Neural correlates of the behavioral-autonomic interaction response to potentially threatening stimuli

Frontiers in Human Neuroscience

Volumn , Issue JAN, 2013, Pages

  Farrow, Tom F D ^a   Johnson, Naomi K ^a   Hunter, Michael D ^a   Barker, Anthony T ^b   Wilkinson, Iain D ^a   Woodruff, Peter W R ^a  

^a UNIVERSITY OF SHEFFIELD   (United Kingdom)

^b SHEFFIELD TEACHING HOSPITALS NHS FOUNDATION TRUST   (United Kingdom)

Author keywords

Affective tone; Autonomic arousal; Emotional salience; Functional magnetic resonance imaging (fMRI); Skin conductance response (SCR); Threat

Indexed keywords

ADULT; ANTERIOR CINGULATE; AROUSAL; ARTICLE; AUDITORY STIMULATION; AUTONOMIC NERVOUS SYSTEM FUNCTION; BEHAVIORAL SCIENCE; BRAIN CORTEX; BRAIN FUNCTION; BRAIN REGION; ELECTRODERMAL RESPONSE; FACTORIAL ANALYSIS; FRONTAL CORTEX; FUNCTIONAL MAGNETIC RESONANCE IMAGING; FUSIFORM GYRUS; HESCHL GYRUS; HUMAN; HUMAN EXPERIMENT; INSULA; MALE; NERVE PROJECTION; NERVE STIMULATION; NEUROPSYCHOLOGICAL TEST; NEUROPSYCHOLOGY; NORMAL HUMAN; PARAHIPPOCAMPAL GYRUS; PARIETOOCCIPITOTHALAMIC REGION; PHOTOGRAPHY; PRECUNEUS; PSYCHOAUTONOMIC INTERACTION; STIMULUS RESPONSE; TEMPORAL GYRUS; THREAT; VISUAL STIMULATION;

EID: 84933675947     PISSN: 16625161     EISSN: 16625161     Source Type: Journal    
DOI: 10.3389/fnhum.2012.00349     Document Type: Article

References (91)

