The neuro-symphony of stress

Nature Reviews Neuroscience - Tập 10 Số 6 - Trang 459-466 - 2009
Marian Joëls1, Tallie Z. Baram2
1SILS-CNS, University of Amsterdam, The Netherlands
2Departments of Pediatrics and Anatomy & Neurobiology, Tallie Z. Baram is at the University of California, Irvine, Medical Sciences I, ZOT 4475, Irvine, California 92697-4475, USA. [email protected],

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Ulrich-Lai, Y. M. & Herman, J. P. et al. Neural regulation of endocrine and autonomic stress responses. Nature Rev. Neurosci. (in the press).

De Kloet, E. R., Joëls, M. & Holsboer, F. Stress and the brain: from adaptation to disease. Nature Rev. Neurosci. 6, 463–475 (2005).

Fenoglio, K. A., Brunson, K. L. & Baram, T. Z. Hippocampal neuroplasticity induced by early-life stress: functional and molecular aspects. Front. Neuroendocrinol. 27, 180–192 (2006).

McEwen, B. S. Physiology and neurobiology of stress and adaptation: central role of the brain. Physiol. Rev. 87, 873–904 (2007).

McGaugh, J. L. The amygdala modulates the consolidation of memories of emotionally arousing experiences. Annu. Rev. Neurosci. 27, 1–28 (2004).

Joëls, M., Karst, H., Krugers, H. J. & Lucassen, P. J. Chronic stress: implications for neuronal morphology, function and neurogenesis. Front. Neuroendocrinol. 28, 72–96 (2007).

Lupien, S. J. et al. Stress hormones and human memory function across the lifespan. Psychoneuroendocrinology 30, 225–242 (2005).

Shors, T. J. Stressful experience and learning across the lifespan. Annu. Rev. Psychol. 57, 55–85 (2006).

Baram, T. Z. & Hatalski, C. G. Neuropeptide-mediated excitability: a key triggering mechanism for seizure generation in the developing brain. Trends Neurosci. 21, 471–476 (1998).

Rice, C. J., Sandman, C. A., Lenjavi, M. R. & Baram, T. Z. A novel mouse model for acute and long-lasting consequences of early life stress. Endocrinology 149, 4892–4900 (2008).

Chen, Y., Fenoglio, K. A., Dube, C. M., Grigoriadis, D. E. & Baram, T. Z. Cellular and molecular mechanisms of hippocampal activation by acute stress are age-dependent. Mol. Psychiatry 11, 992–1002 (2006).

Brunson, K. L. et al. Mechanisms of late-onset cognitive decline after early-life stress. J. Neurosci. 25, 9328–9338 (2005).

Maier, S. F. & Watkins, L. R. Stressor controllability and learned helplessness: the roles of the dorsal raphe nucleus, serotonin, and corticotropin-releasing factor. Neurosci. Biobehav. Rev. 29, 829–841 (2005).

Morilak, D. A. et al. Role of brain norepinephrine in the behavioral response to stress. Prog. Neuropsychopharmacol. Biol. Psychiatry 29, 1214–1224 (2005).

Goto, Y., Otani, S. & Grace, A. A. The yin and yang of dopamine release: a new perspective. Neuropharmacology 53, 583–587 (2007).

Linthorst, A. C. & Reul, J. M. Stress and the brain: solving the puzzle using microdialysis. Pharmacol. Biochem. Behav. 90, 163–173 (2008).

Mitsushima, D., Yamada, K., Takase, K., Funabashi, T. & Kimura, F. Sex differences in the basolateral amygdala: the extracellular levels of serotonin and dopamine, and their responses to restraint stress in rats. Eur. J. Neurosci. 24, 3245–3254 (2006).

Piazza, P. V. et al. Glucocorticoids have state-dependent stimulant effects on the mesencephalic dopaminergic transmission. Proc. Natl Acad. Sci. USA 93, 8716–8720 (1996).

Amat, J. et al. Medial prefrontal cortex determines how stressor controllability affects behavior and dorsal raphe nucleus. Nature Neurosci. 8, 365–371 (2005).

Jackson, M. E. & Moghaddam, B. Stimulus-specific plasticity of prefrontal cortex dopamine neurotransmission. J. Neurochem. 88, 1327–1334 (2004).

Aston-Jones, G. & Cohen, J. D. An integrative theory of locus coeruleus-norepinephrine function: adaptive gain and optimal performance. Annu. Rev. Neurosci. 28, 403–450 (2005).

