Chronic stress modulates neural and cardiovascular responses during reversal learning

Neuroscience

Volumn 193, Issue , 2011, Pages 193-204

  Ohira, H ^a   Matsunaga, M ^b   Kimura, K ^a,c   Murakami, H ^a,d   Osumi, T ^a,e   Isowa, T ^f   Fukuyama, S ^g,h   Shinoda, J ^g   Yamada, J ^g  

^a NAGOYA UNIVERSITY   (Japan)

^b NATIONAL INSTITUTE FOR PHYSIOLOGICAL SCIENCES   (Japan)

^c KWANSEI GAKUIN UNIVERSITY   (Japan)

^d STONY BROOK UNIVERSITY   (United States)

^e KEIO UNIVERSITY   (Japan)

^f MIE UNIVERSITY   (Japan)

^g Kizawa Memorial Hospital   (Japan)

^h KANAGAWA DENTAL COLLEGE   (Japan)

Author keywords

Cardiovascular response; Chronic job stress; Positron emission tomography (PET); Reversal learning

Indexed keywords

ADULT; ARTICLE; BEHAVIOR; BLOOD PRESSURE; BRAIN BLOOD FLOW; BRAIN FUNCTION; CARDIOVASCULAR PARAMETERS; CHRONIC STRESS; COGNITION; CONTROLLED STUDY; HEART FUNCTION; HEART RATE; HUMAN; HUMAN EXPERIMENT; INSULA; JOB STRESS; LEARNING; MALE; MESENCEPHALON; NORMAL HUMAN; ORBITAL CORTEX; POSITRON EMISSION TOMOGRAPHY; PREFRONTAL CORTEX; PRIORITY JOURNAL; SELF REPORT; STATISTICS; TASK PERFORMANCE;

ADULT; ANALYSIS OF VARIANCE; BLOOD PRESSURE; BRAIN; BRAIN MAPPING; CARDIOVASCULAR PHYSIOLOGICAL PHENOMENA; CEREBROVASCULAR CIRCULATION; CHRONIC DISEASE; HEART RATE; HUMANS; MALE; POSITRON-EMISSION TOMOGRAPHY; REVERSAL LEARNING; SELF REPORT; STATISTICS AS TOPIC; STRESS, PSYCHOLOGICAL; TIME FACTORS;

EID: 80052508355     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2011.07.014     Document Type: Article

References (86)

