Right ventromedial prefrontal lesions result in paradoxical cardiovascular activation with emotional stimuli

Brain

Volumn 129, Issue 12, 2006, Pages 3343-3355

  Hilz, Max J ^a,d   Devinsky, Orrin ^a,f   Szczepanska, Hanna ^a,b   Borod, Joan C ^b,c   Marthol, Harald ^a,d   Tutaj, Marcin ^a,e  

^a NEW YORK UNIVERSITY   (United States)

^b MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^c CITY UNIVERSITY OF NEW YORK   (United States)

^d UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

^e JAGIELLONIAN UNIVERSITY MEDICAL COLLEGE   (Poland)

^f NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Cardiovascular autonomic system; Emotion; Prefrontal cortex; Somatic markers; Valence hypothesis

Indexed keywords

ADULT; ANXIETY; AROUSAL; ARTICLE; BLOOD PRESSURE; BRAIN DAMAGE; BREATHING; CARDIOVASCULAR FUNCTION; CLINICAL ARTICLE; DECISION MAKING; EMOTION; END TIDAL CARBON DIOXIDE TENSION; FEMALE; HEART ARRHYTHMIA; HEART RATE; HEMISPHERE; HUMAN; HYPERTENSION; MALE; OXYGEN SATURATION; PHYSICAL ACTIVITY; PREFRONTAL CORTEX; PRIORITY JOURNAL; REST; RR INTERVAL; VALSALVA MANEUVER; VISUAL STIMULATION;

EID: 33845340808     PISSN: 00068950     EISSN: 14602156     Source Type: Journal    
DOI: 10.1093/brain/awl299     Document Type: Article

References (67)

