The neuro-symphony of stress

Nature Reviews Neuroscience

Volumn 10, Issue 6, 2009, Pages 459-466

  Joëls, Marian ^a   Baram, Tallie Z ^b  

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MONOAMINE; NEUROPEPTIDE; NEUROTRANSMITTER; STEROID;

BRAIN FUNCTION; BRAIN NERVE CELL; CELLULAR DISTRIBUTION; HUMAN; MEMORY; MENTAL STRESS; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN INTERACTION; REVIEW; TEMPORAL CORTEX;

ANIMALS; BRAIN; BRAIN MAPPING; HOMEOSTASIS; HUMANS; NERVE NET; NEURONAL PLASTICITY; NEUROTRANSMITTER AGENTS; STRESS, PSYCHOLOGICAL;

EID: 67349151166     PISSN: 1471003X     EISSN: 14710048     Source Type: Journal    
DOI: 10.1038/nrn2632     Document Type: Review

References (82)

1. Ulrich-Lai, Y. M. & Herman, J. P. et al. Neural regulation of endocrine and autonomic stress responses. Nature Rev. Neurosci. (in the press).
2. De Kloet, E. R., Joëls, M. & Holsboer, F. Stress and the brain: from adaptation to disease. Nature Rev. Neurosci. 6, 463-475 (2005).
3. 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).
4. McEwen, B. S. Physiology and neurobiology of stress and adaptation: central role of the brain. Physiol. Rev. 87, 873-904 (2007).
5. McGaugh, J. L. The amygdala modulates the consolidation of memories of emotionally arousing experiences. Annu. Rev. Neurosci. 27, 1 -28 (2004).
6. 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).
7. Lupien, S. J. et al. Stress hormones and human memory function across the lifespan. Psychoneuroendocrinology 30, 225-242 (2005).
8. Shors, T. J. Stressful experience and learning across the lifespan. Annu. Rev. Psychol. 57, 55-85 (2006).
9. 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).
10. 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).
11. 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 agedependent. Mol. Psychiatry 11, 992-1002 (2006).
12. Brunson, K. L. et al. Mechanisms of late-onset cognitive decline after early-life stress. J. Neurosci. 25, 9328-9338 (2005).
13. 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).
14. Morilak, D. A. et al. Role of brain norepinephrine in the behavioral response to stress. Prog. Neuropsychopharmacol. Biol. Psychiatry 29, 1214-1224 (2005).
15. 5. Goto, Y., Otani, S. & Grace, A. A. The yin and yang of dopamine release: a new perspective. Neuropharmacology 53, 583-587 (2007).
16. Linthorst, A. C. & Reul, J. M. Stress and the brain: solving the puzzle using microdialysis. Pharmacol. Biochem. Behav. 90, 163-173 (2008).
17. 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).
18. Piazza, P. V. et al. Glucocorticoids have statedependent stimulant effects on the mesencephalic dopaminergic transmission. Proc. NatlAcad. Sci. USA 93,8716-8720 (1996).
19. Amat, J. et al. Medial prefrontal cortex determines how stressor controllability affects behavior and dorsal raphe nucleus. Nature Neurosci. 8, 365-371 (2005).
20. Jackson, M. E. & Moghaddam, B. Stimulus-specific plasticity of prefrontal cortex dopamine neurotransmission. J. Neurochem. 88, 1327-1334 (2004).
21. 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).
22. 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).
23. 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. CSemin. Med. Genet. 148, 89-98 (2008).
24. 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).
25. 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).
26. Koob, G. F. A role for brain stress systems in addiction. Neuron 59, 11 -34 (2008).
27. Chen, Y., Bender, R. A., Frotscher, M. & Baram, T. Z. Novel and transient populations of corticotropinreleasing hormone-expressing neurons in developing hippocampus suggest unique functional roles: a quantitative spatiotemporal analysis. J. Neurosci. 21, 7171-7181 (2001).
28. 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).
29. 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).
30. 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).
31. 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).
32. Bale, T. L. et al. Mice deficient for corticotropinreleasing hormone receptor-2 display anxiety-like behaviour and are hypersensitive to stress. Nature Genet. 24, 410-414 (2000).
33. 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).
34. Roozendaal, B., Brunson, K. L., Holloway, B. L., McGaugh, J. L. & Baram, T. Z. Involvement of stressreleased corticotropin-releasing hormone in the basolateral amygdala in regulating memory consolidation. Proc. NatlAcad. Sci. USA 99, 13908-13913 (2002).
35. 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).
36. 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).
37. 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).
38. Chen, Y. et al. Modulation of dendritic differentiation by corticotropin-releasing factor in the developing hippocampus. Proc. NatlAcad. Sci. USA 101, 15782-15787 (2004).
39. 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).
40. Ehlers, C. L. et al. Corticotropin releasing factor produces increases in brain excitability and convulsive seizures in rats. Brain Res. 278, 332-336 (1983).
41. Kozicz, T. On the role of urocortin 1 in the nonpreganglionic Edinger-Westphal nucleus in stress adaptation. Gen. Comp. Endocrinol. 153, 235-240 (2007).
42. 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).
