Emotional appraisal is influenced by cardiac afferent information

Emotion

Volumn 12, Issue 1, 2012, Pages 180-191

  Gray, Marcus A ^a,b   Beacher, Felix D ^a   Minati, Ludovico ^a   Nagai, Yoko ^a   Kemp, Andrew H ^c   Harrison, Neil A ^a   Critchley, Hugo D ^a  

^a UNIVERSITY OF SUSSEX   (United Kingdom)

^b MONASH UNIVERSITY   (Australia)

^c UNIVERSITY OF SYDNEY   (Australia)

Author keywords

Baroreceptor; Disgust expressions; Emotion; FMRI; Homeostasis

Indexed keywords

ADULT; ARTICLE; BRAIN DEPTH STIMULATION; CARDIOVASCULAR RESPONSE; DECISION MAKING; DISGUST; EMOTION; EMOTIONALITY; FACIAL EXPRESSION; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HAPPINESS; HEART RATE; HUMAN; MALE; ORBITAL CORTEX; PERIAQUEDUCTAL GRAY MATTER; PREFRONTAL CORTEX; PRESSORECEPTOR; SYSTOLE; AMYGDALOID NUCLEUS; BRAIN; ELECTROCARDIOGRAPHY; HEART; INNERVATION; INSTRUMENTATION; METHODOLOGY; NEUROPSYCHOLOGICAL TEST; NUCLEAR MAGNETIC RESONANCE IMAGING; OXIMETRY; PHYSIOLOGY; SENSORY NERVE;

ADULT; AMYGDALA; BRAIN; ELECTROCARDIOGRAPHY; EMOTIONS; FACIAL EXPRESSION; FEMALE; HEART; HEART RATE; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; NEUROPSYCHOLOGICAL TESTS; OXIMETRY; PERIAQUEDUCTAL GRAY; PREFRONTAL CORTEX; PRESSORECEPTORS; SYSTOLE; VISCERAL AFFERENTS;

EID: 84864353749     PISSN: 15283542     EISSN: 19311516     Source Type: Journal    
DOI: 10.1037/a0025083     Document Type: Article

References (80)