1. Anderson SW, Bechara A, Damasio H, Tranel D, Damasio AR. Impairment of social and moral behavior related to early damage in human prefrontal cortex. Nat Neurosci 1999; 2: 1032-7.
2. Barrash J, Tranel D, Anderson SW. Acquired personality disturbances associated with bilateral damage to the ventromedial prefrontal region. Dev Neuropsychol 2000; 18: 355-81.
3. Bechara A, Damasio AR, Damasio H, Anderson SW. Insensitivity to future consequences following damage to human prefrontal cortex. Cognition 1994; 50: 7-15.
4. Bechara A, Tranel D, Damasio H, Damasio AR. Failure to respond autonomically to anticipated future outcomes following damage to prefrontal cortex. Cereb Cortex 1996; 6: 215-25.
5. Bechara A, Damasio H, Damasio AR. Emotion, decision making and the orbitofrontal cortex. Cereb Cortex 2000; 10: 295-307.
6. Benarroch EE. Overview of the organization of the central autonomic network. In: Benarroch EE, editor. Central autonomic network: functional organization and clinical correlations. Armonk, NY: Futura Publishing Company, Inc.; 1997. p. 3-28.
7. Bernardi L, Bianchini B, Spadacini G, Leuzzi S, Valle F, Marchesi E, et al. Demonstrable cardiac reinnervation after human heart transplantation by carotid baroreflex modulation of RR interval. Circulation 1995; 92: 2895-903.
8. Black M, Graham DI. Sudden unexplained death in adults caused by intracranial pathology. J Clin Pathol 2002; 55: 44-50.
9. Borod JC, Madigan N. Neuropsychology of emotion and emotional disorders: an overview and research directions. In: Borod JC, editor. The neuropsychology of emotion. New York: Oxford University Press; 2000. p. 3-28.
10. Borod JC, Koff E, White B. Facial asymmetry in posed and spontaneous expressions of emotion. Brain Cogn 1983; 2: 165-75.
11. Borod JC, Koff E, Lorch MP, Nicholas M. Channels of emotional expression in patients with unilateral brain damage. Arch Neurol 1985; 42: 345-8.
12. Borod JC, Koff E, Lorch MP, Nicholas M. The expression and perception of facial emotion in brain-damaged patients. Neuropsychologia 1986; 24: 169-80.
13. Bradley BW, McCanne TR. Autonomic responses to stress: the effects of progressive relaxation, the relaxation response, expectancy of relief. Biofeedback Self Regul 1981; 6: 235-51.
14. Bradley MM, Codispoti M, Cuthbert BN, Lang PJ. Emotion, motivation I: defensive and appetitive reactions in picture processing. Emotion 2001; 1: 276-98.
15. Brody LR, Hall JA. Gender and emotion. In: Lewis M, Haviland JM, editors. Handbook of emotions. New York: Guilford Press; 1993. p. 447-60.
16. Brys M, Brown CM, Marthol H, Franta R, Hilz MJ. Dynamic cerebral autoregulation remains stable during physical challenge in healthy persons. Am J Physiol Heart Circ Physiol 2003; 285: H1048-54.
17. Buck R. The slide-viewing technique for measuring nonverbal sending accuracy: a guide for replication. Catalog Select Doc Psychol 1978; 8: 63.
18. Buck R, Duffy RJ. Nonverbal communication of affect in brain-damaged patients. Cortex 1980; 16: 351-62.
19. Burr RL, Cowan MJ. Autoregressive spectral models of heart rate variability. Practical issues. J Electrocardiol 1992; 25 (Suppl): 224-33.
20. Critchley HD, Corfield DR, Chandler MP, Mathias CJ, Dolan RJ. Cerebral correlates of autonomic cardiovascular arousal: a functional neuroimaging investigation in humans. J Physiol 2000; 523: 259-70.
21. Critchley HD, Taggart P, Sutton PM, Holdright DR, Batchvarov V, Hnatkova K, et al. Mental stress and sudden cardiac death: asymmetric midbrain activity as a linking mechanism. Brain 2005; 128: 75-85.
22. Damasio AR. Descartes' error: emotion, reason and the human brain. New York, NY: Avon Books; 1994.
23. Damasio AR, Grabowski TJ, Bechara A, Damasio H, Ponto LL, Parvizi J, et al. Subcortical and cortical brain activity during the feeling of self-generated emotions. Nat Neurosci 2000; 3: 1049-56.
24. Davidson RJ. Cerebral asymmetry, emotion and affective style. In: Davidson RJ, Hugdahl K, editors. Brain asymmetry. Cambridge, MA: MIT Press; 1995. p. 361-87.
25. Davidson RJ, Irwin W. The functional neuroanatomy of emotion and affective style. Trends Cogn Sci 1999; 3: 11-21.
26. Davison GC, Williams ME, Nezami E, Bice TL, DeQuattro VL. Relaxation, reduction in angry articulated thoughts, improvements in borderline hypertension and heart rate. J Behav Med 1991; 14: 453-68.
27. Devinsky O, D'Esposito M. Neurology of cognitive and behavioral disorders. New York: Oxford University Press; 2004.
28. Diamond BJ, Mayes AR, Meudell PR. Autonomic and recognition indices of memory in amnesic and healthy control subjects. Cortex 1996; 32: 439-59.
29. Dimond SJ, Farrington L, Johnson P. Differing emotional response from right and left hemisphere. Nature 1976; 261: 689-91.
30. Ewing DJ, Clarke BF. Diagnosis and management of diabetic autonomic neuropathy. Br Med J 1982; 285: 916-8.
31. Frysztak RJ, Neafsey EJ. The effect of medial frontal cortex lesions on cardiovascular conditioned emotional responses in rat. Brain Res 1994; 643: 181-93.
32. Gainotti G. Disorders of emotional behaviour. J Neurol 2001; 248: 743-9.
33. George MS, Ketter TA, Parekh PI, Herscovitch P, Post RM. Gender differences in regional cerebral blood flow during transient self-induced sadness or happiness. Biol Psychiatry 1996; 40: 859-71.
34. Gross JJ, Frederickson BL, Levenson RW. The psychophysiology of crying. Psychophysiology 1994; 31: 460-8.
35. Heilman KM, Schwartz HD, Watson RT. Hypoarousal in patients with the neglect syndrome and emotional indifference. Neurology 1978; 28: 229-32.
36. Herpertz SC, Kunert HJ, Schwenger UB, Sass H. Affective responsiveness in borderline personality disorder: a psychophysiological approach. Am J Psychiatry 1999; 156: 1550-6.
