From the heart to the mind: Cardiac vagal tone modulates top-down and bottom-up visual perception and attention to emotional stimuli

Frontiers in Psychology

Volumn 5, Issue MAY, 2014, Pages

  Park, Gewnhi ^a   Thayer, Julian F ^b  

^a AZUSA PACIFIC UNIVERSITY   (United States)

^b OHIO STATE UNIVERSITY   (United States)

Author keywords

Attention; Cardiac vagal tone; Emotion regulation; Perception; Spatial frequency

Indexed keywords

EID: 84904571085     PISSN: None     EISSN: 16641078     Source Type: Journal    
DOI: 10.3389/fpsyg.2014.00278     Document Type: Review

References (80)

1. Ahern, G. L., Sollers, J. J., Lane, R. D., Labiner, D. M., Herring, A. M., Weinand, M. E., et al. (2001). Heart rate and heart rate variability changes in the intracarotid sodium amobarbital (ISA) test. Epilepsia 42, 912-921. doi: 10.1046/j.1528-1157.2001.042007912.x
2. Bär, K.-J., Berger, S., Metzner, M., Boettger, M. K., Schulz, S. C., Ramachandraiah, C. T., et al. (2009). Autonomic dysfunction in unaffected first-degree relatives of patients suffering from schizophrenia. Schizophr. Bull. 36, 1050-1058. doi: 10.1093/schbul/sbp024
3. Bär, K.-J., Wernich, K., Boettger, S., Cordes, J., Boettger, M. K., Loffler, S., et al. (2008). Relationship between cardiovagal modulation and psychotic state in patients with paranoid schizophrenia. Psychiatry Res. 157, 255-257. doi: 10.1016/j.psychres.2007.04.021
4. Bartolomeo, P., Sieroff, E., Decaix, C., and Chokron, S. (2001). Modulating the attentional bias in unilateral neglect: the effects of the strategic set. Exp. Brain Res. 137, 432-444. doi: 10.1007/s002210000642
5. Beauchaine, T. P., and Gatzke-Kopp, L., and Mead, H. K. (2007). Polyvagal theory and development psychopathology: emotion dysregulation and conduct problems from preschool to adolescence. Biol. Psychol. 74, 174-184. doi: 10.1016/j.biopsycho.2005.08.008
6. Benarroch, E. (1993). The central autonomic network: functional organization, dysfunction, and perspective. Mayo Clin. Proc. 68, 988-1001. doi: 10.1016/S0025-6196(12)62272-1
7. Berger, A., Henik, A., and Rafal, R. (2005). Competition between endogenous and exogenous orienting of visual attention. J. Exp. Psychol. Gen. 134, 207-221. doi: 10.1037/0096-3445.134.2.207
8. Butler, E. A., Wilhelm, F. H., and Gross, J. J. (2006). Respiratory sinus arrhythmia, emotion, and emotion regulation during social interaction. Psychophysiology 43, 612-622. doi: 10.1111/j.1469-8986.2006.00467.x
9. Callicott, J. H., Mattay, V. S., Verchinski, B. A., Marenco, S., Egan, M. F., and Weinberger, D. R. (2003). Complexity of prefrontal cortical dysfunction in schizophrenia: more than up or down. Am. J. Psychiatry 160, 2209-2215. doi: 10.1176/appi.ajp.160.12.2209
10. Castro, M. N., Vigo, D. E., Weidema, H., Fahrer, R. D., Chu, E. M., Achaval, D., et al. (2008). Heart rate variability response to mental arithmetic stress in patients with schizophrenia: autonomic response to stress in schizophrenia. Schizophr. Res. 99, 294-303. doi: 10.1016/j.schres.2007.08.025
11. Cisler, J. M., and Koster, E. H. W. (2010). Mechanisms of attentional biases towards threat in anxiety disorders: an integrative review. Clin. Psychol. Rev. 30, 203-216. doi: 10.1016/j.cpr.2009.11.003
