Blunted cardiac stress reactivity relates to neural hypoactivation

Psychophysiology

Volumn 50, Issue 3, 2013, Pages 219-229

  Ginty, Annie T ^a   Gianaros, Peter J ^b   Derbyshire, Stuart W G ^a   Phillips, Anna C ^a   Carroll, Douglas ^a  

^a UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^b UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

FMRI; Heart rate; Stress reactivity

Indexed keywords

EID: 84873283250     PISSN: 00485772     EISSN: 14698986     Source Type: Journal    
DOI: 10.1111/psyp.12017     Document Type: Article

References (106)

1. Adolphs, R., Gosselin, F., Buchanan, T. W., Tranel, D., Schyns, P., & Damasio, A. R. (2005). A mechanism for impaired fear recognition after amygdala damage. Nature, 433, 68-72.
2. Al'Absi, M., Devereux, R. B., Rao, D. C., Kitzman, D., Oberman, A., Hopkins, P., Arnett, D. K. (2006). Blood pressure stress reactivity and left ventricular mass in a random community sample of African-American and Caucasian men and women. The American Journal of Cardiology, 97, 240-244.
3. Al'Absi, M., Hatsukami, D., & Davis, G. L. (2005). Attenuated adrenocorticotropic responses to psychological stress are associated with early smoking relapse. Psychopharmacology (Berlin), 181, 107-117.
4. Al'Absi, M., Wittmers, L. E., Erickson, J., Hatsukami, D., & Crouse, B. (2003). Attenuated adrenocortical and blood pressure responses to psychological stress in ad libitum and abstinent smokers. Pharmacology, Biochemistry, and Behavior, 74, 401-410.
5. Allen, G. V., Saper, C. B., Hurley, K. M., & Cechetto, D. F. (1991). Organization of visceral and limbic connections in the insula cortex of the rat. The Journal of Comparative Neurology, 311, 1-16.
6. Andrews, M. M., Meda, S. A., Thomas, A. D., Potenza, M. N., Krystal, J. H., Worhunsky, P., Pearlson, G. D. (2011). Individuals family history positive for alcoholism show functional magnetic resonance imaging differences in reward sensitivity that are related to impulsivity factors. Biological Psychiatry, 69, 675-683.
7. Balanos, G. M., Phillips, A. C., Frenneaux, M. P., McIntyre, D., Lykidis, C., Griffin, H. S., & Carroll, D. (2010). Metabolically exaggerated cardiac reactions to acute psychological stress: The effects of resting blood pressure status and possible underlying mechanisms. Biological Psychology, 85, 104-111.
8. Barbas, H., Saha, S., Rempel-Clower, N., & Ghashghaei, T. (2003). Serial pathways from primate prefrontal cortex to autonomic areas may influence emotional expression. BMC Neuroscience, 4, 25-37.
9. Barnett, P. A., Spence, J. D., Manuck, S. B., & Jennings, J. R. (1997). Psychological stress and the progression of carotid artery disease. Journal of Hypertension, 15, 49-55.
10. Batterink, L., Yokum, S., & Stice, E. (2010). Body mass correlates inversely with inhibitory control in response to food among adolescent girls: An fMRI study. Neuroimage, 52, 1696-1703.
11. Bechara, A., Damasio, H., Damasio, A. R., & Lee, G. P. (1999). Different contributions of the human amygdala and ventromedial prefrontal cortex to decision-making. Journal of Neuroscience, 19, 5473-5481.
12. Beck, A., Schlagenhauf, F., Wustenberg, T., Hein, J., Kienast, T., Kahnt, T., Wrase, J. (2009). Ventral striatal activation during reward anticipation correlates with impulsivity in alcoholics. Biological Psychiatry, 66, 734-742.
13. Bennarroch, E. E. (1997). Central autonomic network: Functional organization and clinical correlations. Armonk, NY: Futura Publishing Company.
14. Buchanan, T. W., Etzel, J. A., Adolphs, R., & Tranel, D. (2006). The influence of autonomic arousal and semantic relatedness on memory for emotional words. International Journal of Psychophysiology, 61, 26-33.
15. Bush, G., Luu, P., & Posner, M. I. (2000). Cognitive and emotional influences in anterior cingulate cortex. Trends in Cognitive Science, 4, 215-222.
16. Bush, G., & Shin, L. M. (2006). The Multi-Source Interference Task: An fMRI task that reliably activates the cingulo-frontal-parietal cognitive/attention network. Nature Protocols, 1, 308-313.
