Too much of a good thing: Blocking noradrenergic facilitation in medial prefrontal cortex prevents the detrimental effects of chronic stress on cognition

Neuropsychopharmacology

Volumn 38, Issue 4, 2013, Pages 585-595

  Jett, Julianne D ^a   Morilak, David A ^a  

^a University of Texas Health Science Center   (United States)

Author keywords

chronic stress; cognitive flexibility; depression; medial prefrontal cortex; norepinephrine

Indexed keywords

ADRENERGIC RECEPTOR; ALPHA 1 ADRENERGIC RECEPTOR BLOCKING AGENT; ALPHA ADRENERGIC RECEPTOR; BETA 1 ADRENERGIC RECEPTOR BLOCKING AGENT; BETA 2 ADRENERGIC RECEPTOR BLOCKING AGENT; NORADRENALIN;

ACUTE STRESS; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CHRONIC STRESS; CHRONIC UNPREDICTABLE STRESS; COGNITION; COGNITIVE DEFECT; CONTROLLED STUDY; MALE; MICRODIALYSIS; NONHUMAN; NORADRENALIN RELEASE; NORADRENERGIC SYSTEM; PREFRONTAL CORTEX; PRIORITY JOURNAL; RAT;

ADRENERGIC BETA-ANTAGONISTS; ANIMALS; CHRONIC DISEASE; COGNITION; COGNITION DISORDERS; MALE; NOREPINEPHRINE; PREFRONTAL CORTEX; RATS; RATS, SPRAGUE-DAWLEY; STRESS, PSYCHOLOGICAL;

EID: 84873745560     PISSN: 0893133X     EISSN: 1740634X     Source Type: Journal    
DOI: 10.1038/npp.2012.216     Document Type: Article

References (85)