1. Aron A.R., Robbins T.W., Poldrack R.A. Inhibition and the right inferior frontal cortex. Trends Cogn Sci 2004, 8:170-177.
2. Balleine B.W., Dickinson A. Goal-directed instrumental action: contingency and incentive learning and their cortical substrates. Neuropharmacology 1998, 37:407-419.
3. Balleine B.W., O'Doherty J.P. Human and rodent homologies in action control: corticostriatal determinants of goal-directed and habitual action. Neuropsychopharmacology 2010, 35:48-69.
4. Beauchaine T.P., Gatzke-Kopp L., Mead H.K. Polyvagal theory and developmental psychopathology: emotion dysregulation and conduct problems from preschool to adolescence. Biol Psychol 2007, 74:174-184.
5. Bellebaum C., Koch B., Schwarz M., Daum I. Focal basal ganglia lesions are associated with impairments in reward-based reversal learning. Brain 2008, 131:829-841.
6. Cerqueira J.J., Mailliet F., Almeida O.F., Jay T.M., Sousa N. The prefrontal cortex as a key target of the maladaptive response to stress. J Neurosci 2007, 27:2781-2787.
7. Cools R., Clark L., Owen A.M., Robbins T.W. Defining the neural mechanisms of probabilistic reversal learning using event-related functional magnetic resonance imaging. J Neurosci 2002, 22:4563-4567.
8. Critchley H.D., Corfield D.R., Chandler M.P., Mathias C.J., Dolan R.J. Cerebral correlates of autonomic cardiovascular arousal: a functional neuroimaging investigation in humans. J Physiol 2000, 523:259-270.
9. De Mey C., Schroeter V., Butzer R., Roll S., Belz G.G. Method specificity of non-invasive blood pressure measurement: oscillometry and finger pulse pressure vs acoustic methods. Br J Clin Pharmacol 1995, 40:291-297.
10. Dias-Ferreira E., Sousa J.C., Melo I., Morgado P., Mesquita A.R., Cerqueira J.J., Costa R.M., Sousa N. Chronic stress causes frontostriatal reorganization and affects decision-making. Science 2009, 325:621-625.
11. Elovainio M., Ferrie J.E., Singh-Manoux A., Gimeno D., De Vogli R., Shipley M.J., Vahtera J., Brunner E.J., Marmot M.G., Kivimäki M. Cumulative exposure to high-strain and active jobs as predictors of cognitive function: the Whitehall II study. Occup Environ Med 2009, 66:32-37.
12. Endo N., Saiki J., Saito H. Determinants of occurrence of negative priming for novel shapes with matching paradigm. Jpn J Psychol 2001, 72:204-212. In Japanese.
13. Freyer T., Valerius G., Kuelz A.K., Speck O., Glauche V., Hull M., Voderholzer U. Test-retest reliability of event-related functional MRI in a probabilistic reversal learning task. Psychiatry Res 2009, 174:40-46.
14. Friston K.J., Holmes A.P., Worsley K.J., Poline J.B., Frith C.D., Frackowiak R.S.J. SPMs in functional imaging: a general linear approach. Hum Brain Mapp 1995, 1:214-220.
15. Ghahremani D.G., Monterosso J., Jentsch J.D., Bilder R.M., Poldrack R.A. Neural components underlying behavioral flexibility in human reversal learning. Cereb Cortex 2010, 20:1843-1852.
16. Gianaros P.J., Derbyshire S.W., May J.C., Siegle G.J., Gamalo M.A., Jennings J.R. Anterior cingulate activity correlates with blood pressure during stress. Psychophysiology 2005, 42:627-635.
17. Gianaros P.J., Jennings J.R., Sheu L.K., Derbyshire S.W., Matthews K.A. Heightened functional neural activation to psychological stress covaries with exaggerated blood pressure reactivity. Hypertension 2007, 49:134-140.
18. Gianaros P.J., Sheu L.K. A review of neuroimaging studies of stressor-evoked blood pressure reactivity: emerging evidence for a brain-body pathway to coronary heart disease risk. Neuroimage 2009, 47:922-936.
19. Gianaros P.J., Sheu L.K., Matthews K.A., Jennings J.R., Manuck S.B., Hariri A.R. Individual differences in stressor-evoked blood pressure reactivity vary with activation, volume, and functional connectivity of the amygdala. J Neurosci 2008, 28:990-999.
20. Gianaros P.J., Van Der Veen F.M., Jennings J.R. Regional cerebral blood flow correlates with heart period and high-frequency heart period variability during working-memory tasks: implications for the cortical and subcortical regulation of cardiac autonomic activity. Psychophysiology 2004, 41:521-530.