1. Allen, P., Freeman, D., and McGuire, P. (2007). Slow habituation of arousal associated with psychosis proneness. Psychol. Med. 37, 577-582.
2. Anders, S., Lotze, M., Erb, M., Grodd, W., and Birbaumer, N. (2004). Brain activity underlying emotional valence and arousal: a responserelated fMRI study. Hum. Brain Mapp. 23, 200-209.
3. Ashburner, J., and Friston, K. J. (2005). Unified segmentation. Neuroimage 26, 839-851.
4. Baron-Cohen, S., and Wheelwright, S. (2004). The empathy quotient: an investigation of adults with Asperger syndrome or high functioning autism, and normal sex differences. J. Autism Dev. Disord. 34, 163-175.
5. Benedek, M., and Kaernbach, C. (2010a). A continuous measure of phasic electrodermal activity. J. Neurosci. Methods 190, 80-91.
6. Benedek, M., and Kaernbach, C. (2010b). Decomposition of skin conductance data by means of nonnegative deconvolution. Psychophysiology 47, 647-658.
7. Bertolino, A., Arciero, G., Rubino, V., Latorre, V., De Candia, M., Mazzola, V., et al. (2005). Variation of human amygdala response during threatening stimuli as a function of 5'HTTLPR genotype and personality style. Biol. Psychiatry 57, 1517-1525.
8. Bishop, S. J., Duncan, J., and Lawrence, A. D. (2004). State anxiety modulation of the amygdala response to unattended threatrelated stimuli. J. Neurosci. 24, 10364-10368.
9. Blackford, J. U., Buckholtz, J. W., Avery, S., and Zald, D. H. (2010). A unique role for the human amygdala in novelty detection. Neuroimage 50, 1188-1193.
10. Blackwood, N. J., Howard, R. J., ffytche, D. H., Simmons, A., Bentall, R. P., and Murray, R. M. (2000). Imaging attentional and attributional bias: an fMRI approach to paranoid delusions. Psychol. Med. 30, 873-883.
11. Blood, A. J., Zatorre, R. J., Bermudez, P., and Evans, A. C. (1999). Emotional responses to pleasant and unpleasant music correlate with activity in paralimbic brain regions. Nat. Neurosci. 2, 382-387.
12. Bradley, M. M., and Lang, P. J. (1999). International Affective Digitized Sounds (IADS): Stimuli, Instruction Manual and Affective Ratings. The Center for Research in Psychophysiology. Gainesville, FL: University of Florida.
13. Bradley, M. M., Codispoti, M., Cuthbert, B. N., and Lang, P. J. (2001). Emotion and motivation I: defensive and appetitive reactions in picture processing. Emotion 1, 276-298.
14. Braunstein-Bercovitz, H. (2000). Is the attentional dysfunction in schizotypy related to anxiety? Schizophr. Res. 46, 255-267.
15. Britton, J. C., Taylor, S. F., Sudheimer, K. D., and Liberzon, I. (2006). Facial expressions and complex IAPS pictures: common and differential networks. Neuroimage 31, 906-919.
16. Bryant, R. A., Kemp, A. H., Felmingham, K. L., Liddell, B., Olivieri, G., Peduto, A., et al. (2008). Enhanced amygdala and medial prefrontal activation during nonconscious processing of fear in posttraumatic stress disorder: an fMRI study. Hum. Brain Mapp. 29, 517-523.
17. Bush, G., Luu, P., and Posner, M. I. (2000). Cognitive and emotional influences in anterior cingulate cortex. Trends Cogn. Sci. 4, 215-222.
18. Butler, T., Pan, H., Tuescher, O., Engelien, A., Goldstein, M., Epstein, J., et al. (2007). Human fear-related motor neurocircuitry. Neuroscience 150, 1-7.
19. Calder, A. J., Lawrence, A. D., and Young, A. W. (2001). Neuropsychology of fear and loathing. Nat. Rev. Neurosci. 2, 352-363.
20. Cloitre, M., Heimberg, R. G., Holt, C. S., and Liebowitz, M. R. (1992). Reaction time to threat stimuli in panic disorder and social phobia. Behav. Res. Ther. 30, 609-617.
21. Coccaro, E. F., Noblett, K. L., and McCloskey, M. S. (2009). Attributional and emotional responses to socially ambiguous cues: validation of a new assessment of social/emotional information processing in healthy adults and impulsive aggressive patients. J. Psychiatr. Res. 43, 915-925.
22. Cohen, A. S., and Minor, K. S. (2010). Emotional experience in patients with schizophrenia revisited: meta-analysis of laboratory studies. Schizophr. Bull. 36, 143-150.
23. Compton, R. J., Banich, M. T., Mohanty, A., Milham, M. P., Herrington, J., Miller, G. A., et al. (2003). Paying attention to emotion: an fMRI investigation of cognitive and emotional stroop tasks. Cogn. Affect. Behav. Neurosci. 3, 81-96.
