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Regulation of Excitatory Synapses by Stress Hormones

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Synaptic Stress and Pathogenesis of Neuropsychiatric Disorders

Abstract

Shortly after stress, brain levels of many transmitters and hormones such as corticosterone are elevated. In the brain, corticosterone affects those cells that express high-affinity mineralocorticoid receptors (MRs) and/or lower-affinity glucocorticoid receptors (GRs). Principal neurons in the hippocampal cornus ammoni 1 (CA1) area and dentate gyrus abundantly express both MR and GR, while principal cells in the basolateral amygdala have high GR but relatively low MR levels. Neurons in all three areas quickly respond to corticosterone with an enhancement in spontaneous glutamatergic transmission, an effect that is nongenomic and involves MR. This rapid effect is transient in hippocampal cells but sustained in amygdala neurons. The areas differ in their slow gene-mediated response to corticosterone. Hippocampal CA1 cells show an increased current amplitude in response to spontaneously released glutamate-containing vesicles; synaptically evoked responses are generally unaffected. The number of action potentials during a period of depolarization is attenuated, via a slow GR-dependent pathway. By contrast, basolateral amygdala neurons show higher excitability and more efficient transfer of action potentials several hours after corticosteroid exposure. The dichotomy between the two areas could explain why emotional aspects of stressful events are generally better retained than neutral aspects.

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Abbreviations

AHP:

Afterhyperpolarization

AMPA:

α-Amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid

BLA:

Basolateral amygdala

BSA:

Bovine serum albumin

CA1:

Cornus ammoni 1

(m)EPSC/EPSP:

(Miniature) Excitatory postsynaptic current/potential

ERK:

Extracellular signal-regulated kinase

GR:

Glucocorticoid receptor

LTD:

Long-term depression

LTP:

Long-term potentiation

MEK:

Mitogen-activated protein kinase kinase

MR:

Mineralocorticoid receptor

NMDA:

N-methyl-D-aspartate

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Authors and Affiliations

  1. Department of Translational Neuroscience, Brain Center Rudolf Magnus, University Medical Center, 3584, Utrecht, The Netherlands

    Marian Joëls & Henk Karst

  2. Swammerdam Institute for Life Sciences—Center for Neuroscience, University of Amsterdam, Amsterdam, The Netherlands

    Harm Krugers

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  1. Marian Joëls
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  2. Harm Krugers
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Correspondence to Marian Joëls .

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Editors and Affiliations

  1. Department of Pharmacological and Biomolecular Sciences, University of Milano, Milano, Italy

    Maurizio Popoli

  2. Department of Psychology, University of South Florida, Tampa, Florida, USA

    David Diamond

  3. Psychiatry Depression Research Program, Yale School of Medicine, New Haven, Connecticut, USA

    Gerard Sanacora

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Joëls, M., Krugers, H., Karst, H. (2014). Regulation of Excitatory Synapses by Stress Hormones. In: Popoli, M., Diamond, D., Sanacora, G. (eds) Synaptic Stress and Pathogenesis of Neuropsychiatric Disorders. Springer, New York, NY. https://doi.org/10.1007/978-1-4939-1056-4_2

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