12. Coull, J. T., Frith, C. D., Buchel, C., and Nobre, A. C. (2000). Orienting attention in time: behavioral and neuroanatomical distinction between exogenous and endogenous shifts. Neuropsychologia 38, 808-819. doi: 10.1016/S0028-3932(99)00132-3
13. Darwin, C. (1872). The Expression of Emotions in Man and Animals. London: John Murray.
14. Davidson, R. J., Pizzagalli, D., Nitschke, J. B., and Putnam, K. (2002). Depression: perspectives from affective neuroscience. Annu. Rev. Psychol. 53, 545-574. doi: 10.1146/annurev.psych.53.100901.135148
15. Edwards, J., Jackson, H. J., and Pattison, P. E. (2002). Emotion recognition via facial expression and affective prosody in schizophrenia: a methodological review. Clin. Psychol. Rev. 22, 789-832. doi: 10.1016/S0272-7358(02)00130-7
16. Ellis, R. J., and Thayer, J. F. (2010). Music and autonomic nervous system (dys)function. Music Percept. 27, 317-326. doi: 10.1525/mp.2010.27.4.317
17. El-Sheikh, M., Hinnant, J. B., and Erath, S. (2011). Developmental trajectories of delinquency symptoms in childhood: the role of marital conflict and autonomic nervous system activity. J. Abnorm. Psychol. 120, 16-32. doi: 10.1037/0012-1649.39.2.222
18. Fox, E., Russo, R., and Dutton, K. (2002). Attentional bias for threat: evidence for delayed disengagement from emotional faces. Cogn. Emot. 16, 355-379. doi: 10.1080/02699930143000527
19. Friedman, B. H. (2007). An autonomic flexibility-neurovisceral integration model of anxiety and cardiac vagal tone. Biol. Psychol. 74, 185-199. doi: 10.1016/j.biopsycho.2005.08.009
20. Friedman, B. H., and Thayer, J. F. (1998). Autonomic balance revisited: panic anxiety and heart rate variability. J. Psychosom. Res. 44, 133-151. doi: 10.1016/S0022-3999(97)00202-X
21. Gaebler, M., Danielsa, J. K., Lamkea, J.-P., Fydrichb, T., and Walter, H. (2013). Heart rate variability and its neural correlates during emotional face processing in social anxiety disorder. Biol. Psychol. 94, 319-330. doi: 10.1016/j.biopsycho.2013.06.009
22. Goffaux, V., Hault, B., Michel, C., Vuong, Q. C., and Rossion, B. (2005). The respective role of low and high spatial frequencies in supporting configural and featural processing of faces. Perception 34, 77-86. doi: 10.1068/p5370
23. Gross, J. J. (1998). Antecedent- and response-focused emotion regulation: divergent consequences for experience, expression, and physiology. J. Pers. Soc. Psychol. 74, 224-237. doi: 10.1037/0022-3514.74.1.224
24. Gross, J. J., and Thompson, R. A. (2007). "Emotion regulation: conceptual foundations," in Handbook of Emotion Regulation, ed. J. J. Gross (New York, NY: Guilford Press), 3-24.
25. Hansen, A. L., Johnsen, B. H., and Thayer, J. F. (2003). Vagal influence on working memory and attention. Int. J. Psychophysiol. 48, 263-274. doi: 10.1016/S0167-8760(03)00073-4
26. Heatherton, T. F., and Wagner, D. D. (2011). Cognitive neuroscience of self-regulation failure. Trends Cogn. Sci. 15, 132-139. doi: 10.1016/j.tics.2010.12.005
27. Holmes, A., Green, S., and Vuilleumier, P. (2005). The involvement of distinct visual channels in rapid attention towards fearful facial expressions. Cogn. Emot. 19, 899-922. doi: 10.1080/02699930441000454
