Threat and the Body: How the Heart Supports Fear Processing

Trends in Cognitive Sciences

Volumn 20, Issue 1, 2016, Pages 34-46

  Garfinkel, Sarah N ^a   Critchley, Hugo D ^a,b  

^a UNIVERSITY OF SUSSEX   (United Kingdom)

^b SUSSEX PARTNERSHIP NHS FOUNDATION TRUST   (United Kingdom)

Author keywords

Amygdala; Baroreceptor; Cardiac cycle; Emotion; Interoception; Perception

Indexed keywords

BRAIN; HEART; NEUROIMAGING; PHYSIOLOGY; SENSORY FEEDBACK; SENSORY PERCEPTION;

AMYGDALA; BARORECEPTOR; CARDIAC CYCLES; EMOTION; INTEROCEPTION;

BEHAVIORAL RESEARCH;

COGNITION; CONSCIOUSNESS; EMOTION; FEAR; HEART; HEART BEAT; HEART CYCLE; HUMAN; INTEROCEPTION; MENTAL FUNCTION; NEUROIMAGING; OSCILLATION; PAIN; PRESSORECEPTOR; REVIEW; SYSTOLE; THREAT; VERBAL MEMORY; BRAIN; PHYSIOLOGY;

BRAIN; FEAR; HEART; HUMANS; PRESSORECEPTORS;

EID: 84952637819     PISSN: 13646613     EISSN: 1879307X     Source Type: Journal    
DOI: 10.1016/j.tics.2015.10.005     Document Type: Review

References (113)