1. Anisman H, Zacharko RM (1990). Multiple neurochemical and behavioral consequences of stressors: implications for depression. Pharmacol Ther 46: 119-136.
2. Aston-Jones G, Chiang C, Alexinsky T (1991). Discharge of noradrenergic locus coeruleus neurons in behaving rats and monkeys suggests a role in vigilance. Prog Brain Res 88: 501-520.
3. Aston-Jones G, Rajkowski J, Cohen J (1999). Role of locus coeruleus in attention and behavioral flexibility. Biol Psychiatry 46: 1309-1320.
4. Aston-Jones G, Rajkowski J, Cohen J (2000). Locus coeruleus and regulation of behavioral flexibility and attention. Prog Brain Res 126: 165-182.
5. Austin MP, Mitchell P, Goodwin GM (2001). Cognitive deficits in depression: possible implications for functional neuropathology. Br J Psychiatry 178: 200-206.
6. Bagley J, Moghaddam B (1997). Temporal dynamics of glutamate efflux in the prefrontal cortex and in the hippocampus following repeated stress: effects of pretreatment with saline or diazepam. Neuroscience 77: 65-73.
7. Beck AT (2005). The current state of cognitive therapy: a 40-year retrospective. Arch Gen Psychiatry 62: 953-959.
8. Beck AT, Brown G, Steer RA, Eidelson JI, Riskind JH (1987). Differentiating anxiety and depression: a test of the cognitive content-specificity hypothesis. J Abnorm Psychol 96: 179-183.
9. Berridge CW, Page ME, Valentino RJ, Foote SL (1993). Effects of locus coeruleus inactivation on electroencephalographic activity in neocortex and hippocampus. Neuroscience 55: 381-393.
10. Berridge CW, Waterhouse BD (2003). The locus coeruleusnoradrenergic system: modulation of behavioral state and state-dependent cognitive processes. Brain Res Brain Res Rev 42: 33-84.
11. Birrell JM, Brown VJ (2000). Medial frontal cortex mediates perceptual attentional set shifting in the rat. J Neurosci 20: 4320-4324.
12. Bondi CO, Barrera G, Lapiz MD, Bedard T, Mahan A, Morilak DA (2007). Noradrenergic facilitation of shock-probe defensive burying in lateral septum of rats, and modulation by chronic treatment with desipramine. Prog Neuropsychopharmacol Biol Psychiatry 31: 482-495.
13. Bondi CO, Jett JD, Morilak DA (2010). Beneficial effects of desipramine on cognitive function of chronically stressed rats are mediated by alpha1-adrenergic receptors in medial prefrontal cortex. Prog Neuropsychopharmacol Biol Psychiatry 34: 913-923.
14. Bondi CO, Rodriguez G, Gould GG, Frazer A, Morilak DA (2008). Chronic unpredictable stress induces a cognitive deficit and anxiety-like behavior in rats that is prevented by chronic antidepressant drug treatment. Neuropsychopharmacology 33: 320-331.
15. Bruno V, Scapagnini U, Canonico PL (1993). Excitatory amino acids and neurotoxicity. Funct Neurol 8: 279-292.
16. Cecchi M, Khoshbouei H, Javors M, Morilak DA (2002a). Modulatory effects of norepinephrine in the lateral bed nucleus of the stria terminalis on behavioral and neuroendocrine responses to acute stress. Neuroscience 112: 13-21.
17. Cecchi M, Khoshbouei H, Morilak DA (2002b). Modulatory effects of norepinephrine, acting on alpha 1 receptors in the central nucleus of the amygdala, on behavioral and neuroendocrine responses to acute immobilization stress. Neuropharmacology 43: 1139-1147.
18. Channon S (1996). Executive dysfunction in depression: the Wisconsin Card Sorting Test. J Affect Disord 39: 107-114.
19. Cole BJ, Robbins TW (1992). Forebrain norepinephrine: role in controlled information processing in the rat. Neuropsychopharmacology 7: 129-142.
20. Cook SC, Wellman CL (2004). Chronic stress alters dendritic morphology in rat medial prefrontal cortex. J Neurobiol 60: 236-248.
21. de Kloet ER, Joels M, Holsboer F (2005). Stress and the brain: from adaptation to disease. Nat Rev Neurosci 6: 463-475.
22. Disner SG, Beevers CG, Haigh EA, Beck AT 2011). Neural mechanisms of the cognitive model of depression. Nat Rev Neurosci 12: 467-477.