Adamec, R., Holmes, A. & Blundell, J. Vulnerability to lasting anxiogenic effects of brief exposure to predator stimuli: sex, serotonin and other factors-relevance to PTSD. Neurosci. Biobehav. Rev. 32, 1287–1292 (2008).

Mathew, S. J., Price, R. B. & Charney, D. S. Recent advances in the neurobiology of anxiety disorders: implications for novel therapeutics. Am. J. Med. Genet. C Semin. Med. Genet. 148, 89–98 (2008).

Swanson, L. W., Sawchenko, P. E., Rivier, J. & Vale, W. W. Organization of ovine corticotropin-releasing factor immunoreactive cells and fibers in the rat brain: an immunohistochemical study. Neuroendocrinology 36, 165–186 (1983).

Landgraf, R. & Neumann, I. D. Vasopressin and oxytocin release within the brain: a dynamic concept of multiple and variable modes of neuropeptide communication. Front. Neuroendocrinol. 25, 150–176 (2004).

Koob, G. F. A role for brain stress systems in addiction. Neuron 59, 11–34 (2008).

Chen, Y., Bender, R. A., Frotscher, M. & Baram, T. Z. Novel and transient populations of corticotropin-releasing hormone-expressing neurons in developing hippocampus suggest unique functional roles: a quantitative spatiotemporal analysis. J. Neurosci. 21, 7171–7181 (2001).

Valentino, R. J. & Van Bockstaele, E. Convergent regulation of locus coeruleus activity as an adaptive response to stress. Eur. J. Pharmacol. 583, 194–203 (2008).

Aldenhoff, J. B., Gruol, D. L., Rivier, J., Vale, W. & Siggins, G. R. Corticotropin releasing factor decreases postburst hyperpolarizations and excites hippocampal neurons. Science 221, 875–877 (1983).

Gallagher, J. P., Orozco-Cabal, L. F., Liu, J. & Shinnick-Gallagher, P. Synaptic physiology of central CRH system. Eur. J. Pharmacol. 583, 215–225 (2008).

Coste, S. C. et al. Abnormal adaptations to stress and impaired cardiovascular function in mice lacking corticotropin-releasing hormone receptor-2. Nature Genet. 24, 403–409 (2000).

Bale, T. L. et al. Mice deficient for corticotropin-releasing hormone receptor-2 display anxiety-like behaviour and are hypersensitive to stress. Nature Genet. 24, 410–414 (2000).

Muller, M. B. et al. Limbic corticotropin-releasing hormone receptor 1 mediates anxiety-related behavior and hormonal adaptation to stress. Nature Neurosci. 6, 1100–1107 (2003).

Roozendaal, B., Brunson, K. L., Holloway, B. L., McGaugh, J. L. & Baram, T. Z. Involvement of stress-released corticotropin-releasing hormone in the basolateral amygdala in regulating memory consolidation. Proc. Natl Acad. Sci. USA 99, 13908–13913 (2002).

Merali, Z., Khan, S., Michaud, D. S., Shippy, S. A. & Anisman, H. Does amygdaloid corticotropin-releasing hormone (CRH) mediate anxiety-like behaviors? Dissociation of anxiogenic effects and CRH release. Eur. J. Neurosci. 20, 229–239 (2004).

Blank, T., Nijholt, I., Eckart, K. & Spiess, J. Priming of long-term potentiation in mouse hippocampus by corticotropin-releasing factor and acute stress: implications for hippocampus-dependent learning. J. Neurosci. 22, 3788–3794 (2002).

Wang, H. L., Wayner, M. J., Chai, C. Y. & Lee, E. H. Corticotrophin-releasing factor produces a long-lasting enhancement of synaptic efficacy in the hippocampus. Eur. J. Neurosci. 10, 3428–3437 (1998).

Chen, Y. et al. Modulation of dendritic differentiation by corticotropin-releasing factor in the developing hippocampus. Proc. Natl Acad. Sci. USA 101, 15782–15787 (2004).

Chen, Y., Dube, C. M., Rice, C. J. & Baram, T. Z. Rapid loss of dendritic spines after stress involves derangement of spine dynamics by corticotropin-releasing hormone. J. Neurosci. 28, 2903–2911 (2008).

Ehlers, C. L. et al. Corticotropin releasing factor produces increases in brain excitability and convulsive seizures in rats. Brain Res. 278, 332–336 (1983).

Kozicz, T. On the role of urocortin 1 in the non-preganglionic Edinger-Westphal nucleus in stress adaptation. Gen. Comp. Endocrinol. 153, 235–240 (2007).