1. James W. What is an Emotion?. Mind 1884, 9:188-205.
2. Lange, C.G. (ed.) (1885/1912) The Mechanisms of the Emotions, Houghton Mifflin.
3. Cannon W.B. The James-Lange theory of emotions: a critical examination and an alternative theory. Am. J. Psychol. 1927, 39:106-124.
4. Gendron M., Barrett L.F. Reconstructing the past: a century of ideas about emotion in psychology. Emot. Rev. 2009, 1:316-339.
5. Dunn B.D., et al. Can you feel the beat? Interoceptive awareness is an interactive function of anxiety- and depression-specific symptom dimensions. Behav. Res. Ther. 2010, 48:1133-1138.
6. Kreibig S.D. Autonomic nervous system activity in emotion: a review. Biol. Psychol. 2010, 84:394-421.
7. Dunn B.D., et al. Listening to your heart: how interoception shapes emotion experience and intuitive decision making. Psychol. Sci. 2010, 21:1835-1844.
8. Garfinkel S.N., et al. What the heart forgets: cardiac timing influences memory for words and is modulated by metacognition and interoceptive sensitivity. Psychophysiology 2013, 50:505-512.
9. Garfinkel S.N., et al. Fear from the heart: sensitivity to fear stimuli depends on individual heartbeats. J. Neurosci. 2014, 34:6573-6582.
10. Domschke K., et al. Interoceptive sensitivity in anxiety and anxiety disorders: an overview and integration of neurobiological findings. Clin. Psychol. Rev. 2010, 30:1-11.
11. Ehlers A. Interoception and panic disorder. Adv. Behav. Res. Ther. 1993, 15:3-21.
12. Paulus M.P., Stein M.B. Interoception in anxiety and depression. Brain Struct. Funct. 2010, 214:451-463.
13. Cameron O.G. Interoception: the inside story - a model for psychosomatic processes. Psychosom. Med. 2001, 63:697-710.
14. Sherrington C.S. The Integrative Action of the Nervous System 1948, Cambridge University Press.
15. Craig A.D. How Do You Feel? An Interoceptive Moment with your Neurobiological Self 2015, Princeton University Press.
16. Janig W. Integrative Action of the Autonomic Nervous System: Neurobiology of Homeostasis 2006, Cambridge University Press.
17. Critchley H.D., Harrison N.A. Visceral influences on brain and behavior. Neuron 2013, 77:624-638.
18. McEwen B.S., Gianaros P.J. Central role of the brain in stress and adaptation: links to socioeconomic status, health, and disease. Ann. N. Y. Acad. Sci. 2010, 1186:190-222.
19. Damasio A.R. The Feeling of what Happens: Body and Emotion in the Making of Consciousness 1999, Harcourt Brace.
20. Damasio A.R., et al. Somatic markers and the guidance of behavior: theory and preliminary testing. Frontal Lobe Function and Dysfunction 1991, 217-229. Oxford University Press. H.S. Levin (Ed.).
21. Critchley H.D. Neural mechanisms of autonomic, affective, and cognitive integration. J. Comp. Neurol. 2005, 493:154-166.
22. Critchley H.D. Psychophysiology of neural, cognitive and affective integration: fMRI and autonomic indicants. Int. J. Psychophysiol. 2009, 73:88-94.
23. Seeley W.W., et al. Dissociable intrinsic connectivity networks for salience processing and executive control. J. Neurosci. 2007, 27:2349-2356.
24. Thayer J.F., et al. Heart rate variability, prefrontal neural function, and cognitive performance: the neurovisceral integration perspective on self-regulation, adaptation, and health. Ann. Behav. Med. 2009, 37:141-153.
25. Ottaviani C., et al. The autonomic phenotype of rumination. Int. J. Psychophysiol. 2009, 72:267-275.
26. Ruiz-Padial E., et al. The effect of conscious and non-conscious presentation of biologically relevant emotion pictures on emotion modulated startle and phasic heart rate. Int. J. Psychophysiol. 2011, 79:341-346.
27. Wager T.D., et al. 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 2009, 47:821-835.
28. Wager T.D., et al. Brain mediators of cardiovascular responses to social threat. Part II: Prefrontal-subcortical pathways and relationship with anxiety. Neuroimage 2009, 47:836-851.
29. Critchley H.D., et al. Fear conditioning in humans: the influence of awareness and autonomic arousal on functional neuroanatomy. Neuron 2002, 33:653-663.
