Stress prompts habit behavior in humans

Journal of Neuroscience

Volumn 29, Issue 22, 2009, Pages 7191-7198

  Schwabe, Lars ^a   Wolf, Oliver T ^a  

^a RUHR UNIVERSITY BOCHUM   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; ARTICLE; BLOOD SAMPLING; CONTROLLED STUDY; FEMALE; FOOD; GOAL ATTAINMENT; HABIT; HUMAN; HUMAN TISSUE; LEARNING; MALE; MENTAL CAPACITY; NORMAL HUMAN; PRIORITY JOURNAL; REINFORCEMENT; SATIETY; STRESS; TASK PERFORMANCE;

ANALYSIS OF VARIANCE; BLOOD PRESSURE; CONDITIONING, OPERANT; EMOTIONS; EXTINCTION, PSYCHOLOGICAL; FEMALE; GOALS; HABITS; HUMANS; HYDROCORTISONE; MALE; PROBABILITY; PSYCHOMOTOR PERFORMANCE; REINFORCEMENT (PSYCHOLOGY); SALIVA; SATIATION; STRESS, PSYCHOLOGICAL; YOUNG ADULT;

EID: 66749101239     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0979-09.2009     Document Type: Article

References (59)

1. Adams C (1982) Variations in the sensitivity of instrumental responding to reinforcer devaluation. Q J Exp Psychol 34B:77-98.
2. Balleine BW, Dickinson A (1991) Instrumental performance following reinforcer devaluation depends upon incentive learning. Q J Exp Psychol 43:279-296.
3. Balleine BW, Dickinson A (1998) The role of incentive learning in instrumental outcome revaluation by sensory-specific satiety. Anim Learn Behav 26:46-59. (Pubitemid 28124631)
4. Balleine BW, Killcross S (2006) Parallel incentive processing: an integrated view of amygdala function. Trends Neurosci 29:272-279.
5. Balleine BW, Killcross AS, Dickinson A (2003) The effect of lesions of the basolateral amygdala on instrumental conditioning. J Neurosci 23:666-675. (Pubitemid 36139565)
6. Barrett D, Gonzalez-Lima F (2004) Behavioral effects of metyrapone on pavlovian extinction. Neurosci Lett 371:91-96. (Pubitemid 39440751)
7. Bayley PJ, Frascino JC, Squire LR (2005) Robust habit learning in the absence of awareness and independent of the medial temporal lobe. Nature 436:550-553. (Pubitemid 41112927)
8. Berke JD, Hyman SE (2000) Addiction, dopamine, and the molecular mechanisms of memory. Neuron 25:515-532.
9. Blundell P, Hall G, Killcross S (2001) Lesions of the basolateral amygdala disrupt selective aspects of reinforcer representation in rats. J Neurosci 21:9018-9026. (Pubitemid 33054863)
10. Brennan AR, Arnsten AF (2008) Neuronal mechanisms underlying attention deficit hyperactivity disorder: the influence of arousal on prefrontal cortical function. Ann N Y Acad Sci 1129:236-245.
11. Brinks V, de Kloet ER, Oitzl MS (2009) Corticosterone facilitates extinction of fear memory in BALB/c mice but strengthens cue related fear in C57BL/6 mice. Exp Neurol 216:375-382.
12. Buchanan TW, Tranel D, Adolphs R (2006) Impaired memory retrieval correlates with individual differences in cortisol response but not autonomic response. Learn Mem 13:382-387. (Pubitemid 43830686)
13. Cerqueira JJ, Mailliet F, Almeida OF, Jay TM, Sousa N (2007) The prefrontal cortex as a key target of the maladaptive response to stress. J Neurosci 27:2781-2787. (Pubitemid 46438976)
14. Colwill RM, Rescorla RA (1985) Postconditioning devaluation of a reinforcer affects instrumental responding. J Exp Psychol Anim Behav Process 11:120-132.
15. Corbit LH, Balleine BW (2003) The role of prelimbic cortex in instrumental conditioning. Behav Brain Res 146:145-157. (Pubitemid 37476141)
16. 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. (Pubitemid 37115047)
17. Dalley JW, Cardinal RN, Robbins TW (2004) Prefrontal executive and cognitive functions in rodents: neural and neurochemical substrates. Neurosci Biobehav Rev 28:771-784. (Pubitemid 39535871)