23. Fales CL, Barch DM, Rundle MM, Mintun MA, Mathews J, Snyder AZ et al (2009). Antidepressant treatment normalizes hypoactivity in dorsolateral prefrontal cortex during emotional interference processing in major depression. J Affect Disord 112: 206-211.
24. Feyissa AM, Chandran A, Stockmeier CA, Karolewicz B (2009). Reduced levels of NR2A and NR2B subunits of NMDA receptor and PSD-95 in the prefrontal cortex in major depression. Prog Neuropsychopharmacol Biol Psychiatry 33: 70-75.
25. Gehrman PR, Harb GC (2010). Treatment of nightmares in the context of posttraumatic stress disorder. J Clin Psychol 66: 1185-1194.
26. Glavin GB (1985). Stress and brain noradrenaline: a review. Neurosci Biobehav Rev 9: 233-243.
27. Hasler G, van der Veen JW, Tumonis T, Meyers N, Shen J, Drevets WC (2007). Reduced prefrontal glutamate/glutamine and gamma-aminobutyric acid levels in major depression determined using proton magnetic resonance spectroscopy. Arch Gen Psychiatry 64: 193-200.
28. Jacobs BL, Abercrombie ED, Fornal CA, Levine ES, Morilak DA, Stafford IL (1991). Single-unit and physiological analyses of brain norepinephrine function in behaving animals. Prog Brain Res 88: 159-165.
29. Jett JD, Bédard T, Rodriguez G, Morilak DA (2008). Blockade of adrenergic receptors during chronic unpredictable stress prevents the detrimental effects on cognitive flexibility in rats. Soc Neurosci Abstr 34, Online: Program number 195: 8.
30. Ji XH, Cao XH, Zhang CL, Feng ZJ, Zhang XH, Ma L et al (2008). Pre-and postsynaptic beta-adrenergic activation enhances excitatory synaptic transmission in layer V/VI pyramidal neurons of the medial prefrontal cortex of rats. Cereb Cortex 18: 1506-1520.
31. Joels M, Baram TZ (2009). The neuro-symphony of stress. Nat Rev Neurosci 10: 459-466.
32. Joels M, Fernandez G, Roozendaal B 2011). Stress and emotional memory: a matter of timing. Trends Cogn Sci 15: 280-288.
33. Joels M, Pu Z, Wiegert O, Oitzl MS, Krugers HJ (2006). Learning under stress: how does it work? Trends Cogn Sci 10: 152-158.
34. Kendler KS, Karkowski LM, Prescott CA (1998). Stressful life events and major depression: risk period, long-term contextual threat, and diagnostic specificity. J Nerv Ment Dis 186: 661-669.
35. Kendler KS, Karkowski LM, Prescott CA (1999). Causal relationship between stressful life events and the onset of major depression. Am J Psychiatry 156: 837-841.
36. Krugers HJ, Karst H, Joels M (2012). Interactions between noradrenaline and corticosteroids in the brain: from electrical activity to cognitive performance. Front Cell Neurosci 6: 15.
37. Lapiz MD, Morilak DA (2006). Noradrenergic modulation of cognitive function in rat medial prefrontal cortex as measured by attentional set shifting capability. Neuroscience 137: 1039-1049.
38. Lapiz MD, Zhao Z, Bondi CO, O'Donnell JM, Morilak DA (2007). Blockade of autoreceptor-mediated inhibition of norepinephrine release by atipamezole is maintained after chronic reuptake inhibition. Int J Neuropsychopharmacol 10: 827-833.
39. Lee YA, Goto Y 2011). Chronic stress modulation of prefrontal cortical NMDA receptor expression disrupts limbic structure-prefrontal cortex interaction. Eur J Neurosci 34: 426-436.
40. Liston C, McEwen BS, Casey BJ (2009). Psychosocial stress reversibly disrupts prefrontal processing and attentional control. Proc Natl Acad Sci USA 106: 912-917.
41. Liston C, Miller MM, Goldwater DS, Radley JJ, Rocher AB, Hof PR et al (2006). Stress-induced alterations in prefrontal cortical dendritic morphology predict selective impairments in perceptual attentional set-shifting. J Neurosci 26: 7870-7874.
42. Liu RJ, Aghajanian GK (2008). Stress blunts serotonin-and hypocretin-evoked EPSCs in prefrontal cortex: role of corticosterone-mediated apical dendritic atrophy. Proc Natl Acad Sci USA 105: 359-364.
43. Lupinsky D, Moquin L, Gratton A (2010). Interhemispheric regulation of the medial prefrontal cortical glutamate stress response in rats. J Neurosci 30: 7624-7633.