17. Bush, G., Spencer, T. J., Holmes, J., Shin, L. M., Valera, E. M., Seidman, L. J., Biederman, J. (2008). Functional magnetic resonance imaging of methylphenidate and placebo in attention-deficit/hyperactivity disorder during the multi-source interference task. Archives of General Psychiatry, 65, 102-114.
18. Bush, G., Vogt, B. A., Holmes, J., Dale, A. M., Greve, D., Jenike, M. A., & Rosen, B. R. (2002). Dorsal anterior cingulate cortex: A role in reward based decision making. Proceedings of the National Academy of Sciences of the United States of America, 99, 523-529.
19. Carroll, D., Ginty, A. T., Der, G., Hunt, K., Benzeval, M., & Phillips, A. C. (2012). Increased blood pressure reactions to acute mental stress are associated with 16-year cardiovascular disease mortality. Psychophysiology, 49, 1444-1448.
20. Carroll, D., Lovallo, W. R., & Phillips, A. C. (2009). Are large physiological reactions to acute psychological stress always bad for health? Social and Personality Psychology Compass, 3, 725-743.
21. Carroll, D., Phillips, A. C., & Der, G. (2008). Body mass index, abdominal adiposity, obesity and cardiovascular reactions to psychological stress in a large community sample. Psychosomatic Medicine, 70, 653-660.
22. Carroll, D., Phillips, A. C., Hunt, K., & Der, G. (2007). Symptoms of depression and cardiovascular reactions to acute psychological stress: Evidence from a population study. Biological Psychology, 75, 68-74.
23. Carroll, D., Phillips, A. C., & Lovallo, W. R. (2011). The behavioural and health corollaries of blunted physiological reactions to acute psychological stress: Revising the reactivity hypothesis. In R. A. Wright & G. H. E. Gendolla (Eds.), Motivation perspectives of cardiovascular response (pp. 243-263). Washington, DC: APA Press.
24. Carroll, D., Ring, C., Hunt, K., Ford, G., & Macintyre, S. (2003). Blood pressure reactions to stress and the prediction of future blood pressure: Effects of sex, age, and socioeconomic position. Psychosomatic Medicine, 65, 1058-1064.
25. Carroll, D., Smith, G. D., Sheffield, D., Shipley, M. J., & Marmot, M. G. (1995). Pressor reactions to psychological stress and prediction of future blood pressure: Data from the Whitehall II Study. British Medical Journal, 310, 771-776.
26. Carroll, D., Smith, G. D., Shipley, M. J., Steptoe, A., Brunner, E. J., & Marmot, M. G. (2001). Blood pressure reactions to acute psychological stress and future blood pressure status: A 10-year follow-up of men in the Whitehall II study. Psychosomatic Medicine, 63, 737-743.
27. Carroll, D., Turner, J. R., Lee, H. J., & Stephenson, J. (1984). Temporal consistency of individual differences in cardiac response to a video game. Biological Psychology, 19, 81-93.
28. Cechetto, D. F. (1994). Identification of a cortical site for stress-induced cardiovascular dysfunction. Integrative Physiological and Behavioral Science, 29, 362-373.
29. Cechetto, D. F., & Chen, S. J. (1990). Subcortical sites mediating sympathetic responses from insula cortex in rats. American Journal of Physiology, 258, R245-R255.
30. Cechetto, D. F., & Shoemaker, J. K. (2009). Functional neuroanatomy of autonomic regulation. NeuroImage, 47, 795-803.
31. Chida, Y., & Steptoe, A. (2010). Greater cardiovascular responses to laboratory mental stress are associated with poor subsequent cardiovascular risk status. Hypertension, 55, 1026-1032.
32. Critchley, H. D., Corfield, D. R., Chandler, M. P., Mathias, C. J., & Dolan, R. J. (2000). Cerebral correlates of autonomic cardiovascular arousal: A functional neuroimaging investigation in humans. Journal of Phsyiology, 15, 259-270.
33. Critchley, H. D., Mathias, C. J., Josephs, O., O'Doherty, J., Zanini, S., Dewar, B. K., Dolan, R. J. (2003). Human cingulate cortex and autonomic control: Converging neuroimaging and clinical evidence. Brain, 126, 2139-2152.
34. Critchley, H. D., Rotshtein, P., Nagai, Y., O'Doherty, J., Mathias, C. J., & Dolan, R. J. (2005). Activity in the human brain predicting differential heart rate responses to emotional facial expressions, NeuroImage, 24, 751-762.