18. 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 Plasticity 2007:60803. (Pubitemid 46629680)
19. Dickinson A (1985) Actions and habits: the development of behavioral autonomy. Philos Trans R Soc Lond B Biol Sci 308:67-78.
20. Dickinson A, Balleine BW, Watt A, Gonzalez F, Boakes RA (1995) Motivational control after extended instrumental training. Anim Learn Behav 23:197-206.
21. Everitt BJ, Robbins TW (2005) Neural systems of reinforcement for drug addiction: from actions to habits to compulsion. Nat Neurosci 8:1481-1489. (Pubitemid 41573659)
22. Everitt BJ, Dickinson A, Robbins TW (2001) The neuropsychological basis of addictive behaviour. Brain Res Brain Res Rev 36:129-138. (Pubitemid 33020742)
23. Fallon JL, Ciofi P (1992) Distribution of monoamines within the amygdala. In: The amygdala: neurobiological aspects of emotion, memory, and mental dysfunction (Aggleton J, ed), pp 94-114. New York: Wiley.
24. Goldstein LE, Rasmusson AM, Bunney BS, Roth RH (1996) Role of the amygdala in the coordination of behavioral, neuroendocrine, and prefrontal cortical monoamine responses to psychological stress in the rat. J Neurosci 16:4787-4798. (Pubitemid 26251073)
25. Hatfield T, Han JS, Conley M, Gallagher M, Holland P (1996) Neurotoxic lesions of basolateral, but not central, amygdala interfere with Pavlovian second-order conditioning and reinforcer devaluation effects. J Neurosci 16:5256-5265. (Pubitemid 26269683)
26. Hull CL (1943) Principles of behavior. New York: Appleton-Century-Crofts.
27. Killcross S, Coutureau E (2003) Coordination of actions and habits in the medial prefrontal cortex of rats. Cereb Cortex 13:400-408. (Pubitemid 36373685)
28. 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. (Pubitemid 32622947)
29. Kirschbaum C, Kudielka BM, Gaab J, Schommer NC, Hellhammer DH (1999) Impact of gender, menstrual cycle phase, and oral contraceptives on the activity of the hypothalamus-pituitary-adrenal axis. Psychosom Med 61:154-162. (Pubitemid 29168644)
30. Knowlton BJ, Mangels JA, Squire LR (1996) A neostriatal habit learning system in humans. Science 273:1399-1402. (Pubitemid 26296530)
31. Lupien SJ, Gillin CJ, Hauger RL (1999) Working memory is more sensitive than declarative memory to the acute effects of corticosteroids: a doseresponse study in humans. Behav Neurosci 113:420-430. (Pubitemid 29340055)
32. Lupien SJ, Maheu F, Tu M, Fiocco A, Schramek TE (2007) The effects of stress and stress hormones on human cognition: implications for the field of brain and cognition. Brain Cogn 65:209-237. (Pubitemid 350051538)
33. Maroun M, Richter-Levin G (2003) Exposure to acute stress blocks the induction of long-term potentiation of the amygdala-prefrontal cortex pathway in vivo. J Neurosci 23:4406-4409. (Pubitemid 36706170)
34. Matsumoto K, Tanaka K (2004) The role of the medial prefrontal cortex in achieving goals. Curr Opin Neurobiol 14:178-185. (Pubitemid 38479934)
35. McEwen BS, De Kloet ER, RosteneW (1986) Adrenal steroid receptors and actions in the nervous system. Physiol Rev 66:1121-1188. (Pubitemid 17181300)
36. McGaugh JL (2002) Memory consolidation and amygdala: a systems perspective. Trends Neurosci 25:456-461. (Pubitemid 35222999)
37. Mendelson JH, Sholar MB, Goletiani N, Siegel AJ, Mello NK (2005) Effects of low- and high-nicotine cigarette smoking on mood states and the HPA axis in men. Neuropsychopharmacology 30:1751-1763. (Pubitemid 43086032)
38. Nelson A, Killcross S (2006) Amphetamine exposure enhances habit formation. J Neurosci 26:3805-3812.
39. Packard MG, Wingard JC (2004) Amygdala and "emotional" modulation of the relative use of multiple memory systems. Neurobiol Learn Mem 82:243-252. (Pubitemid 39298719)