1. Abboud, F. M. (1979). Integration of reflex responses in the control of blood pressure and vascular resistance. American Journal of Cardiology, 44, 903-911. doi:10.1016/0002-9149(79)90221-2
2. Angrilli, A., Mini, A., Mucha, R. F., & Rau, H. (1997). The influence of low blood pressure and baroreceptor activity on pain responses. Physiology and Behavior, 62, 391-397. doi:10.1016/S0031-9384(97)00039-5
3. Ashburner, J., & Friston, K. J. (2005). Unified segmentation. Neuroimage, 26, 839-851. doi:10.1016/j.neuroimage.2005.02.018
4. Barbas, H. (2000). Connections underlying the synthesis of cognition, memory, and emotion in the primate prefrontal cortices. Brain Research Bulletin, 52, 319-330. doi:10.1016/S0361-9230(99)00245-2
5. 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. doi:10.1186/ 1471-2202-4-25
6. Beacher, F. D., Gray, M. A., Mathias, C. J., & Critchley, H. D. (2009). Vulnerability to simple faints is predicted by regional differences in brain anatomy. Neuroimage, 47, 937-945. doi:10.1016/j.neuroimage.2009.05.038
7. Behbehani, M. M. (1995). Functional characteristics of the midbrain periaqueductal gray. Progress in Neurobiology, 46, 575-605. doi:10.1016/ 0301-0082(95)00009-K
8. Brody, S., Angrilli, A., Weiss, U., Birbaumer, N., Mini, A., Veit, R., & Rau, H. (1997). Somatotosensory evoked potentials during baroreceptor stimulation in chronic low back pain patients and normal controls. International Journal of Psychophysiology, 25, 201-210. doi:10.1016/ S0167-8760(96)00740-4
9. Brody, S., & Rau, H. (1994). Behavioral and psychophysiological predictors of self-monitored 19 month blood pressure change in normotensives. Journal of Psychosomatic Research, 38, 885-891. doi:10.1016/ 0022-3999(94)90075-2
10. Chakrabarti, B., Bullmore, E., & Baron-Cohen, S. (2006). Empathizing with basic emotions, common and discrete neural substrates. Social Neuroscience, 1, 364-384. doi:10.1080/17470910601041317
11. Craig, A. D. (2002). How do you feel? Interoception: The sense of the physiological condition of the body. Nature Reviews. Neuroscience, 3, 655-666.
12. Craig, A. D. (2003). Interoception: The sense of the physiological condition of the body. Current Opinion in Neurobiology, 13, 500-505. doi:10.1016/S0959-4388(03)00090-4
13. Craig, A. D. (2009). How do you feel-now? The anterior insula and human awareness. Nature Reviews. Neuroscience, 10, 59-70. doi:10.1038/nrn2555
14. Critchley, H. D. (2009). Psychophysiology of neural, cognitive and affective integration, fMRI and autonomic indicants. International Journal of Psychophysiology, 73, 88-94. doi:10.1016/j.ijpsycho.2009.01.012
15. Critchley, H. D., Mathias, C. J., & Dolan, R. J. (2001). Neural correlates of first and second-order representation of bodily states. Nature Neuroscience, 4, 207-212. doi:10.1038/84048
16. Critchley, H. D., Mathias, C. J., & Dolan, R. J. (2002). Fear-conditioning in humans: The influence of awareness and arousal on functional neuroanatomy. Neuron, 33, 653-663. doi:10.1016/S0896-6273(02)00588-3
17. 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, 24751, 762.
18. Critchley, H. D., Wiens, S., Rotshstein, P., öhman, A., & Dolan, R. J. (2004). Neural systems supporting awareness. Nature Neuroscience, 7, 189-195. doi:10.1038/nn1176
19. Damasio, A. R. (1994). Descartes' error: Emotion, reason and the human brain. New York, NY: Grosset Putnam.
20. Damasio, A. R. (1999). The feeling of what happens: Body and emotion in the making of consciousness. New York, NY: Harcourt Brace.
21. Damasio, A. R., Tranel, D., & Damasio, H. C. (1991). Somatic markers and the guidance of behavior: Theory and preliminary testing. In H. S. Levin, H. M. Eisenberg, & L. B. Benton (Eds.), Frontal lobe function and dysfunction (Chapt 11). New York, NY: Oxford University Press.
22. Dimberg, U., Thunberg, M., & Elmehed, K. (2000). Unconscious Facial Reactions to Emotional Facial Expressions. Psychological Science, 11, 86-89. doi:10.1111/1467-9280.00221
23. Droste, C., Kardos, A., Brody, S., Greenlee, M. W., Roskamm, H., & Rau, H. (1994). Baroreceptor stimulation: Pain perception and sensory thresholds. Biological Psychology, 37, 101-113. doi:10.1016/0301-0511(94)90025-6