35. Dampney, R. A. (1994). Functional organization of central pathways regulating the cardiovascular system. Physiology Review, 74, 323-364.
36. Dampney, R. A., Coleman, M. J., Fontes, M. A., Hirooka, Y., & Horiuchi, J. (2003). Functional organization of brain pathways subserving the baroreceptor reflex: Studies in conscious animals using immediate early gene expression. Cellular and Molecular Neurobiology, 23, 597-616.
37. de Rooij, S. R., & Roseboom, T. J. (2010). Further evidence for an association between self-reported health and cardiovascular as well as cortisol reactions to acute psychological stress. Psychophysiology, 47, 1172-1175.
38. de Rooij, S. R., Schene, A. H., Phillips, D. I., & Roseboom, T. J. (2010). Depression and anxiety: Associations with biological and perceived stress reactivity to a psychological stress protocol in a middle-aged population. Psychoneuroendocrinology, 35, 866-877.
39. de Vries-Bouw, M., Popma, A., Vermeiren, R., Doreleijers, T. A., van de Ven, P. M., & Jansen, L. M. (2011). Psychophysiology, 48, 1597-1604.
40. Everson, S. A., Kaplan, G. A., Goldberg, D. E., & Salonen, J. T. (1996). Anticipatory blood pressure response to exercise predicts future high blood pressure in middle-aged men. Hypertension, 27, 1059-1064.
41. Everson, S. A., Lynch, J. W., Chesney, M. A., Kaplan, G. A., Goldberg, D. E., Shade, S. B., Salonen, J. T. (1997). Interaction of workplace demands and cardiovascular reactivity in progression of carotid atherosclerosis: Population based study. British Medical Journal, 314, 553-558.
42. Everson, S. A., Lynch, J. W., Kaplan, G. A., Lakka, T. A., Sivenius, J., & Salonen, J. T. (2001). Stress-induced blood pressure reactivity and incident stroke in middle-aged men. Stroke, 32, 1263-1270.
43. Fellahi, J., Caille, V., Charron, C., Deschamps-Berger, P., & Vieillard-Baron, A. (2009). Noninvasive assessment of cardiac index in healthy volunteers: A comparison between thoracic impedance cardiography and Doppler echocardiography. Anesthesia and Analgesia, 108, 1553-1559.
44. Georgiades, A., Lemne, C., de Faire, U., Lindvall, K., & Fredrikson, M. (1997). Stress-induced blood pressure measurements predict left ventricular mass over three years among borderline hypertensive men. European Journal of Clinical Investigation, 27, 733-739.
45. Gerin, W., Pickering, T. G., Glynn, L., Christenfeld, N., Schwartz, A., Carroll, D., & Davidson, K. (2000). An historical context for behavioral models of hypertension. Journal of Psychosomatic Research, 48, 369-377.
46. Gianaros, P. J., Derbyshire, S. W., May, J. C., Siegle, G. J., Gamalo, M. A., & Jennings, J. R. (2005). Anterior cingulate activity correlates with blood pressure during stress. Psychophysiology, 42, 627-635.
47. Gianaros, P. J., May, J. C., Siegle, G. J., & Jennings, J. R. (2005). Is there a functional neural correlate of individual differences in cardiovascular reactivity? Psychosomatic Medicine, 67, 31-39.
48. Gianaros, P. J., Onyewuenyi, I. C., Sheu, L. K., Christie, I. C., & Critchley, H. D. (2012). Brain systems for baroreflex supression during stress in humans. Human Brain Mapping, 33, 1700-1706.
49. Gianaros, P. J., & Sheu, L. K. (2009). A review of neuroimaging studies of stressor-evoked blood pressure reactivity: Emerging evidence for a brain-body pathway to coronary heart disease risk. NeuroImage, 47, 922-936.
50. Gianaros, P. J., Sheu, L. K., Matthews, K. A., Jennings, J. R., Manuck, S. B., & Hariri, A. R. (2008). Individual differences in stressor-evoked blood pressure reactivity vary with activation, volume, and functional connectivity of the amygdala. Journal of Neuroscience, 28, 990-999.
51. Gianaros, P. J., Sheu, L. K., Remo, A. M., Christie, I. C., Critchley, H. D., & Wang, J. (2009). Heightened resting neural activity predicts exaggerated stressor-evoked blood pressure reactivity. Hypertension, 53, 819-825.