24. Corbetta, M., and Shulman, G. L. (2002). Control of goal-directed and stimulus driven attention in the brain. Nat. Rev. Neurosci. 3, 201-215.
25. Craig, A. D. (2003). Interoception: the sense of the physiological condition of the body. Curr. Opin. Neurobiol. 13, 500-505.
26. Craig, A. D. (2009). How do you feel now? The anterior insula and human awareness. Nat. Rev. Neurosci. 10, 59-70.
27. Critchley, H. D. (2009). Psychophysiology of neural, cognitive and affective integration: fMRI and autonomic indicants. Int. J. Psychophysiol. 73, 88-94.
28. Critchley, H. D., Elliot, R., Mathias, C. J., and Dolan, R. J. (2000). Neural activity relating to generation and representation of galvanic skin conductance responses: a functional magnetic resonance imaging study. J. Neurosci. 20, 3033-3040.
29. Critchley, H. D., Mathias, C. J., Josephs, O., O'Doherty, J., Zanini, S., Dewar, B. K., et al. (2003). Human cingulate cortex and autonomic control: converging neuroimaging and clinical evidence. Brain 126, 2139-2152.
30. Critchley, H. D., Wiens, S., Rotshtein, P., Öhman, A., and Dolan, R. J. (2004). Neural systems supporting interoceptive awareness. Nat. Neurosci. 7, 189-195.
31. Dalton, K. M., Kalin, N. H., Grist, T. M., and Davidson, R. J. (2005). Neural-cardiac coupling in threatevoked anxiety. J. Cogn. Neurosci. 17, 969-980.
32. Digman, J. M. (1990). Personality structure: emergence of the five factor model. Annu. Rev. Psychol. 41, 417-440.
33. Di Salle, F., Esposito, F., Scarabino, T., Formisano, E., Marciano, E., Saulino, C., et al. (2003). FMRI of the auditory system: understanding the neural basis of auditory gestalt. Magn. Reson. Imaging 21, 1213-1224.
34. Drabant, E. M., Kuo, J. R., Ramel, W., Blechert, J., Edge, M. D., Cooper, J. R., et al. (2011). Experiential, autonomic, and neural responses during threat anticipation vary as a function of threat intensity and neuroticism. Neuroimage 55, 401-410.
35. Eden, G. F., Joseph, J. E., Brown, H. E., Brown, C. P., and Zeffiro, T. A. (1999). Utilizing hemodynamic delay and dispersion to detect fMRI signal change without auditory interference: the behaviour interleaved gradients technique. Magn. Reson. Med. 41, 13-20.
36. Eldar, E., Ganor, O., Admon, R., Bleich, A., and Hendler, T. (2007). Feeling the real world: limbic response to music depends on related content. Cereb. Cortex 17, 2828-2840.
37. Estes, Z., and Verges, M. (2008). Freeze or flee? Negative stimuli elicit selective responding. Cognition 108, 557-565.
38. Fredrikson, M., Furmark, T., Olsson, M. T., Fischer, H., Andersson, J., and Långstrom, B. (1998). Functional neuroanatomical correlates of electrodermal activity: a positron emission tomographic study. Psychophysiology 35, 179-185.
39. Gard, D. E., and Kring, A. M. (2009). Emotion in the daily lives of schizophrenia patients: context matters. Schizophr. Res. 115, 379-380.
40. Garrett, A. S., and Maddock, R. J. (2006). Separating subjective emotion from the perception of emotion-inducing stimuli: an fMRI study. Neuroimage 33, 263-274.
41. Grimm, S., Schmidt, C. F., Bermpohl, F., Heinzel, A., Dahlem, Y., Wyss, M., et al. (2006). Segregated neural representation of distinct emotion dimensions in the prefrontal cortex-an fMRI study. Neuroimage 30, 325-340.
42. Heinzel, A., Bermpohl, F., Niese, R., Pfennig, A., Pascual-Leone, A., Schlaug, G., et al. (2005). How do we modulate our emotions? Parametric fMRI reveals cortical midline structures as regions specifically involved in the processing of emotional valences. Brain Res. Cogn. Brain Res. 25, 348-358.
43. Henderson, L. A., Stathis, A., James, C., Brown, R., McDonald, S., and Macefield, V. G. (2012). Real-time imaging of cortical areas involved in the generation of increases in skin sympathetic nerve activity when viewing emotionally charged images. Neuroimage 62, 30-40.
44. Horan, W. P., Blanchard, J. J., Clark, L. A., and Green, M. F. (2008). Affective traits in schizophrenia and schizotypy. Schizophr. Bull. 34, 856-874.
45. Hugdahl, K. (1996). Cognitive influences on human autonomic nervous system function. Curr. Opin. Neurobiol. 6, 252-258.
46. Isenberg, N., Silbersweig, D., Engelien, A., Emmerich, S., Malavadek, K., Beattie, B., et al. (1999). Linguistic threat activates the human amygdala. Proc. Natl. Acad. Sci. U.S.A. 96, 10456-10459.