Harbuz, M. S. et al. Paradoxical responses of hypothalamic corticotropin-releasing factor (CRF) messenger ribonucleic acid (mRNA) and CRF-41 peptide and adenohypophysial proopiomelanocortin mRNA during chronic inflammatory stress. Endocrinology 130, 1394–1400 (1992).

Raggenbass, M. Overview of cellular electrophysiological actions of vasopressin. Eur. J. Pharmacol. 583, 243–254 (2008).

Young, E. A., Abelson, J. & Lightman, S. L. Cortisol pulsatility and its role in stress regulation and health. Front. Neuroendocrinol. 25, 69–76 (2004).

Karssen, A. M. et al. Multidrug resistance P-glycoprotein hampers the access of cortisol but not of corticosterone to mouse and human brain. Endocrinology 142, 2686–2694 (2001).

Mason, B. L., Pariante, C. M. & Thomas, S. A. A revised role for p-glycoprotein in the brain distribution of dexamethasone, cortisol, and corticosterone in wild type and ABCB1A/B-deficient mice. Endocrinology 149, 5244–5253 (2008).

Droste, S. K. et al. Corticosterone levels in the brain show a distinct ultradian rhythm but a delayed response to forced swim stress. Endocrinology 149, 3244–3253 (2008).

Chen, Y., Brunson, K. L., Muller, M. B., Cariaga, W. & Baram, T. Z. Immunocytochemical distribution of corticotropin-releasing hormone receptor type-1 (CRF1)-like immunoreactivity in the mouse brain: light microscopy analysis using an antibody directed against the C-terminus. J. Comp. Neurol. 420, 305–323 (2000).

Lu, N. Z. et al. International Union of Pharmacology. LXV. The pharmacology and classification of the nuclear receptor superfamily: glucocorticoid, mineralocorticoid, progesterone, and androgen receptors. Pharmacol. Rev. 58, 782–797 (2006).

Kim, J. J. & Diamond, D. M. The stressed hippocampus, synaptic plasticity and lost memories. Nature Rev. Neurosci. 3, 453–462 (2002).

Champagne, D. L. et al. Maternal care and hippocampal plasticity: evidence for experience-dependent structural plasticity, altered synaptic functioning, and differential responsiveness to glucocorticoids and stress. J. Neurosci. 28, 6037–6045 (2008).

Duvarci, S. & Paré, D. Glucocorticoids enhance the excitability of principal basolateral amygdala neurons. J. Neurosci. 27, 4482–4491 (2007).

Bloom, F. E. The functional significance of neurotransmitter diversity. Am. J. Physiol. 246, C184–C194 (1984).

Nishi, M., Ogawa, H., Ito, T., Matsuda, K. I. & Kawata, M. Dynamic changes in subcellular localization of mineralocorticoid receptor in living cells: in comparison with glucocorticoid receptor using dual-color labeling with green fluorescent protein spectral variants. Mol. Endocrinol. 15, 1077–1092 (2001).

Olijslagers, J. E. et al. Rapid changes in hippocampal CA1 pyramidal cell function via pre- as well as postsynaptic membrane mineralocorticoid receptors. Eur. J. Neurosci. 27, 2542–2550 (2008).

Chen, Y. et al. Hippocampal corticotropin releasing hormone: pre- and postsynaptic location and release by stress. Neuroscience 126, 533–540 (2004).

Swanson, L. W., Kohler, C. & Björklund, A. in Handbook of Chemical Neuroanatomy vol. 5 (eds Björklund, A., Hökfelt, T. & Swanson, L. W.) 125–227 (Elsevier, Amsterdam, 1987).

Oleskevich, S., Descarries, L. & Lacaille, J. C. Quantified distribution of the noradrenaline innervation in the hippocampus of adult rat. J. Neurosci. 9, 3803–3815 (1989).

Johnson, L. R., Farb, C., Morrison, J. H., McEwen, B. S. & LeDoux, J. E. Localization of glucocorticoid receptors at postsynaptic membranes in the lateral amygdala. Neuroscience 136, 289–299 (2005).

Reyes, B. A., Valentino, R. J. & Van Bockstaele, E. J. Stress-induced intracellular trafficking of corticotropin-releasing factor receptors in rat locus coeruleus neurons. Endocrinology 149, 122–130 (2008).

Joëls, M., Pu, Z., Wiegert, O. & Krugers, H. J. Learning under stress: how does it work? Trends Cogn. Sci. 10, 152–158 (2006).