52. Ginty, A. T., Phillips, A. C., Der, G., Deary, I. J., & Carroll, D. (2011a). Heart rate reactivity is associated with future cognitive ability and cognitive change in a large community sample. International Journal of Psychophysiology, 82, 167-174.
53. Ginty, A. T., Phillips, A. C., Der, G., Deary, I. J., & Carroll, D. (2011b). Cognitive ability and simple reaction time predict cardiac reactivity in the West of Scotland Twenty-07 Study. Psychophysiology, 48, 1022-1027.
54. Ginty, A. T., Phillips, A. C., Higgs, S., Heaney, J. L. J., & Carroll, D. (2012). Disordered eating behaviour is associated with blunted cortisol and cardiovascular reactions to acute psychologyical stress. Psychoneuroendocrinology, 37, 715-724.
55. Ginty, A. T., Phillips, A. C., Roseboom, T. J., Carroll, D., & de Rooij, S. R. (2012). Cardiovascular and cortisol reactions to acute psychological stress and cognitive ability in the Dutch Famine Birth Cohort Study. Psychophysiology, 49, 391-400.
56. Glahn, D. C., Lovallo, W. R., & Fox, P. T. (2007). Reduced amygdala activation in young adults at high risk of alcoholism: Studies from the Oklahoma family health patterns project. Biological Psychiatry, 61, 1306-1309.
57. Gronwall, D. (1977). Paced audiotry serial-addition task: A measure of recovery from concussion. Perceptual and Motor Skills, 44, 367-373.
58. Hagemann, D., Waldstein, S. R., & Thayer, J. F. (2003). Central autonomic nervous system integration in emotion. Brain and Cognition, 52, 78-87.
59. Heaney, J. L., Ginty, A. T., Carroll, D., & Phillips, A. C. (2011). Preliminary evidence that exercise dependence is associated with blunted cardiac and cortisol reactions to acute psychological stress. International Journal of Psychophysiology, 79, 323-329.
60. Holsen, L. M., Spaeth, S. B., Lee, J.-H., Ogden, L. A., Klibanski, A., Whitfield-Gabrieli, S., Goldstein, J. M. (2011). Stress response circuitry hypoactivation related to hormonal dysfunction in women with major depression. Journal of Affective Disorders, 131, 379-387.
61. Joos, A. A., Saum, B., Zeeck, A., Perlov, E., Glauche, V., Hartmann, A., (in press). Frontocingular dysfunction in bulimia nervosa when confronted with disease-specific stimuli. European Eating Disorders Review.
62. Kapuku, G. K., Treiber, F. A., Davis, H. C., Harshfield, G. A., Cook, B. B., & Mensah, G. A. (1999). Hemodynamic function at rest, during acute stress, and in the field: Predictors of cardiac structure and function 2 years later in youth. Hypertension, 34, 1026-1031.
63. Kirschbaum, C., Strasburger, C. J., & Langkrar, J. (1993). Attenuated cortisol response to psychological stress but not to CRH or ergometry in young habitual smokers. Pharmacology, Biochemistry, and Behavior, 44, 527-531.
64. Koo-Loeb, J. H., Pedersen, C., & Girdler, S. S. (1998). Blunted cardiovascular and catecholamine stress reactivity in women with bulima nervosa. Psychiatry Research, 80, 13-27.
65. Koski, L., & Paus, T. (2000). Functional connectivity of the anterior cingulate cortex within the human frontal lobe: A brain mapping meta-analysis. Experimental Brain Research, 133, 55-65.
66. Lovallo, W. R. (2011). Do low levels of stress reactivity signal poor states of health? Biological Psychology, 86, 121-128.
67. Lovallo, W. R., Dickensheets, S. L., Myers, D. A., Thomas, T. L., & Nixon, S. J. (2000). Blunted stress cortisol response in abstinent alcoholic and polysubstance-abusing men. Alcoholism, Clinical and Experimental Research, 24, 651-658.
68. Lynch, J. W., Everson, S. A., Kaplan, G. A., Salonen, R., & Salonen, J. T. (1998). Does low socioeconomic status potentiate the effects of heightened cardiovascular responses to stress on the progression of carotid atherosclerosis? American Journal of Public Health, 88, 389-394.
69. Mannie, Z. N., Taylor, M. J., Harmer, C. J., Cowen, P. J., & Norbury, R. (2011). Frontolimbic responses to emotional faces in young people at familial risk of depression. Journal of Affective Disorders, 130, 127-132.