24. Dworkin, B. R., Elbert, T., Rau, H., Birbaumer, N., Pauli, P., Droste, C., & Brunia, C. H. (1994). Central effects of baroreceptor activation in humans: Attenuation of skeletal reflexes and pain perception. Proceedings of the National Academy of Science USA, 91, 6329-6333. doi: 10.1073/pnas.91.14.6329
25. Edwards, L., Inui, K., Ring, C., Wang, X., & Kakigi, R. (2007). Painrelated evoked potentials are modulated across the cardiac cycle. Pain, 137, 488-494. doi:10.1016/j.pain.2007.10.010
26. Edwards, L., McIntyre, D., Carroll, D., Ring, C., France, C. R., & Martin, U. (2003). Effects of artificial and natural baroreceptor stimulation on nociceptive responding and pain. Psychophysiol, 40, 762-769. doi: 10.1111/1469-8986.00076
27. Edwards, L., McIntyre, D., Carroll, D., Ring, C., & Martin, U. (2002). The human nociceptive flexion reflex threshold is higher during systole than diastole. Psychophysiology, 39, 678-681. doi:10.1111/1469-8986.3950678
28. Edwards, L., Ring, C., McIntyre, D., Winer, J. B., & Martin, U. (2009). Sensory detection thresholds are modulated across the cardiac cycle: Evidence that cutaneous sensibility is greatest for systolic stimulation. Psychophysiology, 46, 252-256. doi:10.1111/j.1469-8986.2008.00769.x
29. Ekman, P., Levenson, R. W., & Friesen, W. V. (1983). Autonomic nervous system activity distinguishes among emotions. Science, 221, 1208- 1210. doi:10.1126/science.6612338
30. Fields, H. L., & Basbaum, A. I. (1999). Central nervous system mechanisms of pain modulation. In: P. D. Wall & R. Melzack (Eds.), Textbook of pain (pp. 309-329). Edinburgh, U.K.: Churchill Livingstone.
31. Friston, K. J., Josephs, O., Zarahn, E., Holmes, A. P., Rouquette, S., & Poline, J. (2000). To smooth or not to smooth? Bias and efficiency in fMRI time-series analysis. Neuroimage, 12, 196-208. doi:10.1006/ nimg.2000.0609
32. Frith, C. D., & Allen, H. A. (1983). The skin conductance orienting response as an index of attention. Biological Psychology, 17, 27-39. doi:10.1016/0301-0511(83)90064-9
33. George, M. S., Ketter, T. A., Gill, D. S., Haxby, J. V., Ungerleider, L. G., Herscovitch, P., & Post, R. M. (1993). Brain regions involved in recognizing facial emotion or identity: An oxygen-15 PET study. Journal of Neuropsychiatry, 5, 384-394.
34. Gray, M. A., & Critchley, H. D. (2007b). Interoceptive basis to craving. Neuron, 54, 183-186. doi:10.1016/j.neuron.2007.03.024
35. Gray, M. A., Harrison, N. A., Wiens, S., & Critchley, H. D. (2007c). Modulation of emotional appraisal by false physiological feedback during fMRI. PLoS One, 2, e546. doi:10.1371/journal.pone.0000546
36. Gray, M. A., Minati, L., Harrison, N. A., Gianaros, P. J., Napadow, V., & Critchley, H. D. (2009b). Physiological recordings, basic concepts and implementation during functional magnetic resonance imaging. Neuroimage, 47, 1105-1115. doi:10.1016/j.neuroimage.2009.05.033
37. Gray, M. A., Minati, L., Paoletti, G., & Critchley, H. D. (2010). Baroreceptor activation attenuates attentional effects on pain-evoked potentials. Pain, 151, 853-861. doi:10.1016/j.pain.2010.09.028
38. Gray, M. A., Rylander, K., Harrison, N. A., Wallin, B. G., & Critchley, H. D. (2009a). Following one's heart, cardiac rhythms gate central initiation of sympathetic reflexes. Journal of Neuroscience, 29, 1817- 1825. doi:10.1523/JNEUROSCI.3363-08.2009
39. Gray, M. A., Taggart, P., Sutton, P. M., Groves, D., Holdright, D. R., Bradbury, D., ...Critchley, H. D. (2007a). A cortical potential reflecting cardiac function. Proceedings of the National Academy of Sciences of the United States of America, 104, 6818-6823. doi:10.1073/ pnas.0609509104
40. Harrison, N., Singer, T., Rotshtein, P., Dolan, R. J., & Critchley, H. D. (2006). Pupil size modulates the empathic experience of sadness. Social cognitive and Affective Neuroscience (SCAN), 1, 1-13.
41. Harrison, N. A., Brydon, L., Walker, C., Gray, M. A., Steptoe, A., Dolan, R. J., & Critchley, H. D. (2009b). Neural origins of human sickness in interoceptive responses to inflammation. Biological Psychiatry, 66, 415-422. doi:10.1016/j.biopsych.2009.03.007