44. Ma S, Morilak DA (2005a). Chronic intermittent cold stress sensitises the hypothalamic-pituitary-adrenal response to a novel acute stress by enhancing noradrenergic influence in the rat paraventricular nucleus. J Neuroendocrinol 17: 761-769.
45. Ma S, Morilak DA (2005b). Norepinephrine release in medial amygdala facilitates activation of the hypothalamic-pituitaryadrenal axis in response to acute immobilisation stress. J Neuroendocrinol 17: 22-28.
46. Magarinos AM, McEwen BS (1995). Stress-induced atrophy of apical dendrites of hippocampal CA3c neurons: comparison of stressors. Neuroscience 69: 83-88.
47. Marek GJ, Aghajanian GK (1999). 5-HT2A receptor or alpha1-adrenoceptor activation induces excitatory postsynaptic currents in layer V pyramidal cells of the medial prefrontal cortex. Eur J Pharmacol 367: 197-206.
48. Martin KP, Wellman CL 2011). NMDA receptor blockade alters stress-induced dendritic remodeling in medial prefrontal cortex. Cereb Cortex 21: 2366-2373.
49. McAlonan K, Brown VJ (2003). Orbital prefrontal cortex mediates reversal learning and not attentional set shifting in the rat. Behav Brain Res 146: 97-103.
50. McEwen BS (2003). Mood disorders and allostatic load. Biol Psychiatry 54: 200-207.
51. McEwen BS (2004). Protection and damage from acute and chronic stress: allostasis and allostatic overload and relevance to the pathophysiology of psychiatric disorders. Ann NY Acad Sci 1032: 1-7.
52. McEwen BS, Conrad CD, Kuroda Y, Frankfurt M, Magarinos AM, McKittrick C (1997). Prevention of stress-induced morphological and cognitive consequences. Eur Neuropsychopharmacol 7(Suppl 3): S323-S328.
53. McGaugh JL, Roozendaal B (2002). Role of adrenal stress hormones in forming lasting memories in the brain. Curr Opin Neurobiol 12: 205-210.
54. McGaughy J, Ross RS, Eichenbaum H (2008). Noradrenergic, but not cholinergic, deafferentation of prefrontal cortex impairs attentional set-shifting. Neuroscience 153: 63-71.
55. Merkl A, Schubert F, Quante A, Luborzewski A, Brakemeier EL, Grimm S et al 2011). Abnormal cingulate and prefrontal cortical neurochemistry in major depression after electroconvulsive therapy. Biol Psychiatry 69: 772-779.
56. Merriam EP, Thase ME, Haas GL, Keshavan MS, Sweeney JA (1999). Prefrontal cortical dysfunction in depression determined by Wisconsin Card Sorting Test performance. Am J Psychiatry 156: 780-782.
57. Moghaddam B, Bolinao ML, Stein-Behrens B, Sapolsky R (1994). Glucocorticoids mediate the stress-induced extracellular accumulation of glutamate. Brain Res 655: 251-254.
58. Morilak DA, Barrera G, Echevarria DJ, Garcia AS, Hernandez A, Ma S et al (2005). Role of brain norepinephrine in the behavioral response to stress. Prog Neuropsychopharmacol Biol Psychiatry 29: 1214-1224.
59. Morilak DA, Frazer A (2004). Antidepressants and brain monoaminergic systems: a dimensional approach to understanding their behavioural effects in depression and anxiety disorders. Int J Neuropsychopharmacol 7: 193-218.
60. Murphy FC, Sahakian BJ, Rubinsztein JS, Michael A, Rogers RD, Robbins TW et al (1999). Emotional bias and inhibitory control processes in mania and depression. Psychol Med 29: 1307-1321.
61. Musazzi L, Racagni G, Popoli M 2011). Stress, glucocorticoids and glutamate release: effects of antidepressant drugs. Neurochem Int 59: 138-149.
62. Nakane H, Shimizu N, Hori T (1994). Stress-induced norepinephrine release in the rat prefrontal cortex measured by microdialysis. Am J Physiol 267(6 Pt 2): R1559-R1566.
63. Nomura S, Watanabe M, Ukei N, Nakazawa T (1981). Stress and beta-adrenergic receptor binding in the rat's brain. Brain Res 224: 199-203.
64. Nutt DJ (2002). The neuropharmacology of serotonin and noradrenaline in depression. Int Clin Psychopharmacol 17(Suppl 1): S1-12.
65. Pardon MC, Ma S, Morilak DA (2003). Chronic cold stress sensitizes brain noradrenergic reactivity and noradrenergic facilitation of the HPA stress response in Wistar Kyoto rats. Brain Res 971: 55-65.