30. Herbert B.M., et al. Interoceptive sensitivity and emotion processing: an EEG study. Int. J. Psychophysiol. 2007, 65:214-227.
31. Wiens S. Interoception in emotional experience. Curr. Opin. Neurol. 2005, 18:442-447.
32. Wiens S., et al. Heartbeat detection and the experience of emotions. Cogn. Emot. 2000, 14:417-427.
33. Schandry R. Heart beat perception and emotional experience. Psychophysiology 1981, 18:483-488.
34. Katkin E.S., et al. A methodological analysis of 3 techniques for the assessment of individual-differences in heartbeat detection. Psychophysiology 1983, 20:452.
35. Whitehead W.E., et al. Relation of heart-rate control to heartbeat perception. Biofeedback Self Regul. 1977, 2:371-392.
36. Wiens S., Palmer S.N. Quadratic trend analysis and heartbeat detection. Biol. Psychol. 2001, 58:159-175.
37. Brener J., et al. The effects of manipulating beliefs about heart-rate on the accuracy of heartbeat counting in the Schandry task. Psychophysiology 1995, 32:S22.
38. Ring C., et al. Effects of heartbeat feedback on beliefs about heart rate and heartbeat counting: a cautionary tale about interoceptive awareness. Biol. Psychol. 2015, 104:193-198.
39. Werner N.S., et al. Implicit memory for emotional words is modulated by cardiac perception. Biol. Psychol. 2010, 85:370-376.
40. Suzuki K., et al. Multisensory integration across exteroceptive and interoceptive domains modulates self-experience in the rubber-hand illusion. Neuropsychologia 2013, 51:2909-2917.
41. Tsakiris M., et al. Just a heartbeat away from one's body: interoceptive sensitivity predicts malleability of body-representations. Proc. Biol. Sci. 2011, 278:2470-2476.
42. Critchley H.D., et al. Interaction between cognition, emotion, and the autonomic nervous system. Handb. Clin. Neurol. 2013, 117:59-77.
43. Duschek S., et al. The behavioral impact of baroreflex function: a review. Psychophysiology 2013, 50:1183-1193.
44. Dworkin B.R., et al. Central effects of baroreceptor activation in humans - attenuation of skeletal reflexes and pain perception. Proc. Natl. Acad. Sci. U.S.A. 1994, 91:6329-6333.
45. Edwards L., et al. The human nociceptive flexion reflex threshold is higher during systole than diastole. Psychophysiology 2002, 39:678-681.
46. Rau H., Elbert T. Psychophysiology of arterial baroreceptors and the etiology of hypertension. Biol. Psychol. 2001, 57:179-201.
47. McIntyre D., et al. Effects of arterial and cardiopulmonary baroreceptor activation on the upper limb nociceptive flexion reflex and electrocutaneous pain in humans. Pain 2008, 137:550-555.
48. McIntyre D., et al. Systolic inhibition of nociceptive responding is moderated by arousal. Psychophysiology 2006, 43:314-319.
49. Edwards L., et al. Modulation of the human nociceptive flexion reflex across the cardiac cycle. Psychophysiology 2001, 38:712-718.
50. Donadio V., et al. Inhibition of human muscle sympathetic activity by sensory stimulation. J. Physiol. 2002, 544:285-292.
51. Wallin B.G. Interindividual differences in muscle sympathetic nerve activity: a key to new insight into cardiovascular regulation?. Acta Physiol. (Oxf.) 2007, 190:265-275.
52. Donadio V., et al. Arousal elicits exaggerated inhibition of sympathetic nerve activity in phobic syncope patients. Brain 2007, 130:1653-1662.
53. Schulz A., et al. Cardiac modulation of startle eye blink. Psychophysiology 2009, 46:234-240.
54. Schulz A., et al. Lateralization effects on the cardiac modulation of acoustic startle eye blink. Biol. Psychol. 2009, 80:287-291.
55. Richter S., et al. Cardiopulmonary baroreceptors affect reflexive startle eye blink. Physiol. Behav. 2009, 98:587-593.
56. Gray M.A., et al. Following one's geart: cardiac rhythms gate central initiation of sympathetic reflexes. J. Neurosci. 2009, 29:1817-1825.
57. Walker B.B., Sandman C.A. Human visual evoked-responses are related to heart-rate. J. Comp. Physiol. Psychol. 1979, 93:717-729.