47. Johnston, S. J., Boehm, S. G., Healy, D., Goebel, R., and Linden, D. E. J. (2010). Neurofeedback: a promising tool for the self-regulation of emotion networks. Neuroimage 49, 1066-1072.
48. Katkin, E. S., Wiens, S., and Öhman, A. (2001). Nonconscious fear conditioning: visceral perception and the development of gut feelings. Psychol. Sci. 12, 366-370.
49. Kemp, A. H., Felmingham, K. L., Falconer, E., Liddell, B. J., Bryant, R. A., and Williams, L. M. (2009). Heterogeneity of non-conscious fear perception in posttraumatic stress disorder as a function of physiological arousal: an fMRI study. Psychiatry Res. 174, 158-161.
50. Kesler-West, M. L., Andersen, A. H., Smith, C. D., Avison, M. J., Davis, C. E., Kryscio, R. J., et al. (2001). Neural substrates of facial emotion processing using fMRI. Brain Res. Cogn. Brain Res. 11, 213-226.
51. Koelsch, S., Fritz, T., Cramon, D. Y. V., Müller, K., and Friederici, A. D. (2005). Investigating emotion with music: an fMRI study. Hum. Brain Mapp. 27, 239-250.
52. Kret, M. E., Denollet, J., Grèzes, J., and de Gelder, B. (2011). The role of negative affectivity and social inhibition in perceiving social threat: an fMRI study. Neuropsychologia 49, 1187-1193.
53. Lang, P. J., Bradley, M. M., and Cuthbert, B. N. (1997). The International Affective Picture System. NIMH Center for the Study of Emotion and Attention. Gainesville, FL: University of Florida.
54. Lee, G. P., Meador, K. J., Loring, D. W., Allison, J. D., Brown, W. S., Paul, L. K., et al. (2004). Neural substrates of emotion as revealed by functional magnetic resonance imaging. Cogn. Behav. Neurol. 17, 9-17.
55. Lieberman, M. D., and Cunningham, W. A. (2009). Type I and Type II error concerns in fMRI research: rebalancing the scale. Soc. Cogn. Affect. Neurosci. 4, 423-428.
56. Lindquist, K. A., Wager, T. D., Kober, H., Bliss-Moreau, E., and Feldman Barrett, L. (2012). The brain basis of emotion: a meta-analytic review. Behav. Brain Sci. 35, 121-202.
57. Malach, R., Levy, I., and Hasson, U. (2002). The topography of highorder human object areas. Trends Cogn. Sci. 6, 176-184.
58. Mardaga, S., Laloyaux, O., and Hansenne, M. (2006). Personality traits modulate skin conductance response to emotional pictures: an investigation with Cloninger's model of personality. Pers. Individ. Diff. 40, 1603-1614.
59. Martin, J. A., and Penn, D. L. (2001). Social cognition and subclinical paranoid ideation. Br. J. Clin. Psychol. 40, 261-265.
60. Mason, O., and Claridge, G. (2006). The Oxford-Liverpool Inventory of Feelings and Experiences (O-LIFE): further description and extended norms. Schizophr. Res. 82, 203-211.
61. Mason, O., Claridge, G., and Jackson, M. (1995). New scales for the assessment of schizotypy. Pers. Individ. Diff. 18, 7-13.
62. Mazziotta, J., Toga, A., Evans, A., Fox, P., Lancaster, J., Zilles, K., et al. (2001). A probabilistic atlas and reference system for the human brain: International Consortium for Brain Mapping (ICBM). Philos. Trans. R. Soc. Lond. B Biol. Sci. 356, 1293-1322.
63. Napadow, V., Dhond, R., Conti, G., Makris, N., Brown, E. N., and Barbieri, R. (2008). Brain correlates of autonomic modulation: combining heart rate variability with fMRI. Neuroimage 42, 169-177.
64. Narumoto, J., Okada, T., Sadato, N., Fukui, K., and Yonekura, Y. (2001). Attention to emotion modulates fMRI activity in human right superior temporal sulcus. Brain Res. Cogn. Brain Res. 12, 225-231.
65. Nelson, H. E. (1982). National Adult Reading Test. Windsor, UK: NFERNelson.
66. Northoff, G., Heinzel, A., Bermpohl, F., Niese, R., Pfennig, A., PascualLeone, A., et al. (2004). Reciprocal modulation and attenuation in the prefrontal cortex: an fMRI study on emotional-cognitive interaction. Hum. Brain Mapp. 21, 202-212.
67. Öhman, A., Flykt, A., and Esteves, F. (2001a). Emotion drives attention: detecting the snake in the grass. J. Exp. Psychol. Gen. 130, 466-478.
68. Öhman, A., Lundqvist, D., and Esteves, F. (2001b). The face in the crowd revisited: a threat advantage with schematic stimuli. J. Pers. Soc. Psychol. 80, 381-396.
69. Öhman, A., Hamm, A., and Hugdahl, K. (2000). "Cognition and the autonomic nervous system: Orienting, anticipation and conditioning," in Principles of Psychophysiology: Physical, Social and Inferential Elements, eds J. T. Cacioppo and L. G. Tassinary (Cambridge, England: Cambridge University Press), 533-576.
