Simultaneous glucocorticoid and noradrenergic activity disrupts the neural basis of goal-directed action in the human brain

Journal of Neuroscience

Volumn 32, Issue 30, 2012, Pages 10146-10155

  Schwabe, Lars ^a   Tegenthoff, Martin ^b   Höffken, Oliver ^b   Wolf, Oliver T ^a  

^a RUHR UNIVERSITY BOCHUM   (Germany)

^b RUHR UNIVERSITY BOCHUM   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

GLUCOCORTICOID; HYDROCORTISONE; YOHIMBINE;

ADULT; ARTICLE; FEMALE; FOOD; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; HUMAN EXPERIMENT; INSTRUMENTAL CONDITIONING; LEARNING TEST; MALE; NORADRENERGIC NERVE; NORMAL HUMAN; ORBITAL CORTEX; PREFRONTAL CORTEX; PRIORITY JOURNAL; REINFORCEMENT; REWARD; TRAINING;

ADOLESCENT; ADRENERGIC ALPHA-2 RECEPTOR ANTAGONISTS; ADULT; BRAIN; BRAIN MAPPING; CONDITIONING, OPERANT; CROSS-OVER STUDIES; EXTINCTION, PSYCHOLOGICAL; FEMALE; GLUCOCORTICOIDS; GOALS; HUMANS; HYDROCORTISONE; MAGNETIC RESONANCE IMAGING; MALE; REWARD; YOHIMBINE;

EID: 84864258460     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1304-12.2012     Document Type: Article

References (49)