58. Cohen R., et al. Loudness judgments, evoked-potentials, and reaction-time to acoustic stimuli early and late in the cardiac cycle in chronic-schizophrenics. Psychiaty Res. 1980, 3:23-29.
59. Requin J., Brouchon M. Mise en evidence chez l'homme d'une fluctuation des seuils perceptifs visuels dans la periode cardiaque. C. R. Seances Soc. Biol. Fil. 1964, 158:1891-1894.
60. Elliott R., Graf V. Visual sensitivity as a function of phase of cardiac cycle. Psychophysiology 1972, 9:357-361.
61. Park H.D., et al. Spontaneous fluctuations in neural responses to heartbeats predict visual detection. Nat. Neurosci. 2014, 17:612-618.
62. Gray M.A., et al. emotional appraisal is influenced by cardiac afferent information. Emotion 2012, 12:180-191.
63. Mini A., et al. Baroreceptor cortical effects, emotions and pain. Int. J. Psychophysiol. 1995, 19:67-77.
64. Metzger L.J., et al. Physiologic reactivity to startling tones in women with posttraumatic stress disorder. J. Abnorm. Psychol. 1999, 108:347-352.
65. Tsunoda T., et al. Social anxiety predicts unconsciously provoked emotional responses to facial expression. Physiol. Behav. 2008, 93:172-176.
66. Anderson A.K., Phelps E.A. Lesions of the human amygdala impair enhanced perception of emotionally salient events. Nature 2001, 411:305-309.
67. De Martino B., et al. Enhanced processing of threat stimuli under limited attentional resources. Cereb. Cortex 2009, 19:127-133.
68. Morris J.S., et al. Human amygdala responses to fearful eyes. Neuroimage 2002, 17:214-222.
69. Dalgleish T. The emotional brain. Nat. Rev. Neurosci. 2004, 5:583-589.
70. Cahill L., et al. Enhanced human memory consolidation with post-learning stress: Interaction with the degree of arousal at encoding. Learn Mem. 2003, 10:270-274.
71. Lacey B.C., Lacey J.I. Two-way communication between the heart and the brain. Significance of time within the cardiac cycle. Am. Psychol. 1978, 33:99-113.
72. Vuilleumier P., et al. Distinct spatial frequency sensitivities for processing faces and emotional expressions. Nat. Neurosci. 2003, 6:624-631.
73. Robbins T.W., Arnsten A.F.T. The neuropsychopharmacology of fronto-executive function: monoaminergic modulation. Annu. Rev. Neurosci. 2009, 32:267-287.
74. Berntson G.G., et al. Ascending visceral regulation of cortical affective information processing. Eur. J. Neurosci. 2003, 18:2103-2109.
75. Nieuwenhuis S., et al. The role of the locus coeruleus in mediating the attentional blink: a neurocomputational theory. J. Exp. Psychol. Gen. 2005, 134:291-307.
76. De Martino B., et al. Noradrenergic neuromodulation of human attention for emotional and neutral stimuli. Psychopharmacology 2008, 197:127-136.
77. McGaugh J.L., et al. Involvement of the amygdala in memory storage: interaction with other brain systems. Proc. Natl. Acad. Sci. U.S.A. 1996, 93:13508-13514.
78. Arieli A., et al. Dynamics of ongoing activity: explanation of the large variability in evoked cortical responses. Science 1996, 273:1868-1871.
79. Schroeder C.E., Lakatos P. Low-frequency neuronal oscillations as instruments of sensory selection. Trends Neurosci. 2009, 32:9-18.
80. Landau A.N., Fries P. Attention samples stimuli rhythmically. Curr. Biol. 2012, 22:1000-1004.
81. Luo H., et al. Neural response phase tracks how listeners learn new acoustic representations. Curr. Biol. 2013, 23:968-974.
82. Sadaghiani S., et al. Distributed and antagonistic contributions of ongoing activity fluctuations to auditory stimulus detection. J. Neurosci. 2009, 29:13410-13417.
83. Hesselmann G., et al. Ongoing activity fluctuations in hMT plus bias the perception of coherent visual motion. J. Neurosci. 2008, 28:14481-14485.
84. Hesselmann G., et al. Spontaneous local variations in ongoing neural activity bias perceptual decisions. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:10984-10989.
85. Boly M., et al. Baseline brain activity fluctuations predict somatosensory perception in humans. Proc. Natl. Acad. Sci. U.S.A. 2007, 104:12187-12192.