21. Groen Y., Wijers A.A., Mulder L.J., Minderaa R.B., Althaus M. Physiological correlates of learning by performance feedback in children: a study of EEG event-related potentials and evoked heart rate. Biol Psychol 2007, 76:174-187.
22. Haruno M., Kawato M. Heterarchical reinforcement-learning model for integration of multiple cortico-striatal loops: fMRI examination in stimulus-action-reward association learning. Neural Netw 2006, 19:1242-1254.
23. Haruno M., Kawato M. Different neural correlates of reward expectation and reward expectation error in the putamen and caudate nucleus during stimulus-action-reward association learning. J Neurophysiol 2006, 95:948-959.
24. Hejjel L., Roth E. What is the adequate sampling interval of the ECG signal for heart rate variability analysis in the time domain?. Physiol Meas 2004, 25:1405-1411.
25. Holman D.J., Wall T.D. Work characteristics, learning-related outcomes, and strain: a test of competing direct effects, mediated, and moderated models. J Occup Health Psychol 2002, 7:283-301.
26. Hooftman W.E., van Poppel M.N., van der Beek A.J., Bongers P.M., van Mechelen W. Gender differences in the relations between work-related physical and psychosocial risk factors and musculoskeletal complaints. Scand J Work Environ Health 2004, 30:261-728.
27. ISCO-88 international standard classification of occupations 1990, International Labour Office, Geneva.
28. Jennings J.R., van der Molen M.W. Cardiac timing and the central regulation of action. Psychol Res 2002, 66:337-349.
29. Jocham G., Klein T.A., Neumann J., von Cramon D.Y., Reuter M., Ullsperger M. Dopamine DRD2 polymorphism alters reversal learning and associated neural activity. J Neurosci 2009, 29:3695-3704.
30. Karasek R.A. Job demands, job decision latitude, and mental strain: implications for job redesign. Adm Sci Q 1979, 24:285.
31. Karasek R., Brisson C., Kawakami N., Houtman I., Bongers P., Amick B. The Job Content Questionnaire (JCQ): an instrument for internationally comparative assessments of psychosocial job characteristics. J Occup Health Psychol 1998, 3:322-355.
32. Karasek R., Theorell T. Heathy work: stress, productivity, and the reconstruction of working life 1990, Basic Books, Oxford.
33. Kasprowicz M., Schmidt E., Kim D.J., Haubrich C., Czosnyka Z., Smielewski P., Czosnyka M. Evaluation of the cerebrovascular pressure reactivity index using non-invasive finapres arterial blood pressure. Physiol Meas 2010, 31:1217-1228.
34. Kawakami N., Fujigaki Y. Reliability and validity of the Japanese version of Job Content Questionnaire: replication and extension in computer company employees. Ind Health 1996, 34:295-306.
35. Kawakami N., Haratani T., Kobayashi F., Ishizaki M., Hayashi T., Fujita O., Aizawa Y., Miyazaki S., Hiro H., Masumoto T., Hashimoto S., Araki S. Occupational class and exposure to job stressors among employed men and women in Japan. J Epidemiol 2004, 14:204-211.
36. Kehagia A.A., Murray G.K., Robbins T.W. Learning and cognitive flexibility: frontostriatal function and monoaminergic modulation. Curr Opin Neurobiol 2010, 20:199-204.
37. Kimura K., Ohira H., Isowa T., Matsunaga M., Murashima S. Regulation of lymphocytes redistribution via autonomic nervous activity during stochastic learning. Brain Behav Immun 2007, 21:921-934.
38. Kittel F., Leynen F., Stam M., Dramaix M., de Smet P., Mak R., De Backer G., Kornitzer M. Job conditions and fibrinogen in 14226 Belgian workers: the Belstress study. Eur Heart J 2002, 23:1841-1848.
39. Kringelbach M.L. The human orbitofrontal cortex: linking reward to hedonic experience. Nat Rev Neurosci 2005, 6:691-702.
40. Kringelbach M.L., Rolls E.T. The functional neuroanatomy of the human orbitofrontal cortex: evidence from neuroimaging and neuropsychology. Prog Neurobiol 2004, 72:341-372.
41. Lane R.D., McRae K., Reiman E.M., Chen K., Ahern G.L., Thayer J.F. Neural correlates of heart rate variability during emotion. Neuroimage 2009, 44:213-222.
42. Liddle P.F., Kiehl K.A., Smith A.M. Event-related fMRI study of response inhibition. Hum Brain Mapp 2001, 12:100-109.