42. Harrison, N. A., Brydon, . L. Walker, C., Gray, M. A., Steptoe, A., & Critchley, H. D. (2009a). Inflammation causes mood change through alterations in subgenual cingulate activity and mesolimbic connectivity. Biological Psychiatry, 66, 407-414. doi:10.1016/j.biopsych.2009.03.015
43. Hobday, D. I., Aziz, Q., Thacker, N., Hollander, I., Jackson, A. &, Thompson, D. G. (2001). A study of the cortical processing of ano-rectal sensation using functional MRI. Brain, 124, 361-8. doi:10.1093/brain/ 124.2.361
44. Hornak, J., Rolls, E. T., & Wade, D. (1996). Face and voice expression identification in patients with emotional and behavioural changes following ventral frontal lobe damage. Neuropsychologia, 34, 247-261. doi:10.1016/0028-3932(95)00106-9
45. Ishai, A. (2007). Sex, beauty and the orbitofrontal cortex. International journal of Psychophysiology, 63, 181-185. doi:10.1016/j.ijpsycho.2006.03.010
46. James, W. (1894). Physical basis of emotion. Psychological Review, 1, 516-529, reprinted in 1994. Psychological Review, 101, 205-210. doi: 10.1037/0033-295X.101.2.205
47. Jennings, J. R., van der Molen, M. W., & Debski, K. B. (2002). Probing the response selection bottleneck with a cardiac measure: Individual differences in strategy for a psychological refractory period task. Biological Psychology, 59, 207-230. doi:10.1016/S0301-0511(02)00007-8
48. Kardos, A., Rau, H., Greenlee, M. W., Droste, C., Brody, S., & Roskamm, H. (1994). Reduced pain during baroreceptor stimulation in patients with symptomatic and silent myocardial schaemia. Cardiovascular Research, 28, 515-518. doi:10.1093/cvr/28.4.515
49. Katona, P. G., Poitras, J. W., Barneit, G. O., & Terry, B. S. (1970). Cardiac vagal efferent activity and heart period in the carotid sinus reflex. American Journal of Physiology, 218, 1030-1037.
50. Kedzi, P., & Geller, E. (1968). Baroreceptor control of post-ganglionic sympathetic nerve discharge. American Journal of Physiology, 214, 427-435.
51. Kirchheim, H. R. (1976). Systemic arterial baroreceptor reflexes. Physiological Research, 56, 100-177.
52. Koizumi, K., Seller, H., Kaufmann, A., & Brooks, M. C. (1971). Pattern of sympathetic discharges and their relation to baroreceptor and respiratory activities. Brain Research, 27, 281-294. doi:10.1016/0006-8993(71)90254-X
53. Kranz, F., & Ishai, A. (2006). Face perception is modulated by sexual preference. Current biology, 16, 63-68. doi:10.1016/j.cub.2005.10.070
54. Lange, C. G. (1885). The mechanism of the emotions. In B. Rand (Ed.), The classical psychologist (pp. 672-685). Boston, MA: Houghton Mifflin.
55. Li, J., Jiangang, L., Liang, J., Zhang, H., Zhao, J., Huber, D. E.,...Shi, G. (2009). A distributed neural system for top-down face processing. Neuroscience Letters, 451, 6-10. doi:10.1016/j.neulet.2008.12.039
56. Lovick, T. A. (1992). Inhibitory modulation of the cardiovascular defense response by the ventrolateral periaqueductal grey matter in rats. Experimental Brain Research, 89, 133-139. doi:10.1007/BF00229010
57. Lundqvist, D., Flykt, A., & öhman, A. (1998). The Karolinska Directed Emotional Faces-KDEF [CD-ROM]. Department of Clinical Neuroscience, Psychology section, Karolinska Institutet, Stockholm.
58. Mason, P. (2005). Ventromedial medulla: Pain modulation and beyond. Journal of Comparative Neurology, 493, 2-8. doi:10.1002/cne.20751
59. McIntyre, D., Edwards, L., Ring, C., Parvin, B., & Carroll, D. (2006). Systolic inhibition of nociceptive responding is moderated by arousal. Psychophysiology, 43, 314-319. doi:10.1111/j.1469-8986.2006.00407.x
60. Medford, N., & Critchley, H. D. (2010). Conjoint activity of anterior insular and anterior cingulate cortex: Awareness and response. Brain Structure and Function, 214, 535-549. doi:10.1007/s00429-010-0265-x
61. Mini, A., Rau, H., Montoya, P., Palomba, D., & Birbaumer, N. (1995). Baroreceptor cortical effects, emotions and pain. International Journal of Psychophysiology, 19, 67-77. doi:10.1016/0167-8760(94)00084-R
62. Mobbs, D., Marchant, J. L., Hassabis, D., Seymour, B., Tan, G., Gray, M. A., ...Frith, C. D. (2009). From threat to fear: The neural organization of defensive fear systems in humans. Journal of Neuroscience, 29, 12236-43. doi:10.1523/JNEUROSCI.2378-09.2009