86. Fox M.D., et al. Intrinsic fluctuations within cortical systems account for intertrial variability in human Behavior. Neuron 2007, 56:171-184.
87. Seth A.K. Interoceptive inference, emotion, and the embodied self. Trends Cogn. Sci. 2013, 17:565-573.
88. Tsakiris M., et al. Having a body versus moving your body: how agency structures body-ownership. Conscious. Cogn. 2006, 15:423-432.
89. Tajadura-Jimenez A., Tsakiris M. Balancing the 'inner' and the 'outer' self: interoceptive sensitivity modulates self-other boundaries. J. Exp. Psychol. Gen. 2014, 143:736-744.
90. Aspell J.E., et al. Keeping in touch with one's self: multisensory mechanisms of self-consciousness. PLoS One 2009, 4:e6488.
91. Friston K.J., et al. The anatomy of choice: active inference and agency. Front. Hum. Neurosci. 2013, 7. article 598.
92. Seth A.K., Critchley H.D. Extending predictive processing to the body: Emotion as interoceptive inference. Behav. Brain Sci. 2013, 36:227-228.
93. Gu X.S., et al. Anterior insular cortex and emotional awareness. J. Comp. Neurol. 2013, 521:3371-3388.
94. Barrett L.F., Simmons W.K. Interoceptive predictions in the brain. Nat. Rev. Neurosci. 2015, 16:419-429.
95. Clark D.M., et al. Misinterpretation of body sensations in panic disorder. J. Consult. Clin. Psychol. 1997, 65:203-213.
96. Teachman B.A., et al. Catastrophic misinterpretations as a predictor of symptom change during treatment for panic disorder. J. Consult. Clin. Psychol. 2010, 78:964-973.
97. Ehlers A., et al. Anxiety induced by false heart-rate feedback in patients with panic disorder. Behav. Res. Ther. 1988, 26:1-11.
98. Olesen J., et al. The economic cost of brain disorders in Europe. Eur. J. Neurol. 2012, 19:155-162.
99. Garfinkel S.N., Critchley H.D. Neural correlates of fear: insights from neuroimaging. Neurosci. Neuroeconom. 2014, 3:111-125.
100. Gianaros P.J., et al. Brain systems for baroreflex suppression during stress in humans. Hum. Brain Mapp. 2012, 33:1700-1716.
101. Mancia G., Mark A.L. Arterial baroreflexes in humans. Comprehensive Physiology (Suppl. 8): Handbook of Physiology, The Cardiovascular System, Peripheral Circulation and Organ Blood Flow 1983, 755-793. Wiley.
102. Cahill L., McGaugh J.L. Mechanisms of emotional arousal and lasting declarative memory. Trends Neurosci. 1998, 21:294-299.
103. Dolcos F., Cabeza R. Event-related potentials of emotional memory: encoding pleasant, unpleasant, and neutral pictures. Cogn. Affect. Behav. Neurosci. 2002, 2:252-263.
104. Kensinger E.A., Corkin S. Memory enhancement for emotional words: are emotional words more vividly remembered than neutral words?. Mem. Cognit. 2003, 31:1169-1180.
105. Bradley M.M., et al. Remembering pictures: pleasure and arousal in memory. J. Exp. Psychol. Learn. Mem. Cogn. 1992, 18:379-390.
106. Clark K.B., et al. Enhanced recognition memory following vagus nerve stimulation in human subjects. Nat. Neurosci. 1999, 2:94-98.
107. Critchley H.D., et al. Vagus nerve stimulation for treatment-resistant depression: behavioral and neural effects on encoding negative material. Psychosom. Med. 2007, 69:17-22.
108. Heims H.C., et al. Cognitive functioning in orthostatic hypotension due to pure autonomic failure. Clin. Auton. Res. 2006, 16:113-120.
109. Nogueira P.J.C., et al. Contribution of the vagus nerve in mediating the memory-facilitating effects of substance P. Behav. Brain Res. 1994, 62:165-169.
110. Williams C.L., Mcgaugh J.L. Reversible lesions of the nucleus of the solitary tract attenuate the memory-modulating effects of posttraining epinephrine. Behav. Neurosci. 1993, 107:955-962.
111. Damasio A.R. The somatic marker hypothesis and the possible functions of the prefrontal cortex. Philos. Trans. R. Soc. Lond. B: Biol. Sci. 1996, 351:1413-1420.
112. Werner N.S., et al. Enhanced cardiac perception is associated with benefits in decision-making. Psychophysiology 2009, 46:1123-1129.
113. Katkin E.S., et al. Nonconscious fear conditioning, visceral perception, and the development of gut feelings. Psychol. Sci. 2001, 12:366-370.