43. Lieberman M.D., Cunningham W.A. Type I and type II error concerns in fMRI research: re-balancing the scale. Soc Cogn Affect Neurosci 2009, 4:423-428.
44. Liston C., McEwen B.S., Casey B.J. Psychosocial stress reversibly disrupts prefrontal processing and attentional control. Proc Natl Acad Sci U S A 2009, 106:912-917.
45. Liston C., Miller M.M., Goldwater D.S., Radley J.J., Rocher A.B., Hof P.R., Morrison J.H., McEwen B.S. Stress-induced alterations in prefrontal cortical dendritic morphology predict selective impairments in perceptual attentional set-shifting. J Neurosci 2006, 26:7870-7874.
46. Lovallo W.R., Gerin W. Psychophysiological reactivity: mechanisms and pathways to cardiovascular disease. Psychosom Med 2003, 65:36-45.
47. Matsunaga M., Isowa T., Kimura K., Miyakoshi M., Kanayama N., Murakami H., Fukuyama S., Shinoda J., Yamada J., Konagaya T., Kaneko H., Ohira H. Association among positive mood, brain, and cardiovascular activities in an affectively positive situation. Brain Res 2009, 1263:93-103.
48. Matthews S.C., Paulus M.P., Simmons A.N., Nelesen R.A., Dimsdale J.E. Functional subdivisions within anterior cingulate cortex and their relationship to autonomic nervous system function. Neuroimage 2004, 22:1151-1156.
49. Menon V., Adleman N.E., White C.D., Glover G.H., Reiss A.L. Error-related brain activation during a Go/NoGo response inhibition task. Hum Brain Mapp 2001, 12:131-143.
50. Mizoguchi K., Yuzurihara M., Ishige A., Sasaki H., Chui D.H., Tabira T. Chronic stress induces impairment of spatial working memory because of prefrontal dopaminergic dysfunction. J Neurosci 2000, 20:1568-1574.
51. O'Callaghan C.J., Straznicky N.E., Komersova K., Louis W.J. Systematic errors in estimating mean blood pressure from finger blood pressure measurements. Blood Press 1998, 7:277-281.
52. O'Doherty J., Kringelbach M.L., Rolls E.T., Hornak J., Andrews C. Abstract reward and punishment representations in the human orbitofrontal cortex. Nat Neurosci 2001, 4:95-102.
53. O'Doherty J., Dayan P., Schultz J., Deichmann R., Friston K., Dolan R.J. Dissociable roles of ventral and dorsal striatum in instrumental conditioning. Science 2004, 304:452-454.
54. Ohira H., Fukuyama S., Kimura K., Nomura M., Isowa T., Ichikawa N., Matsunaga M., Shinoda J., Yamada J. Regulation of natural killer cell redistribution by prefrontal cortex during stochastic learning. Neuroimage 2009, 47:897-907.
55. Ohira H., Ichikawa N., Nomura M., Isowa T., Kimura K., Kanayama N., Fukuyama S., Shinoda J., Yamada J. Brain and autonomic association accompanying stochastic decision-making. Neuroimage 2010, 49:1024-1037.
56. Ohira H., Isowa T., Nomura M., Ichikawa N., Kimura K., Miyakoshi M., Iidaka T., Fukuyama S., Nakajima T., Yamada J. Imaging brain and immune association accompanying cognitive appraisal of an acute stressor. Neuroimage 2008, 39:500-514.
57. Pagnoni G., Zink C.F., Montague P.R., Berns G.S. Activity in human ventral striatum locked to errors of reward prediction. Nat Neurosci 2002, 5:97-98.
58. Pennartz C.M., Berke J.D., Graybiel A.M., Ito R., Lansink C.S., van der Meer M., Redish A.D., Smith K.S., Voorn P. Corticostriatal interactions during learning, memory processing, and decision making. J Neurosci 2009, 29:12831-12838.
59. Perini R., Milesi S., Fisher N.M., Pendergast D.R., Veicsteinas A. Heart rate variability during dynamic exercise in elderly males and females. Eur J Appl Physiol 2000, 82:8-15.
60. Pessiglione M., Petrovic P., Daunizeau J., Palminteri S., Dolan R.J., Frith C.D. Subliminal instrumental conditioning demonstrated in the human brain. Neuron 2008, 59:561-567.
61. Pessiglione M., Seymour B., Flandin G., Dolan R.J., Frith C.D. Dopamine-dependent prediction errors underpin reward-seeking behaviour in humans. Nature 2006, 442:1042-1045.
62. Phillips A.C., Carroll D., Ring C., Sweeting H., West P. Life events and acute cardiovascular reactions to mental stress: a cohort study. Psychosom Med 2005, 67:384-392.