40. Payne JD, Jackson ED, Hoscheidt S, Ryan L, Jacobs WJ, Nadel L (2007) Stress administered prior to encoding impairs neutral but enhances emotional long-term memories. Learn Mem 14:861-868.
41. Reul JM, de Kloet ER (1985) Two receptor systems for corticosterone in rat brain: microdistribution and differential occupation. Endocrinology 117:2505-2511. (Pubitemid 16194083)
42. Robinson TE, Kolb B (2004) Structural plasticity associated with exposure to drugs of abuse. Neuropsychopharmacology 47 [Suppl 1]:33-46.
43. 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. (Pubitemid 38222989)
44. Roozendaal B, Barsegyan A, Lee S (2008) Adrenal stress hormones, amygdala activation, and memory for emotionally arousing experiences. In: Progress in brain research (de Kloet ER, Oitzl MS, Vermetten E, eds). Amsterdam: Elsevier. (Pubitemid 350123226)
45. Rose J, Otto T, Dittrich L (2008) The biopsychology-toolbox: a free, opensource Matlab-toolbox for the control of behavioral experiments. J Neurosci Methods 175:104-107.
46. Schoofs D, Preuss D, Wolf OT (2008) Psychosocial stress induces working memory impairments in an n-back paradigm. Psychoneuroendocrinology 33:643-653.
47. Schwabe L, Oitzl MS, Philippsen C, Richter S, Bohringer A, Wippich W, Schachinger H (2007) Stress modulates the use of spatial and stimulus-response learning strategies in humans. Learn Mem 14:109-116. (Pubitemid 46203573)
48. Schwabe L, Dalm S, Schächinger H, Oitzl MS (2008a) Chronic stress modulates the use of spatial and stimulus-response learning strategies in mice and man. Neurobiol Learn Mem 90:495-503.
49. Schwabe L, Haddad L, Schachinger H (2008b) HPA axis activation by a socially evaluated cold pressor test. Psychoneuroendocrinology 33:890-895.
50. Schwabe L, Oitzl MS, Richter S, Schächinger H (2009a) Modulation of spatial and stimulus-response learning strategies by exogenous cortisol in healthy young women. Psychoneuroendocrinolgy 34:358-366.
51. Schwabe L, Schächinger H, de Kloet ER, Oitzl MS (2009b) Corticosteroids operate as switch between memory systems. J Cogn Neurosci. Advance online publication. Retrieved May 19, 2009. doi: 10.1162/jocn.2009. 21278.
52. Shepard JD, Barron KW, Myers DA (2000) Corticosterone delivery to the amygdala increases corticotropin-releasing factor mRNA in the central amygdaloid nucleus and anxiety-like behavior. Brain Res 861:288-295. (Pubitemid 30173314)
53. Smith AD, Bolam JP (1990) The neural network of the basal ganglia as revealed by the study of synaptic connections of identified neurons. Trends Neurosci 13:259-265. (Pubitemid 20193455)
54. 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. (Pubitemid 46597159)
55. van Stegeren AH, Wolf OT, Everaerd W, Scheltens P, Barkhof F, Rombouts SA (2007) Endogenous cortisol level interacts with noradrenergic activation in the human amygdala. Neurobiol Learn Mem 87:57-66. (Pubitemid 44755270)
56. Wolf OT (2008) The influence of stress hormones on emotional memory: relevance for psychopathology. Acta Psychol (Amst) 127:513-531.
57. Yang YL, Chao PK, Lu KT (2006) Systemic and intra-amygdala administration of glucocorticoid agonist and antagonist modulate extinction of conditioned fear. Neuropsychopharmacology 31:912-924.
58. Yin HH, Knowlton BJ, Balleine BW (2004) Lesions of dorsolateral striatum preserve outcome expectancy but disrupt habit formation in instrumental learning. Eur J Neurosci 19:181-189. (Pubitemid 38122084)
59. Yin HH, Ostlund SB, Knowlton BJ, Balleine BW (2005) The role of the dorsomedial striatum in instrumental conditioning. Eur J Neurosci 22:513-523. (Pubitemid 41097624)