70. Pallesen, K. J., Brattico, E., Bailey, C., Korvenoja, A., Koivisto, J., Gjedde, A., et al. (2005). Emotion processing of major, minor, and dissonant chords: a functional magnetic resonance imaging study. Ann. N.Y. Acad. Sci. 1060, 450-453.
71. Patterson, J. C., Ungerleider, L. G., and Bandettini, P. A. (2002). Task-independent functional brain activity correlation with skin conductance changes: an fMRI study. Neuroimage 17, 1797-1806.
72. Peer, J. E., Rothmann, T. L., Penrod, R. D., Penn, D. L., and Spaulding, W. D. (2004). Social cognitive bias and neurocognitive deficit in paranoid symptoms: evidence for an interaction effect and changes during treatment. Schizophr. Res. 71, 463-471.
73. Plichta, M. M., Gerdes, A. B., Alpers, G. W., Harnisch, W., Brill, S., Wieser, M. J., et al. (2011). Auditory cortex activation is modulated by emotion: a functional near-infrared spectroscopy (fNIRS) study. Neuroimage 55, 1200-1207.
74. Premkumar, P., Cooke, M. A., Fannon, D., Peters, E., Michel, T. M., Aasen, I., et al. (2008). Misattribution bias of threat-related facial expressions is related to a longer duration of illness and poor executive function in schizophrenia and schizoaffective disorder. Eur. Psychiatry 23, 14-19.
75. Rawlings, D., and Freeman, J. L. (1996). A questionnaire for the measurement of paranoia/suspiciousness. Br. J. Clin. Psychol. 35, 451-461.
76. Richards, J. C., Cooper, A. J., and Winkelman, J. H. (2003). Interoceptive accuracy in nonclinical panic. Cogn. Ther. Res. 27, 447-461.
77. Ross, E. D. (1997). "Cortical representation of emotions," in Behavioural Neurology, eds M. Timble and J. Cummings (Oxford: ButterworthHeinemann), 107-126.
78. Shackman, A. J., Salomons, T. V., Slagter, H. A., Fox, A. S., Winter, J. J., and Davidson, R. J. (2011). The integration of negative affect, pain and cognitive control in the cingulate cortex. Nat. Rev. Neurosci. 12, 154-167.
79. Shastri, A., Lomarev, M. P., Nelson, S. J., George, M. S., Holzwarth, M. R., and Bohning, D. E. (2001). A low-cost system for monitoring skin conductance during functional MRI. J. Magn. Reson. Imaging 14, 187-193.
80. Simmons, A., Strigo, I., Matthews, S. C., Paulus, M. P., and Stein, M. B. (2006). Anticipation of aversive visual stimuli is associated with increased insula activation in anxiety-prone subjects. Biol. Psychiatry 60, 402-409.
81. Singer, T., Critchley, H. D., and Preuschoff, K. (2009). A common role of insula in feelings, empathy and uncertainty. Trends Cogn. Sci. 13, 334-340.
82. Talairach, J., and Tournoux, P. (1988). Co-planar Stereotactic Atlas of the Human Brain. Stuttgart: ThiemeVerlag.
83. Tsao, D. Y., Freiwald, W. A., Tootell, R. B. H., and Livingstone, M. S. (2006). A cortical region consisting entirely of face-selective cells. Science 311, 670-674.
84. Tsao, D. Y., and Livingston, M. S. (2008). Mechanisms of face perception. Annu. Rev. Neurosci. 31, 411-437.
85. VaezMousavi, S. M., Barry, R. J., Rushby, J. A., and Clarke, A. R. (2007). Evidence for differentiation of arousal and activation in normal adults. Acta. Neurobiol. Exp. 67, 179-186.
86. van Os, J., Linscott, R. J., MyinGermeys, I., Delespaul, P., and Krabbendam, L. (2009). A systematic review and meta-analysis of the psychosis continuum: evidence for a psychosis pronenesspersistence-impairment model of psychotic disorder. Psychol. Med. 39, 179-195.
87. Vuilleumier, P., Armony, J. L., Driver, J., and Dolan, R. J. (2001). Effects of attention and emotion on face processing in the human brain: an event-related fMRI study. Neuron 30, 829-841.
88. Wallin, B. G. (1981). Sympathetic nerve activity underlying electrodermal and cardiovascular reactions in man. Psychophysiology 18, 470-476.
89. Williams, L. M., Brammer, M. J., Skerrett, D., Lagopolous, J., Rennie, C., Kozek, K., et al. (2000). The neural correlates of orienting: an integration of fMRI and skin conductance orienting. Neuroreport 11, 3011-3015.
90. Wout, M., Aleman, A., Kessels, R. P. C., Larøi, F., and Kahn, R. S. (2004). Emotional processing in a non-clinical psychosisprone sample. Schizophr. Res. 68, 271-281.
91. Zhang, S., Hu, S., Chao, H. H., Luo, X., Farr, O. M., and Li, C. S. (2012). Cerebral correlates of skin conductance responses in a cognitive task. Neuroimage 62, 1489-1498.