McIntyre, C. K. et al. Memory-influencing intra-basolateral amygdala drug infusions modulate expression of Arc protein in the hippocampus. Proc. Natl Acad. Sci. USA 102, 10718–10723 (2005).

Sabban, E. L. & Kvetnansky, R. Stress-triggered activation of gene expression in catecholaminergic systems: dynamics of transcriptional events. Trends Neurosci. 24, 91–98 (2001).

Tasker, J. G., Di, S. & Malcher-Lopes, R. Minireview: rapid glucocorticoid signaling via membrane-associated receptors. Endocrinology 147, 5549–5556 (2006).

Karst, H. et al. Mineralocorticoid receptors are indispensable for nongenomic modulation of hippocampal glutamate transmission by corticosterone. Proc. Natl Acad. Sci. USA 102, 19204–19207 (2005).

Groc, L., Choquet, D. & Chaouloff, F. The stress hormone corticosterone conditions AMPAR surface trafficking and synaptic potentiation. Nature Neurosci. 11, 868–870 (2008).

Joëls, M., Karst, H., DeRijk, R. & de Kloet, E. R. The coming out of the brain mineralocorticoid receptor. Trends Neurosci. 31, 1–7 (2008).

Kreibich, A. et al. Presynaptic inhibition of diverse afferents to the locus ceruleus by κ-opiate receptors: a novel mechanism for regulating the central norepinephrine system. J. Neurosci. 28, 6516–6525 (2008).

Curtis, A. L., Bello, N. T. & Valentino, R. J. Evidence for functional release of endogenous opioids in the locus ceruleus during stress termination. J. Neurosci. 21, RC152 (2001).

Pu, Z., Krugers, H. J. & Joëls, M. Corticosterone time-dependently modulates beta-adrenergic effects on long-term potentiation in the hippocampal dentate gyrus. Learn. Mem. 14, 359–367 (2007).

Akirav, I. & Richter-Levin, G. Mechanisms of amygdala modulation of hippocampal plasticity. J. Neurosci. 22, 9912–9921 (2002).

Roozendaal, B., Okuda, S., de Quervain, D. J. & McGaugh, J. L. Glucocorticoids interact with emotion-induced noradrenergic activation in influencing different memory functions. Neuroscience 138, 901–910 (2006).

Orozco-Cabal, L. et al. Dopamine and corticotropin-releasing factor synergistically alter basolateral amygdala-to-medial prefrontal cortex synaptic transmission: functional switch after chronic cocaine administration. J. Neurosci. 28, 529–542 (2008).

Chalmers, D. T., Lovenberg, T. W. & De Souza, E. B. Localization of novel corticotropin-releasing factor receptor (CRF2) mRNA expression to specific subcortical nuclei in rat brain: comparison with CRF1 receptor mRNA expression. J. Neurosci. 15, 6340–6350 (1995).

Rainbow, T. C., Parsons, B. & Wolfe, B. B. Quantitative autoradiography of b1- and b2-adrenergic receptors in rat brain. Proc. Natl Acad. Sci. USA 81, 1585–1589 (1984).

Reul, J. M. H. M. & de Kloet, E. R. Anatomical resolution of two types of corticosterone receptor sites in rat brain with in vitro autoradiography and computerized image analysis. J. Steroid Biochem. 24, 269–272 (1986).

Härfstrand, A. et al. Glucocorticoid receptor immunoreactivity in monoaminergic neurons of rat brain. Proc. Natl Acad. Sci. USA 83, 9779–9783 (1986).

Van Pett, K. et al. Distribution of mRNAs encoding CRF receptors in brain and pituitary of rat and mouse. J. Comp. Neurol. 428, 191–212 (2000).

Pu, Z., Krugers, H. J. & Joëls, M. Beta-adrenergic facilitation of synaptic plasticity in the rat basolateral amygdala in vitro is gradually reversed by corticosterone. Learn. Mem. 16, 155–160 (2009).

Avishai-Eliner, S., Brunson, K. L., Sandman, C. A. & Baram, T. Z. Stressed-out, or in (utero)? Trends Neurosci. 25, 518–524 (2002).

Lim, M. M. et al. CRF receptors in the nucleus accumbens modulate partner preference in prairie voles. Horm. Behav. 51, 508–515 (2007).

Chavkin, C. Dynorphins are endogenous opioid peptides released from granule cells to act neurohumorally and inhibit excitatory neurotransmission in the hippocampus. Prog. Brain Res. 125, 363–367 (2000).