37. Hilz MJ, Dutsch M, Perrine K, Nelson PK, Rauhut U, Devinsky O. Hemispheric influence on autonomic modulation and baroreflex sensitivity. Ann Neurol 2001; 49: 575-84.
38. Hilz MJ, Devinsky O, Doyle W, Mauerer A, Dutsch M. Decrease of sympathetic cardiovascular modulation after temporal lobe epilepsy surgery. Brain 2002; 125: 985-95.
39. Jennings JR, Nebes RD, Yovetich NA. Aging increases the energetic demands of episodic memory: a cardiovascular analysis. J Exp Psychol Gen 1990; 119: 77-91.
40. Kemmotsu O, Ueda M, Otsuka H, Yamamura T, Winter DC, Eckerle JS. Arterial tonometry for noninvasive, continuous blood pressure monitoring during anesthesia. Anesthesiology 1991; 75: 333-40.
41. Labouvie-Vief G, Lumley MA, Jain E, Heinze H. Age and gender differences in cardiac reactivity and subjective emotion responses to emotional autobiographical memories. Emotion 2003; 3: 115-26.
42. Mandal MK, Borod JC, Asthana HS, Mohanty A, Mohanty S, Koff E. Effects of lesion variables and emotion type on the perception of facial emotion. J Nerv Ment Dis 1999; 187: 603-9.
43. Meadows ME, Kaplan RF. Dissociation of autonomic and subjective responses to emotional slides in right hemisphere damaged patients. Neuropsychologia 1994; 32: 847-56.
44. Morris PL, Robinson RG, Raphael B, Hopwood MJ. Lesion location and poststroke depression. J Neuropsychiatry Clin Neurosci 1996; 8: 399-403.
45. Morrow L, Vrtunsky PB, Kim Y, Boller F. Arousal responses to emotional stimuli and laterality of lesion. Neuropsychologia 1981; 19: 65-71.
46. Neafsey EJ. Prefrontal cortical control of the autonomic nervous system: anatomical and physiological observations. Prog Brain Res 1990; 85: 147-66.
47. Oppenheimer SM, Wilson JX, Guiraudon C, Cechetto DF. Insular cortex stimulation produces lethal cardiac arrhythmias: a mechanism of sudden death? Brain Res 1991; 550: 115-21.
48. Owens NC, Verberne AJ. Medial prefrontal depressor response: involvement of the rostral and caudal ventrolateral medulla in the rat. J Auton Nerv Syst 2000; 78: 86-93.
49. Owens NC, Verberne AJ. Regional haemodynamic responses to activation of the medial prefrontal cortex depressor region. Brain Res 2001; 919: 221-31.
50. Paradiso S, Chemerinski E, Yazici KM, Tartaro A, Robinson RG. Frontal lobe syndrome reassessed: comparison of patients with lateral or medial frontal brain damage. J Neurol Neurosurg Psychiatry 1999; 67: 664-7.
51. Phillips ML, Drevets WC, Rauch SL, Lane R. Neurobiology of emotion perception I: The neural basis of normal emotion perception. Biol Psychiatry 2003; 54: 504-14.
52. Piccirillo G, Elvira S, Bucca C, Viola E, Cacciafesta M, Marigliano V. Abnormal passive head-up tilt test in subjects with symptoms of anxiety power spectral analysis study of heart rate and blood pressure. Int J Cardiol 1997; 60: 121-31.
53. Piccirillo G, Elvira S, Viola E, Bucca C, Durante M, Raganato P, et al. Autonomic modulation of heart rate and blood pressure in hypertensive subjects with symptoms of anxiety. Clin Sci (Lond) 1998; 95: 43-52.
54. Pollatos O, Kirsch W, Schandry R. Brain structures involved in interoceptive awareness and cardioafferent signal processing: a dipole source localization study. Hum Brain Mapp 2005; 26: 54-64.
55. Rolls ET. The functions of the orbitofrontal cortex. Brain Cogn 2004; 55: 11-29.
56. Ross ED. Right hemisphere syndromes and the neurology of emotion. In: Schacter SC, Devinsky O, editors. Behavioral neurology and the legacy of Norman Geschwind. Philadelphia, PA: Lippincott-Raven; 1997. p. 183-91.
57. Sakuragi S, Sugiyama Y, Takeuchi K. Effects of laughing and weeping on mood and heart rate variability. J Physiol Anthropol Appl Human Sci 2002; 21: 159-65.
58. Samuels MA. Neurally induced cardiac damage. Definition of the problem. Neurol Clin 1993; 11: 273-92.
59. Saul JP, Berger RD, Albrecht P, Stein SP, Chen MH, Cohen RJ. Transfer function analysis of the circulation: unique insights into cardiovascular regulation. Am J Physiol 1991; 261: H1231-45.
60. Spielberger CD, Gorsuch RL, Lushene R, Vagg PR, Jacobs GA. Manual for the state-trait anxiety inventory. Pao Alto (CA): Consulting Psychologists Press; 1983.
61. Spyer KM. Central nervous control of the cardiovascular system. In: Mathias CJ, Bannister R, editors. Autonomic failure: a textbook of clinical disorders of the autonomic nervous system. New York: Oxford University Press; 1999. p. 45-55.
62. Starkstein SE, Robinson RG, Honig MA, Parikh RM, Joselyn J, Price TR. Mood changes after right-hemisphere lesions. Br J Psychiatry 1989; 155: 79-85.
63. Task Force of the European Society of Cardiology and the North American Society of Pacing and Electrophysiology. Heart rate variability: standards of measurement, physiological interpretation, and clinical use. Circulation 1996; 93: 1043-65.
64. Tranel D, Bechara A, Denburg NL. Asymmetric functional roles of right and left ventromedial prefrontal cortices in social conduct, decision-making, and emotional processing. Cortex 2002; 38: 589-612.
65. Verberne AJ, Lewis SJ, Worland PJ, Beart PM, Jarrott B, Christie MJ, et al. Medial prefrontal cortical lesions modulate baroreflex sensitivity in the rat. Brain Res 1987; 426: 243-9.
66. Waldstein SR, Kop WJ, Schmidt LA, Haufler AJ, Krantz DS, Fox NA. Frontal electrocortical and cardiovascular reactivity during happiness and anger. Biol Psychol 2000; 55: 3-23.
67. Zamrini EY, Meador KJ, Loring DW, Nichols FT, Lee GP, Figueroa RE, et al. Unilateral cerebral inactivation produces differential left/right heart rate responses. Neurology 1990; 40: 1408-11.