66. Paxinos G, Watson C (1998). The Rat Brain in Stereotaxic Coordinates. 4th Edition Academic Press: San Diego.
67. Popoli M, Yan Z, McEwen BS, Sanacora G (2012). The stressed synapse: the impact of stress and glucocorticoids on glutamate transmission. Nat Rev Neurosci 13: 22-37.
68. Radley JJ, Sisti HM, Hao J, Rocher AB, McCall T, Hof PR et al (2004). Chronic behavioral stress induces apical dendritic reorganization in pyramidal neurons of the medial prefrontal cortex. Neuroscience 125: 1-6.
69. Radley JJ, Williams B, Sawchenko PE (2008). Noradrenergic innervation of the dorsal medial prefrontal cortex modulates hypothalamo-pituitary-adrenal responses to acute emotional stress. J Neurosci 28: 5806-5816.
70. Raskind MA, Peskind ER, Hoff DJ, Hart KL, Holmes HA, Warren D et al (2007). A parallel group placebo controlled study of prazosin for trauma nightmares and sleep disturbance in combat veterans with post-traumatic stress disorder. Biol Psychiatry 61: 928-934.
71. Ressler KJ, Nemeroff CB (2000). Role of serotonergic and noradrenergic systems in the pathophysiology of depression and anxiety disorders. Depress Anxiety 12(Suppl 1): 2-19.
72. Roozendaal B, Schelling G, McGaugh JL (2008). Corticotropinreleasing factor in the basolateral amygdala enhances memory consolidation via an interaction with the beta-adrenoceptorcAMP pathway: dependence on glucocorticoid receptor activation. J Neurosci 28: 6642-6651.
73. Sara SJ, Vankov A, Herve A (1994). Locus coeruleus-evoked responses in behaving rats: a clue to the role of noradrenaline in memory. Brain Res Bull 35: 457-465.
74. Siegle GJ, Thompson W, Carter CS, Steinhauer SR, Thase ME (2007). Increased amygdala and decreased dorsolateral prefrontal BOLD responses in unipolar depression: related and independent features. Biol Psychiatry 61: 198-209.
75. Skaper SD, Facci L, Strijbos PJ (2001). Neuronal protein kinase signaling cascades and excitotoxic cell death. Ann NY Acad Sci 939: 11-22.
76. Stuss DT, Levine B, Alexander MP, Hong J, Palumbo C, Hamer L et al (2000). Wisconsin Card Sorting Test performance in patients with focal frontal and posterior brain damage: effects of lesion location and test structure on separable cognitive processes. Neuropsychologia 38: 388-402.
77. Tait DS, Brown VJ, Farovik A, Theobald DE, Dalley JW, Robbins TW (2007). Lesions of the dorsal noradrenergic bundle impair attentional set-shifting in the rat. Eur J Neurosci 25: 3719-3724.
78. Venero C, Borrell J (1999). Rapid glucocorticoid effects on excitatory amino acid levels in the hippocampus: a microdialysis study in freely moving rats. Eur J Neurosci 11: 2465-2473.
79. Waterhouse BD, Moises HC, Woodward DJ (1981). Alphareceptor-mediated facilitation of somatosensory cortical neuronal responses to excitatory synaptic inputs and iontophoretically applied acetylcholine. Neuropharmacology 20: 907-920.
80. Waterhouse BD, Mouradian R, Sessler FM, Lin RC (2000). Differential modulatory effects of norepinephrine on synaptically driven responses of layer V barrel field cortical neurons. Brain Res 868: 39-47.
81. Wellman CL (2001). Dendritic reorganization in pyramidal neurons in medial prefrontal cortex after chronic corticosterone administration. J Neurobiol 49: 245-253.
82. Woodward DJ, Moises HC, Waterhouse BD, Yeh HH, Cheun JE (1991). Modulatory actions of norepinephrine on neural circuits. Adv Exp Med Biol 287: 193-208.
83. Woolley CS, Gould E, McEwen BS (1990). Exposure to excess glucocorticoids alters dendritic morphology of adult hippocampal pyramidal neurons. Brain Res 531: 225-231.
84. Yuen EY, Liu W, Karatsoreos IN, Feng J, McEwen BS, Yan Z (2009). Acute stress enhances glutamatergic transmission in prefrontal cortex and facilitates working memory. Proc Natl Acad Sci USA 106: 14075-14079.
85. Yuen EY, Liu W, Karatsoreos IN, Ren Y, Feng J, McEwen BS et al 2011). Mechanisms for acute stress-induced enhancement of glutamatergic transmission and working memory. Mol Psychiatry 16: 156-170.