Abstract
Corticosterone, the major stress hormone, serves as a key controller for neuronal responses that underlie behavioral adaptation, as well as maladaptive changes that lead to cognitive and emotional disturbances in stress-related mental disorders. The molecular and cellular mechanisms underlying the complex actions of corticosteroid stress hormones are largely unknown. Here we demonstrate that acute versus chronic stress exerts opposite effects on glutamatergic transmission in prefrontal cortex (PFC), which leads to opposing effects on PFC-dependent cognitive functions. Acute stress induces synaptic potentiation by increasing surface delivery of N-methyl-D-aspartate (NMDA)-type and α-amino-3-hydroxy-methyl-4-isoxazole propionic acid (AMPA)-type glutamate receptor channels via glucocorticoid/serum- and glucocorticoid-inducible kinase (SGK)/Rab4 signaling, resulting in enhanced working memory performance. In contrast, repeated stress induces synaptic depression by increasing the ubiquitin/proteasome-mediated degradation of NMDA and AMPA receptor subunits, resulting in impaired recognition memory.
This is a preview of subscription content, log in via an institution.
Buying options
Tax calculation will be finalised at checkout
Purchases are for personal use only
Learn about institutional subscriptionsAbbreviations
- AMPA:
-
α-amino-3-hydroxy-methyl-4-isoxazole propionic acid
- NMDA:
-
N-methyl-D-aspartate
- PFC:
-
Prefrontal cortex
- GR:
-
Glucocorticoid receptor
- MR:
-
Mineralocorticoid receptors
- ESPC:
-
Excitatory postsynaptic current
- SGK:
-
Serum- and glucocorticoid-inducible kinase
- WM:
-
Working memory
- TOR:
-
Temporal order recognition
- DR:
-
Discrimination ratio
References
Barker GR, Bird F, Alexander V, Warburton EC. Recognition memory for objects, place, and temporal order: a disconnection analysis of the role of the medial prefrontal cortex and perirhinal cortex. J Neurosci. 2007;27:2948–57.
Cerqueira JJ, Mailliet F, Almeida OF, Jay TM, Sousa N. The prefrontal cortex as a key target of the maladaptive response to stress. J Neurosci. 2007;27:2781–7.
Ciechanover A, Brundin P. The ubiquitin proteasome system in neurodegenerative diseases: sometimes the chicken, sometimes the egg. Neuron. 2003;40:427–46.
de Kloet ER, Joëls M, Holsboer F. Stress and the brain: from adaptation to disease. Nat Rev Neurosci. 2005;6:463–75.
Diamond DM, Bennett MC, Fleshner M, Rose GM. Inverted-U relationship between the level of peripheral corticosterone and the magnitude of hippocampal primed burst potentiation. Hippocampus. 1992;2:421–30.
Dix S, Aggleton J. Extending the spontaneous preference test of recognition: evidence of object-location and object-context recognition. Behav Brain Res. 1999;99:191–200.
Ennaceur A, Delacour J. A new one-trial test for neurobiological studies of memory in rats. 1: behavioral data. Behav Brain Res. 1988;31:47–59.
Goldman-Rakic PS. Cellular basis of working memory. Neuron. 1995;14:477–85.
Groc L, Choquet D, Chaouloff F. The stress hormone corticosterone conditions AMPAR surface trafficking and synaptic potentiation. Nat Neurosci. 2008;11:868–70.
Henckens MJ, van Wingen GA, Joëls M, Fernández G. Time-dependent corticosteroid modulation of prefrontal working memory processing. Proc Natl Acad Sci U S A. 2011;108:5801–6.
Joëls M. Corticosteroid effects in the brain: U-shape it. Trends Pharmacol Sci. 2006;27:244–50.
Joëls M, Pu Z, Wiegert O, Oitzl MS, Krugers HJ. Learning under stress: how does it work? Trends Cogn Sci. 2006;10:152–8.
Kato A, Rouach N, Nicoll RA, Bredt DS. Activity-dependent NMDA receptor degradation mediated by retrotranslocation and ubiquitination. Proc Natl Acad Sci U S A. 2005;102:5600–5.
Krugers HJ, Hoogenraad CC, Groc L. Stress hormones and AMPA receptor trafficking in synaptic plasticity and memory. Nat Rev Neurosci. 2010;11:675–81.
Lang F, Cohen P. Regulation and physiological roles of serum- and glucocorticoid-induced protein kinase isoforms. Sci STKE. 2001;2001(108):re17.