1. Adams CD (1982) Variations in the sensitivity of instrumental responding to reinforcer devaluation. Q J Exp Psychol 34:77-98.
2. Arnsten AF (2009) Stress signaling pathways that impair prefrontal cortex structure and function. Nat Rev Neurosci 10:410-422.
3. Balleine BW, Dickinson A (1998a) The role of incentive learning in instrumental outcome revaluation by sensory-specific satiety. Anim Learn Behav 26:46-59.
4. Balleine BW, Dickinson A (1998b) Goal-directed instrumental action: contingency and incentive learning and their cortical substrates. Neuropharmacology 37:407-419.
5. Balleine BW, O'Doherty JP (2010) Human and rodent homologiesin action control: corticostriatal determinantsof goal-directed and habitual action. Neuropsychopharmacology 35:48-69.
6. Charney DS, Heninger GR, Breier A (1984) Noradrenergic function in panic axiety: effects of yohimbine in healthy subjects and patients with agoraphobia and panic disorder. Arch Gen Psychiatry 41:751-763.
7. Chatterton RT Jr, Vogelsong KM, Lu YC, Ellman AB, Hudgens GA (1996) Salivary alpha-amylase as a measure of endogenous adrenergic activity. Clin Physiol 16:433-448.
8. Corbit LH, Muir JL, Balleine BW (2003) Lesions of mediodorsal thalamus and anterior thalamic nuclei produce dissociable effects on instrumental conditioning in rats. Eur J Neurosci 18:1286-1294.
9. Daw ND, Niv Y, Dayan P (2005) Uncertainty-based competition between prefrontal and dorsolateral striatal systems for behavioral control. Nat Neurosci 8:1704-1711.
10. Diamond DM, Campbell AM, Park CR, Halonen J, Zoladz PR (2007) The temporal dynamics model of emotional memory processing: a synthesis on the neurobiological basis of stress-induced amnesia, flashbulb and traumatic memories, and the Yerkes-Dodson law. Neural Plast 2007:60803.
11. Dias-Ferreira E, Sousa JC, Melo I, Morgado P, Mesquita AR, Cerqueira JJ, Costa RM, Sousa N (2009) Chronic stress causes frontostriatal reorganization and affects decision-making. Science 325:621-625.
12. Dickinson A (1985) Actions and habits: the development of behavioral autonomy. Philos Trans R Soc Lond B Biol Sci 308:67-78.
13. Dickinson A, Balleine BW (1994) Motivational control of goal-directed action. Anim Learn Behav 22:1-18.
14. Everitt BJ, Robbins TW (2005) Neural systems of reinforcement for drug addiction: from actions to habits to compulsion. Nat Neurosci 8:1481-1489.
15. Gottfried JA, O'Doherty J, Dolan RJ (2003) Encoding predictive reward value in human amygdala and orbitofrontal cortex. Science 301:1104-1107.
16. Granger DA, Kivlighan KT, el-Sheikh M, Gordis EB, Stroud LR (2007) Salivary alpha-amylase in biobehavioral research: recent developments and applications. Ann N Y Acad Sci 1098:122-144.
17. Killcross S, Coutureau E (2003) Coordination of actions and habits in the medial prefrontal cortex of rats. Cereb Cortex 13:400-408.
18. Kim JJ, Lee HJ, Han JS, Packard MG (2001) Amygdala is critical for stress-induced modulation of hippocampal long-term potentiation and learning. J Neurosci 21:5222-5228.
19. Knowlton BJ, Mangels JA, Squire LR (1996) A neostriatal habit learning system in humans. Science 273:1399-1402.
20. Lyons DM, Lopez JM, Yang C, Schatzberg AF (2000) Stress-level cortisol treatment impairs inhibitory control over behavior in monkeys. J Neuro-sci 20:7816-7821.
21. Morgan CA 3rd, Southwick SM, Grillon C, Davis M, Krystal JH, Charney DS (1993) Yohimibine-facilitated acoustic startle reflex in humans. Psycho-pharmacology 110:342-346.
22. Nater UM, Rohleder N (2009) Salivary alpha-amylaseasa non-invasive bio-marker for the sympathetic nervous system: current state of research. Psychoneuroendocrinology 34:486-496.
23. Ostlund SB, Balleine BW (2005) Lesions of the medial prefrontal cortex disrupt the acquisition but not the expression of goal-directed learning. J Neurosci 25:7763-7770.
24. Patel PD, Lopez JF, Lyons DM, Burke S, Wallace M, Schatzberg AF (2000) Glucocorticoid and mineralocorticoid receptor mRNA expression in squirrel monkey brain. J Psychiatr Res 34:383-392.
25. Piazza PV, Le Moal M (1998) The role of stress in drug self-administration. Trends Pharmacol Sci 19:67-74.
26. Robbins TW, Everitt BJ (1999) Drug addiction: bad habits add up. Nature 398:567-570.
27. Roozendaal B, McReynolds JR, McGaugh JL (2004) The basolateral amygdala interacts with the medial prefrontal cortex in regulating glucocorticoid effects on working memory impairment. J Neurosci 24:1385-1392.
28. Roozendaal B, Okuda S, Van der Zee EA, McGaugh JL (2006a) Gluco-corticoid enhancement of memory requires arousal-induced norad-renergic activation in the basolateral amygdala. Proc Natl Acad Sci U S A 103:6741-6746.
29. Roozendaal B, Okuda S, de Quervain DJ, McGaugh JL (2006b) Glucocorti-coids interact with emotion-induced noradrenergic activation in influencing different memory functions. Neuroscience 138:901-910.
30. Rosmond R, Dallman MF, Björntorp P (1998) Stress-related cortisol secretion in men: relationship with abdominal obesity and endocrine, metabolic and hemodynamic abnormalities. J Clin Endocrinol Metab 83:1853-1859.
31. Schoenbaum G, Setlow B, Saddoris MP, Gallagher M (2003) Encoding predicted outcome and acquired value in orbitofrontal cortex during cue sampling depends upon input from basolateral amygdala. Neuron 39:855-867.
32. Scholz U, La Marca R, Nater UM, Aberle I, Ehlert U, Hornung R, Martin M, KliegelM (2009) Gono-go performance under psychosocial stress: beneficial effects of implementation intentions. Neurobiol Learn Mem 91:89-92.
33. Schwabe L, Wolf OT (2009) Stress prompts habit behavior in humans. J Neurosci 29:7191-7198.
34. Schwabe L, Wolf OT (2010) Socially evaluated cold pressor stress after instrumental learning favors habits over goal-directed action. Psychoneu-roendocrinology 35:977-986.
35. Schwabe L, Wolf OT (2011) Stress-induced modulation ofinstrumental behavior: from goal-directed to habitual control of action. Behav Brain Res 219:321-328.
36. Schwabe L, Wolf OT (2012) Stress modulates the engagement of multiple memory systems in classification learning. J Neurosci. In press.
37. Schwabe L, Oitzl MS, Philippsen C, Böhringer A, Richter S, Wippich W, Schächinger H (2007) Stress modulates the use of spatial and stimulus-response learning strategies in humans. Learn Mem 14:109-116.
38. Schwabe L, Wolf OT, Oitzl MS (2010a) Memory formation under stress: quantity and quality. Neurosci Biobehav Rev 34:584-591.
39. Schwabe L, Tegenthoff M, Höffken O, Wolf OT (2010b) Concurrent gluco-corticoid and noradrenergic activity shifts instrumental behavior from goal-directed to habitual control. J Neurosci 30:8190-8196.
40. Schwabe L, Schächinger H, de Kloet ER, Oitzl MS (2010c) Corticoste-roids operate as switch between memory systems. J Cogn Neurosci 22:1362-1372.
41. Schwabe L, Höffken O, Tegenthoff M, Wolf OT (2011) Preventing the stress-induced shift from goal-directed to habit action with a beta-adrenergic antagonist. J Neurosci 31:17317-17325.
42. Sinha R (2007) The role of stress in addiction relapse. Curr Psychiatr Rep 9:388-395.
43. Steyer R, Schwenkmezger P, Notz P, Eid M (1994) Testtheoretische Anal-ysen des Mehrdimensionalen Befindlichkeitsfragebogens (MDBF). Diag-nostica 40:320-328.
44. Thorpe SJ, Rolls ET, Maddison S (1983) The orbitofrontal cortex: neuronal activity in the behaving monkey. Exp Brain Res 49:93-115.
45. Tricomi E, Balleine BW, O'Doherty JP (2009) A specific role for posterior dorsolateral striatum in human habit learning. Eur J Neurosci 29:2225-2232.
46. Valentin VV, Dickinson A, O'Doherty JP (2007) Determining the neural substrates of goal-directed learning in the human brain. J Neurosci 27:4019-4026.
47. Westermann J, Demir A, Herbst V (2004) Determination of cortisol in saliva and serum by a luminescence-enhanced enzyme immunoassay. Clin Lab 50:11-24.
48. Yin HH, Knowlton BJ, Balleine BW (2004) Lesions of dorsolateral striatum preserve outcome expectancy but disrupt habit formationin instrumental learning. Eur J Neurosci 19:181-189.
49. Yin HH, Ostlund SB, Knowlton BJ, Balleine BW (2005) The role of the dorsomedial striatum in instrumental conditioning. Eur J Neurosci 22: 513-523.