63. Mühlberger, A., Wieser, M. J., Gerdes, A. B., Frey, M. C., Weyers, P., & Pauli, P. (2010). Stop looking angry and smile, please: Start and stop of the very same facial expression differentially activate threat-and reward-related brain networks. Social Cognitive and Affective Neuroscience. [Epub ahead of print].
64. Nakamura, K., Kawashima, R., Ito, K., Sugiura, M., Kato, T., Nakamura, A., ...Kojima, S. (1999). Activation of the right inferior frontal cortex during assessment of facial emotion. Journal of Neurophysiology, 82, 1610-1614.
65. Nicotra, A., Critchley, H. D., Mathias, C. J., & Dolan, R. J. (2006). Emotional and autonomic consequences of spinal cord injury explored using functional brain imaging. Brain, 129, 718-728. doi:10.1093/brain/ awh699
66. O'Doherty, J., Kringelbach, M. L., Rolls, E. T., Hornak, J., & Andrews, C. (2001). Abstract reward and punishment representations in the human orbitofrontal cortex. Nature Neuroscience, 4, 95-102. doi:10.1038/ 82959
67. Oppenheimer, S. M., Kulshreshtha, N., Lenz, F. A., Zhang, Z., Rowland, L. H., & Dougherty, P. M. (1998). Distribution of cardiovascular related cells within the human thalamus. Clinical Autonomic Research, 8, 173- 179. doi:10.1007/BF02281122
68. Penny, W. D., & Friston, K. J. (2003). Classical and Bayesian inference. In R. S. J. Frackowiak, K. J. Friston, C. Frith, R. Dolan, C. J. Price, S. Zeki, J. Ashburner, & W. D. Penny, (Eds.), Human brain function (2nd ed.). New York, NY: Academic Press.
69. Phillips, M. L., Gregory, L. J., Cullen, S., Coen, S., Ng, V., Andrew, C., ...Aziz, Q. (2003). The effect of negative emotional context on neural and behavioural responses to oesophageal stimulation. Brain, 126, 669-684. doi:10.1093/brain/awg065
70. Piché, M., Arsenault, M., & Rainville, P. (2010). Dissection of perceptual, motor and autonomic components of brain activity evoked by noxious stimulation. Pain, 149, 453-462. doi:10.1016/j.pain.2010.01.005
71. Rau, H., Brody, S., Brunia, C. H., Damen, E. P., & Elbert, T. (1993). Activation of carotid baroreceptors inhibits spinal reflexes in man. Electroencephalography and Clinical Neurophysiology, 89, 328-334. doi:10.1016/0168-5597(93)90072-W
72. Rolls, E. T., Hornak, J., Wade, D., & McGrath, J. (1994). Emotion-related learning in patients with social and emotional changes associated with frontal lobe damage. Journal of Neurology, Neurosurgery, and Psychiatry, 57, 1518-1524. doi:10.1136/jnnp.57.12.1518
73. Sonnby-Borgström, M. (2002). Automatic mimicry reactions as related to differences in emotional empathy. Scandinavian Journal of Psychology, 43, 433-443. doi:10.1111/1467-9450.00312
74. Sprengelmeyer, R., Rausch, M., Eysel, U. T., & Przuntek, H. (1998). Neural structures associated with the recognition of facial expressions of basic emotions. Proceedings of the R Society of London B, 265, 1927- 1931. doi:10.1098/rspb.1998.0522
75. Strack, F., Martin, L. L., & Stepper, S. (1988). Inhibiting and facilitating conditions of the human smile: A nonobtrusive test of the facial feedback hypothesis. Journal of Personality and Social Psychology, 54, 768-777. doi:10.1037/0022-3514.54.5.768
76. van der Plas, J., Maes, F. W., & Bohus, B. (1995). Electrophysiological analysis of midbrain periaqueductal gray influence on cardiovascular neurons in the ventrolateral medulla oblongata. Brain Research Bulletin, 38, 447-456. doi:10.1016/0361-9230(95)02012-G
77. Wallin, B. G. (2007). Interindividual differences in muscle sympathetic nerve activity: A key to new insight into cardiovascular regulation? Acta Physiology (Oxford), 190, 265-275. doi:10.1111/j.1748-1716.2007.01730.x
78. Zhang, Z. H., Dougherty, P. M., & Oppenheimer, S. M. (1998). Characerization of baroreceptor-related neurons in the monkey insular cortex. Brain Research, 796, 303-306. doi:10.1016/S0006-8993(98)00268-6
79. Zhang, Z. H., Dougherty, P. M., & Oppenheimer, S. M. (1999). Monkey insular cortex neurons respond to baroreceptive and somatosensory convergent inputs. Neuroscience, 94, 351-360. doi:10.1016/S0306-4522(99)00339-5
80. Zhang, Z. H., & Oppenheimer, S. M. (2000). Baroreceptive and somatosensory convergent thalamic neurons project to the posterior insular cortex in the rat. Brain Research, 861, 241-256. doi:10.1016/S0006-8993(00)01990-9