43. Raggenbass, M. Overview of cellular electrophysiological actions of vasopressin. Eur. J. Pharmacol. 583, 243-254 (2008).
44. Young, E. A., Abelson, J. & Lightman, S. L. Cortisol pulsatility and its role in stress regulation and health. Front. Neuroendocrinol. 25, 69-76 (2004).
45. 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).
46. 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 ABCB1 A/B-deficient mice. Endocrinology 149, 5244-5253 (2008).
47. 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).
48. 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).
49. 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).
50. Kim, J. J. & Diamond, D. M. The stressed hippocampus, synaptic plasticity and lost memories. Nature Rev. Neurosci. 3, 453-462 (2002).
51. Champagne, D. L. et al. Maternal care and hippocampal plasticity: evidence for experiencedependent structural plasticity, altered synaptic functioning, and differential responsiveness to glucocorticoids and stress. J. Neurosci. 28, 6037-6045 (2008).
52. Duvarci, S. & Paré, D. Glucocorticoids enhance the excitability of principal basolateral amygdala neurons. J. Neurosci. 27, 4482-4491 (2007).
53. Bloom, F. E. The functional significance of neurotransmitter diversity. Am. J. Physiol. 246, C184-C194 (1984).
54. 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 dualcolor labeling with green fluorescent protein spectral variants. Mol. Endocrinol. 15, 1077-1092 (2001).
55. 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).
56. Chen, Y. et al. Hippocampal corticotropin releasing hormone: pre- and postsynaptic location and release by stress. Neuroscience 126, 533-540 (2004).
57. 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).
58. 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).
59. 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).
60. Reyes, B. A., Valentino, R. J. & Van Bockstaele, E. J. Stress-induced intracellular trafficking of corticotropinreleasing factor receptors in rat locus coeruleus neurons. Endocrinology 149, 122-130 (2008).
61. Joëls, M., Pu, Z., Wiegert, O. & Krugers, H. J. Learning under stress: how does it work? Trends Cogn. Sci. 10, 152-158 (2006).
62. McIntyre,C. K. et al. Memory-influencing intrabasolateral amygdala drug infusions modulate expression of Arc protein in the hippocampus. Proc. NatlAcad. Sci. USA 102, 10718-10723 (2005).
63. Sabban, E. L. & Kvetnansky, R. Stress-triggered activation of gene expression in catecholaminergic systems: dynamics of transcriptional events. Trends Neurosci. 24, 91-98 (2001).
64. Tasker, J. G., Di, S. & Malcher-Lopes, R. Minireview: rapid glucocorticoid signaling via membraneassociated receptors. Endocrinology 147, 5549-5556 (2006).
65. Karst, H. et al. Mineralocorticoid receptors are indispensable for nongenomic modulation of hippocampal glutamate transmission by corticosterone. Proc. NatlAcad. Sci. USA 102, 19204-19207 (2005).
66. Groc, L., Choquet, D. & Chaouloff, F. The stress hormone corticosterone conditions AMPAR surface trafficking and synaptic potentiation. Nature Neurosci. 11, 868-870 (2008).
67. Joëls, M., Karst, H., DeRijk, R. & de Kloet, E. R. The coming out of the brain mineralocorticoid receptor. Trends Neurosci. 31, 1-7 (2008).
68. Kreibich, A. et al. Presynaptic inhibition of diverse afferents to the locus ceruleus by K-opiate receptors: a novel mechanism for regulating the central norepinephrine system. J. Neurosci. 28, 6516-6525 (2008).
69. 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).
70. Pu, Z., Krugers, H. J. & Joëls, M. Corticosterone timedependently modulates beta-adrenergic effects on long-term potentiation in the hippocampal dentate gyrus. Learn. Mem. 14, 359-367 (2007).
71. Akirav, I. & Richter-Levin, G. Mechanisms of amygdala modulation of hippocampal plasticity. J. Neurosci. 22, 9912-9921 (2002).
72. Roozendaal, B., Okuda, S., de Quervain, D. J. & McGaugh, J. L. Glucocorticoids interact with emotioninduced noradrenergic activation in influencing different memory functions. Neuroscience 138, 901-910 (2006).
73. Orozco-Cabal, L. et al. Dopamine and corticotropinreleasing factor synergistically alter basolateral amygdala-to-medial prefrontal cortex synaptic transmission: functional switch after chronic cocaine administration. J. Neurosci. 28, 529-542 (2008).
74. 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).
75. Rainbow, T. C., Parsons, B. & Wolfe, B. B. Quantitative autoradiography of β 1 - and β2-adrenergic receptors in rat brain. Proc. Natl Acad. Sci. USA 81, 1585-1589 (1984).
76. 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).
77. Härfstrand, A. et al. Glucocorticoid receptor immunoreactivity in monoaminergic neurons of rat brain. Proc. NatlAcad. Sci. USA 83, 9779-9783 (1986).
78. 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).
79. 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).
80. Avishai-Eliner, S., Brunson, K. L., Sandman, C. A. & Baram, T. Z. Stressed-out, or in (utero)? Trends Neurosci. 25, 518-524 (2002).
81. Lim, M. M. et al. CRF receptors in the nucleus accumbens modulate partner preference in prairie voles. Horm. Behav. 51, 508-515 (2007).
82. 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).