralocorticoid receptor heteronuclear RNA in rat hippocampus , 1995, Brain Research.

[13]  B. McEwen.  Stress and hippocampal plasticity. , 1999, Annual review of neuroscience.

[14]  R. Sapolsky,et al.  Stress, Glucocorticoids, and Damage to the Nervous System: The Current State of Confusion. , 1996, Stress.

[15]  J. W. Rudy,et al.  A selective role for corticosterone in contextual-fear conditioning. , 1997, Behavioral neuroscience.

[16]  N. McNaughton,et al.  Comparison between the behavioural effects of septal and hippocampal lesions: A review , 1983, Neuroscience & Biobehavioral Reviews.

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

[18]  J. D. McGaugh,et al.  Basolateral Amygdala Lesions Block the Memory‐enhancing Effect of Glucocorticoid Administration in the Dorsal Hippocampus of Rats , 1997, The European journal of neuroscience.

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

[20]  E. Fuchs,et al.  Memory performance in tree shrews: effects of stressful experiences , 1998, Neuroscience & Biobehavioral Reviews.

[21]  S. Beck,et al.  Long- and short-term administration of corticosterone alters CA1 hippocampal neuronal properties. , 1994, Neuroendocrinology.

[22]  H. Akil,et al.  α, β, and γ Mineralocorticoid Receptor Messenger Ribonucleic Acid Splice Variants: Differential Expression and Rapid Regulation in the Developing Hippocampus. , 1998, Endocrinology.

[23]  Y. Goda,et al.  Synaptic plasticity: The basis of particular types of learning , 1996, Current Biology.

[24]  Michael J. Rowan,et al.  Spatial exploration induces a persistent reversal of long-term potentiation in rat hippocampus , 1998, Nature.

[25]  E. D. Kloet,et al.  Brain corticosteroid receptor balance and homeostatic control , 1991 .

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

[27]  P. Stanton,et al.  LTD, LTP, and the sliding threshold for long‐term synaptic plasticity , 1996, Hippocampus.

[28]  Carmen Sandi,et al.  Corticosterone enhances long-term retention in one-day-old chicks trained in a weak passive avoidance learning paradigm , 1994, Brain Research.

[29]  M. Oitzl,et al.  Selective corticosteroid antagonists modulate specific aspects of spatial orientation learning. , 1992, Behavioral neuroscience.

[30]  D. Diamond,et al.  Psychological stress repeatedly blocks hippocampal primed burst potentiation in behaving rats , 1994, Behavioural Brain Research.

[31]  M. Joëls,et al.  Spatial Learning Deficits in Mice with a Targeted Glucocorticoid Receptor Gene Disruption , 1997, The European journal of neuroscience.

[32]  B. Bohus,et al.  Adrenal steroids and extinction behavior: antagonism by progesterone, deoxycorticosterone and dexamethasone of a specific effect of corticosterone. , 1981, Life sciences.

[33]  M. Joëls,et al.  Corticosteroid actions on amino acid-mediated transmission in rat CA1 hippocampal cells. , 1993 .

[34]  M. Meaney,et al.  Enduring effects of chronic corticosterone treatment on spatial learning, synaptic plasticity, and hippocampal neuropathology in young and mid-aged rats , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[35]  J. Herman,et al.  Regulation of Hippocampal Glucocorticoid Receptor Gene Transcription and Protein Expression In Vivo , 1998, The Journal of Neuroscience.

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

[37]  H T van der Voort,et al.  Partial colocalization of glucocorticoid and mineralocorticoid receptors in discrete compartments in nuclei of rat hippocampus neurons. , 1996, Journal of cell science.

[38]  S. Rose,et al.  Corticosteroid Receptor Antagonists are Amnestic for Passive Avoidance Learning in Day‐old Chicks , 1994, The European journal of neuroscience.

[39]  J. Herman,et al.  Neurocircuitry of stress: central control of the hypothalamo–pituitary–adrenocortical axis , 1997, Trends in Neurosciences.

[40]  W. Hesen,et al.  Mineralocorticoid hormones suppress serotonin-induced hyperpolarization of rat hippocampal CA1 neurons , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[41]  B. McEwen,et al.  Stress and cognitive function , 1995, Current Opinion in Neurobiology.

[42]  Melly S. Oitzl,et al.  An ACTH/MSH(4–9) analog counteracts the behavioral effects of a mineralocorticoid receptor antagonist , 1993, Pharmacology Biochemistry and Behavior.

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

[44]  T. Shors,et al.  Effects of stress and long-term potentiation (LTP) on subsequent LTP and the theta burst response in the dentate gyrus , 1994, Brain Research.

[45]  K. Kaestner,et al.  DNA Binding of the Glucocorticoid Receptor Is Not Essential for Survival , 1998, Cell.

[46]  Kenneth S. Yoon,et al.  Stress: metaplastic effects in the hippocampus , 1998, Trends in Neurosciences.

[47]  M. Joëls,et al.  Brain corticosteroid receptor balance in health and disease. , 1998, Endocrine reviews.

[48]  S. Ogawa,et al.  Role of adrenal steroid mineralocorticoid and glucocorticoid receptors in long-term potentiation in the CA1 field of hippocampal slices , 1996, Brain Research.

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

[50]  J. Newcomer,et al.  Glucocorticoid-induced impairment in declarative memory performance in adult humans , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[51]  M. Beato,et al.  Interaction of steroid hormone receptors with the transcription initiation complex. , 1996, Endocrine reviews.

[52]  H. Akil,et al.  Localization and regulation of glucocorticoid and mineralocorticoid receptor messenger RNAs in the hippocampal formation of the rat. , 1989, Molecular endocrinology.

[53]  G M Rose,et al.  Psychological stress impairs spatial working memory: relevance to electrophysiological studies of hippocampal function. , 1996, Behavioral neuroscience.

[54]  B. McEwen,et al.  Restraint stress reversibly enhances spatial memory performance , 1996, Physiology & Behavior.

[55]  Bruce S. McEwen,et al.  The acute effects of corticosteroids on cognition: integration of animal and human model studies , 1997, Brain Research Reviews.

[56]  James L. McGaugh,et al.  Stress and glucocorticoids impair retrieval of long-term spatial memory , 1998, Nature.

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

[58]  H. Eichenbaum,et al.  Two functional components of the hippocampal memory system , 1994, Behavioral and Brain Sciences.

[59]  W. Abraham,et al.  Glucocorticoid receptor activation lowers the threshold for NMDA-receptor-dependent homosynaptic long-term depression in the hippocampus through activation of voltage-dependent calcium channels. , 1997, Journal of neurophysiology.

[60]  R. Jaffard,et al.  Contextual conditioned fear blocks the induction but not the maintenance of lateral septal LTP in behaving mice. , 1997, Journal of neurophysiology.

[61]  J. D. McGaugh,et al.  Basolateral amygdala lesions block glucocorticoid-induced modulation of memory for spatial learning. , 1996, Behavioral neuroscience.

[62]  M. Joëls.  Steroid Hormones and Excitability in the Mammalian Brain , 1997, Frontiers in Neuroendocrinology.

[63]  W Wippich,et al.  Stress- and treatment-induced elevations of cortisol levels associated with impaired declarative memory in healthy adults. , 1996, Life sciences.

[64]  M. Oitzl,et al.  The Effect of Corticosterone on Reactivity to Spatial Novelty is Mediated by Central Mineralocorticosteroid Receptors , 1994, The European journal of neuroscience.