Lee JB, Wei J, Liu W, Cheng J, Feng J, Yan Z. Histone Deacetylase 6 gates the synaptic action of acute stress in prefrontal cortex. J Physiol. 2012;90:1535–46.
Lin A, Hou Q, Jarzylo L, Amato S, Gilbert J, Shang F, Man HY. Nedd4-mediated AMPA receptor ubiquitination regulates receptor turnover and trafficking. J Neurochem. 2011;119:27–39.
Lisman JE, Fellous JM, Wang XJ. A role for NMDA-receptor channels in working memory. Nat Neurosci. 1998;1:273–5.
Liston C, Miller MM, Goldwater DS, Radley JJ, Rocher AB, Hof PR, et al. Stress-induced alterations in prefrontal cortical dendritic morphology predict selective impairments in perceptual attentional set-shifting. J Neurosci. 2006;26:7870–4.
Liu W. Yuen EY, Yan Z. The stress hormone corticosterone increases synaptic AMPA receptors via SGK regulation of the GDI-Rab4 complex. J Biol Chem. 2010;285:6101–8.
Mabb AM, Ehlers MD. Ubiquitination in postsynaptic function and plasticity. Annu Rev Cell Dev Biol. 2010;26:179–210.
McEwen BS. Protective and damaging effects of stress mediators. N Engl J Med. 1998;338:171–9.
McEwen BS. Stress and hippocampal plasticity. Annu Rev Neurosci. 1999;22:105–22.
McEwen BS. Physiology and neurobiology of stress and adaptation: central role of the brain. Physiol Rev. 2007;87:873–904.
Middleton FA, Mirnics K, Pierri JN, Lewis DA, Levitt P. Gene expression profiling reveals alterations of specific metabolic pathways in schizophrenia. J Neurosci. 2002;22:2718–29.
Moghaddam B. Bringing order to the glutamate chaos in schizophrenia. Neuron. 2003;40:881–4.
Popoli M, Yan Z, McEwen BS, Sanacora G. The stressed synapse: the impact of stress and glucocorticoids on glutamate transmission. Nat Rev Neurosci. 2012;13:22–37.
Schwarz LA, Hall BJ, Patrick GN. Activity-dependent ubiquitination of GluA1 mediates a distinct AMPA receptor endocytosis and sorting pathway. J Neurosci. 2010;30:16718–29.
Shors TJ. Stressful experience and learning across the lifespan. Annu Rev Psychol. 2006;57:55–85.
Shors TJ, Weiss C, Thompson RF. Stress-induced facilitation of classical conditioning. Science. 1992;257:537–9.
Tsai G, Coyle JT. Glutamatergic mechanisms in schizophrenia. Annu Rev Pharm Toxicol. 2002;42:165–79.
Wei J, Yuen EY, Liu W, Li X, Zhong P, Karatsoreos IN, McEwen BS, Yan Z Estrogen protects against the detrimental effects of repeated stress on glutamatergic transmission and cognition. Mol Psychiatry. 2013 (Epub ahead of print).
Yuen EY, Liu W, Karatsoreos IN, Feng J, McEwen BS, Yan Z. Acute stress enhances glutamatergic transmission in prefrontal cortex and facilitates working memory. Proc Natl Acad Sci U S A. 2009;106:14075–9.
Yuen EY, Liu W, Karatsoreos IN, Ren Y, Feng J, McEwen BS, Yan Z. Mechanisms for acute stress-induced enhancement of glutamatergic transmission and working memory. Mol Psychiatry. 2011;16:156–70.
Yuen EY, Wei J, Liu W, Zhong P, Li X, Yan Z. Repeated stress causes cognitive impairment by suppressing glutamate receptor expression and function in prefrontal cortex. Neuron. 2012;73:962–77.
Zerial M, McBride H. Rab proteins as membrane organizers. Nat Rev Mol Cell Biol. 2001;2:107–17.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2014 Springer Science+Business Media New York
About this chapter
Cite this chapter
Zhen, Y. (2014). Dual Regulation of Glutamatergic Transmission and Cognition by Stress in Prefrontal Cortex. 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_4
Download citation
DOI: https://doi.org/10.1007/978-1-4939-1056-4_4
Published:
Publisher Name: Springer, New York, NY
Print ISBN: 978-1-4939-1055-7
Online ISBN: 978-1-4939-1056-4
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)