63. Phillips A.C., Hunt K., Der G., Carroll D. Blunted cardiac reactions to acute psychological stress predict symptoms of depression five years later: evidence from a large community study. Psychophysiology 2011, 48:142-148.
64. Remijnse P.L., Nielen M.M., Uylings H.B., Veltman D.J. Neural correlates of a reversal learning task with an affectively neutral baseline: an event-related fMRI study. Neuroimage 2005, 26:609-618.
65. Remijnse P.L., Nielen M.M., van Balkom A.J., Cath D.C., van Oppen P., Uylings H.B., Veltman D.J. Reduced orbitofrontal-striatal activity on a reversal learning task in obsessive-compulsive disorder. Arch Gen Psychiatry 2006, 63:1225-1236.
66. Roberts A.C. Primate orbitofrontal cortex and adaptive behaviour. Trends Cogn Sci 2006, 10:83-90.
67. Sacker A., Bartley M.J., Frith D., Fitzpatrick R.M., Marmot M.G. The relationship between job strain and coronary heart disease: evidence from an English sample of the working male population. Psychol Med 2001, 31:279-290.
68. Saul J.P. Beat-to-beat variations of heart rate reflect modulation of cardiac autonomic outflow. News Physiol Sci 1990, 5:32-37.
69. Saul J.P., Rea R.F., Eckberg D.L., Berger R.D., Cohen R.J. Heart rate and muscle sympathetic nerve variability during reflex changes of autonomic activity. Am J Physiol 1990, 258:H713-H721.
70. Schnall P.L., Schwartz J.E., Landsbergis P.A., Warren K., Pickering T.G. Relation between job strain, alcohol, and ambulatory blood pressure. Hypertension 1992, 19:488-494.
71. Schwabe L., Dalm S., Schächinger H., Oitzl M.S. Chronic stress modulates the use of spatial and stimulus-response learning strategies in mice and man. Neurobiol Learn Mem 2008, 90:495-503.
72. Schwabe L., Wolf O.T. Stress-induced modulation of instrumental behavior: from goal-directed to habitual control of action. Behav Brain Res 2011, 219:321-328.
73. Shohamy D., Myers C.E., Hopkins R.O., Sage J., Gluck M.A. Distinct hippocampal and basal ganglia contributions to probabilistic learning and reversal. J Cogn Neurosci 2008, 21:1821-1833.
74. Tanaka S.C., Balleine B.W., O'Doherty J.P. Calculating consequences: brain systems that encode the causal effects of actions. J Neurosci 2008, 28:6750-6755.
75. Taris T.W., Feij J.A. Learning and strain among newcomers: a three-wave study on the effects of job demands and job control. J Psychol 2004, 138:543-563.
76. Thayer J.F., Brosschot J.F. Psychosomatics and psychopathology: looking up and down from the brain. Psychoneuroendocrinology 2005, 30:1050-1058.
77. Thayer J.F., Lane R.D. Claude Bernard and heart-brain connection: further elaboration of a model of neurovisceral integration. Neurosci Biobehav Rev 2009, 33:81-88.
78. Tobler P.N., Fiorillo C.D., Schultz W. Adaptive coding of reward value by dopamine neurons. Science 2005, 307:1642-1645.
79. Tremblay L., Schultz W. Relative reward preference in primate orbitofrontal cortex. Nature 1999, 398:704-708.
80. Tricomi E., Balleine B.W., O'Doherty J.P. A specific role for posterior dorsolateral striatum in human habit learning. Eur J Neurosci 2009, 29:2225-2232.
81. Wang J, Smailes E, Sareen J, Schmitz N, Fick G, Patten S (in press) Three job-related stress models and depression: a population-based study. Soc Psychiatry Psychiatr Epidemiol, in press.
82. Wieclaw J., Agerbo E., Mortensen P.B., Burr H., Tuchsen F., Bonde J.P. Psychosocial working conditions and the risk of depression and anxiety disorders in the Danish workforce. BMC Public Health 2008, 8:280.
83. Wong S.W., Massé N., Kimmerly D.S., Menon R.S., Shoemaker J.K. Ventral medial prefrontal cortex and cardiovagal control in conscious humans. Neuroimage 2007, 35:698-708.
84. Xue G., Ghahremani D.G., Poldrack R.A. Neural substrates for reversing stimulus-outcome and stimulus-response associations. J Neurosci 2008, 28:11196-11204.
85. Yin H.H., Knowlton B.J., Balleine B.W. Inactivation of dorsolateral striatum enhances sensitivity to changes in the action-outcome contingency in instrumental conditioning. Behav Brain Res 2006, 166:189-196.
86. Yin H.H., Ostlund S.B., Knowlton B.J., Balleine B.W. The role of the dorsomedial striatum in instrumental conditioning. Eur J Neurosci 2005, 22:513-523.