70. Markovitz, J. H., Raczynski, J. M., Wallace, D., Chettur, V., & Chesney, M. A. (1998). Cardiovascular reactivity to video game predicts subsequent blood pressure increases in young men: The CARDIA study. Psychosomatic Medicine, 60, 186-191.
71. Marsh, R., Horga, G., Wang, Z., Wang, P., Klahr, K. W., Berner, L. A., Peterson, B. S. (2011). An fMRI study of self-regulatory control and conflict resolution in adolescents with bulimia nervosa. American Journal of Psychiatry, 168, 1210-1220.
72. Matthews, K. A., Owens, J. F., Kuller, L. H., Sutton-Tyrrell, K., Lassila, H. C., & Wolfson, S. K. (1998). Stress-induced pulse pressure change predicts women's carotid atherosclerosis. Stroke, 29, 1525-1530.
73. Matthews, K. A., Woodall, K. L., & Allen, M. T. (1993). Cardiovascular reactivity to stress predicts future blood pressure status. Hypertension, 22, 479-485.
74. Moss, H. B., Vanyukov, M., Yao, J. K., & Kirillova, G. P. (1999). Salivary cortisol responses in prepubertal boys: The effects of parental substance abuse and association with drug use behavior during adolescence. Biological Psychiatry, 45, 1293-1299.
75. Murdison, K. A., Treiber, F. A., Mensah, G., Davis, H., Thompson, W., & Strong, W. B. (1998). Prediction of left ventricular mass in youth with family histories of essential hypertension. The American Journal of the Medical Sciences, 315, 118-123.
76. Nettelbeck, T., & Rabbitt, P. M. (1992). Aging, cognitive performance, and mental speed. Intelligence, 16, 189-205.
77. Newman, J. D., McGarvey, S. T., & Steele, M. S. (1999). Longitudinal association of cardiovascular reactivity and blood pressure in Samoan adolescents. Psychosomatic Medicine, 61, 243-249.
78. Ongur, D., & Price, J. L. (2000). The organization of networks within the orbital and medial prefrontal cortex of rats, monkeys, and humans. Cerebral Cortex, 10, 206-219.
79. Oppenheimer, S. (1993). The anatomy and physiology of cortical mechanisms of cardiac control. Stroke, 24, I3-I5.
80. Paus, T. (2001). Primate anterior cingulate cortex: Where motor control, drive, and cognition interface. Nature Reviews Neuroscience, 2, 417-424.
81. Panknin, T. L., Dickensheets, S. L., Nixon, S. J., & Lovallo, W. R. (2002). Attenuated heart rate responses to public speaking in individuals with alcohol dependence. Alcoholism, Clinical and Experimental Research, 26, 841-847.
82. Phillips, A. C., Der, G., & Carroll, D. (2009). Self-reported health and cardiovascular reactions to psychological stress in a large community sample. Psychophysiology, 46, 1020-1027.
83. Phillips, A. C., Der, G., Hunt, K., & Carroll, D. (2009). Haemodynamic reactions to acute psychological stress and smoking status in a large community sample. International Journal of Psychophysiology, 73, 273-278.
84. Phillips, A. C., Hunt, K., Der, G., & Carroll, D. (2011). Blunted cardiac reactions to acute psychological stress predict symptoms of depression five years later: Evidence from a large community study. Psychophysiology, 48, 1469-8986.
85. Resstel, L. B., & Correa, F. M. (2006). Involvement of the medial prefrontal cortex in central cardiovascular modulation in the rat. Autonomic Neuroscience, 126, 130-138.
86. Ruggiero, D. A., Mraovitch, S., Granata, A. R., Anwar, M., & Reis, D. J. (1987). A role in the insula cortex in cardiovascular function. Journal of Comparative Neurology, 257, 189-207.
87. Salomon, K., Clift, A., Karlsdottir, M., & Rottenberg, J. (2009). Major depressive disorder is associated with attenuated cardiovascular reactivity and impaired recovery among those free of cardiovascular disease. Health Psychology, 28, 157-165.
88. Schwartz, A. R., Gerin, W., Davidson, K. W., Pickering, T. G., Brosschot, J. F., Thayer, J. F., Linden, W. (2003). Toward a causal model of cardiovascular responses to stress and the development of cardiovascular disease. Psychosomatic Medicine, 65, 22-35.
89. Schwerdtfeger, A., & Rosenkaimer, A. K. (2011). Depressive symptoms and attenuated physiological reactivity to laboratory stressors. Biological Psychology, 87, 430-438.
90. Sheu, L. K., Jennings, J. R., & Gianaros, P. J. (2012). Test-retest reliability of an fMRI paradigm for studies of cardiovascular reactivity. Psychophysiology, 49, 873-884.
91. Shima, K., & Tanji, J. (1998). Role for cingulate motor area cells in voluntary movement selection based on reward. Science, 282, 1335-1338.
92. Sorocco, K. H., Lovallo, W. R., Vincent, A. S., & Collins, F. L. (2006). Blunted hypothalamic-pituitary-adrenocortical axis responsivity to stress in persons with a family history of alcoholism. International Journal of Psychophysiology, 59, 210-217.
93. Soufer, R., Bremner, J. D., Arrighi, J. A., Cohen, I., Zaret, B. L., Burg, M. M., & Goldman-Rakic, P. (1998). Cerebral cortical hyperactivation in response to mental stress in patients with coronary artery disease. Proceedings of the National Academy of Sciences of the United States of America, 95, 6454-6459.
94. Stice, E., Spoor, S., Bohon, C., Veldhuizen, M. G., & Small, D. M. (2008). Relation of reward from food intake and anticipated food intake to obesity: A functional magnetic resonance imaging study. Journal of Abnormal Psychology, 117, 924-935.
95. Stice, E., Yokum, S., Blum, K., & Bohon, C. (2010). Weight gain is associated with reduced striatal response to palatable food. Journal of Neuroscience, 30, 13105-13109.
96. Taylor, T. R., Kamarck, T. W., & Dianzumba, S. (2003). Cardiovascular reactivity and left ventricular mass: An integrative review. Annals of Behavioral Medicine, 26, 182-193.
97. Thayer, J. F., & Lane, R. D. (2009). Claude Bernard and the heart-brain connection: Further elaboration of a model of neurovisceral integration. Neuroscience and Biobehavioral Reviews, 33, 81-88.
98. Treiber, F. A., Kamarck, T., Schneiderman, N., Sheffield, D., Kapuku, G., & Taylor, T. (2003). Cardiovascular reactivity and development of preclinical and clinical disease states. Psychosomatic Medicine, 65, 46-62.
99. Treiber, F. A., Turner, J. R., Davis, H., & Strong, W. B. (1997). Prediction of resting cardiovascular functioning in youth with family histories of essential hypertension: A 5-year follow-up. International Journal of Behavioral Medicine, 4, 278-291.
100. Verberne, A. J. M., & Owens, N. C. (1998). Cortical modulation of the cardiovascular system. Progress in Neurobiology, 54, 149-158.
101. Wager, T., van Ast, V., Huges, B., Davidson, M., Lindquist, M., & Ochsner, K. (2009). Brain mediators of cardiovascular responses to social threat. II. Prefrontal-subcortical pathways and relationship with anxiety. NeuroImage, 47, 836-851.
102. Wager, T. D., Waugh, C. E., Lindquist, M., Noll, D. C., Fredrickson, B. L., & Taylor, S. F. (2009). Brain mediators of cardiovascular responses to social threat, Part I: Reciprocal dorsal and ventral sub-regions of the medial prefrontal cortex and heart-rate reactivity. NeuroImage, 47, 821-835.
103. Waldstein, S. R., Siegel, E. L., Lefkowitz, D., Maier, K. J., Brown, J. R., Obuchowski, A. M., & Katzel, L. I. (2004). Stress-induced blood pressure reactivity and silent cerebrovascular disease. Stroke, 35, 1294-1298.
104. Wang, J., Rao, H., Wetmore, G. S., Furlan, P. M., Korczkowski, M., Dinges, D. F., & Detre, J. A. (2005). Perfusion functional MRI reveals cerebral blood flow pattern under psychological stress. Proceedings of the National Academy of Sciences, 102, 17804-17809.
105. Williams, Z. M., Bush, G., Rauch, S. L., Cosgrove, G. R., & Eskandar, E. N. (2004). Human anterior cingulate neurons and the integration of monetary reward with motor responses. Nature Neuroscience, 7, 1370-1375.
106. Yasui, Y., Breder, C. D., Saper, C. B., & Cechetto, D. F. (1991). Autonomic responses and efferent pathways from the insula cortex in the rat. Journal of Comparative Neurology, 303, 355-374.