28. Huang-Pollock, C. L., and Jigg, J. L. (2003). Searching for the attention deficit in attention deficit hyperactivity disorder: the case of visuospatial orienting. Clin. Psychol. Rev. 23, 801-830. doi: 10.1016/S0272-7358(03)00073-4
29. Johnstone, T., van Reekum, C. M., Urry, H. L., Kalin, N. H., and Davidson, R. J. (2007). Failure to regulate: counterproductive recruitment of top-down prefrontal-subcortical circuitry in major depression. J. Neurosci. 27, 8877-8884. doi: 10.1523/JNEUROSCI.2063-07.2007
30. Kim, M. J., and Whalen, P. J. (2009). The structural integrity of an amygdala-prefrontal pathway predicts trait anxiety. J. Neurosci. 29, 11614-11618. doi: 10.1523/JNEUROSCI.2335-09.2009
31. Klein, R. M., and MacInnes, W. J. (1999). Inhibition of return is a foraging facilitator in visual search. Psychol. Sci. 10, 346-352. doi: 10.1111/1467-9280.00166
32. Koster, E. H. W., Crombez, G., Verschuere, B., Damme, S. V., and Wiersema, J. R. (2006). Components of attentional bias to threat in high trait anxiety: facilitated engagement, impaired disengagement, and attentional avoidance. Behav. Res. Ther. 44, 1757-1771. doi: 10.1016/j.brat.2005.12.011
33. Lane, R. D., McRae, K., Reiman, E. M., Chen, K., Ahern, G. L., and Thayer, J. F. (2009). Neural correlates of heart rate variability during emotion. Neuroimage 44, 213-222. doi: 10.1016/j.neuroimage.2008.07.056
34. Lane, R. D., Weidenbacher, H., Smith R., Fort, C., Thayer, J. F., and Allen, J. J. B. (2013). Subgenual anterior cingulate cortex activity covariation with cardiac vagal control is altered in depression. J. Affect. Disord. 150, 565-570. doi: 10.1016/j.jad.2013.02.005
35. Lee, S. H., and Park, G. (2011). "Psychophysiological markers of anxiety disorders and anxiety symptoms," in Anxiety Disorders, ed. V. Kalinin (Rijeka: InTech), 203-226. Retrieved from: http://www.intechopen.com/books/anxiety-disorders/psychophysiologicalmarkers-of-anxiety-disorders-and-anxiety-symptoms
36. Levy, M. (1971). Sympathetic-parasympathetic interactions in the heart. Circ. Res. 29, 437-445. doi: 10.1161/01.RES.29.5.437
37. Lewis, D. A., Hashimoto, T., and Volk, D. W. (2005). Cortical inhibitory neurons and schizophrenia. Nat. Rev. Neurosci. 6, 312-324. doi: 10.1038/nrn1648
38. Li, C. S. R., and Sinha, R. (2008). Inhibitory control and emotional stress regulation: neuroimaging evidence for frontal-limbic dysfunction in psycho-stimulant addiction. Neurosci. Biobehav. Rev. 32, 581-597. doi: 10.1016/j.neubiorev.2007.10.003
39. Livingstone, M., and Hubel, D. (1988). Segregation of form, color, movement, and depth: anatomy, physiology, and perception. Science 240, 740-749. doi: 10.1126/science.3283936
40. Lyonfields, J. D., Borkovec, T. D., and Thayer, J. F. (1995). Vagal tone in generalized anxiety disorder and the effects of aversive imagery and worrisome thinking. Behav. Ther. 26, 457-466. doi: 10.1016/S0005-7894(05)80094-2
41. Mathews, A., Mackintosh, B., and Fulcher, E. P. (1997). Cognitive biases in anxiety and attention to threat. Trends Cogn. Sci. 1, 340-345. doi: 10.1016/S1364-6613(97)01092-9
42. Merigan, W. H., and Maunsell, J. H. R. (1993). How parallel are the primate visual pathways? Annu. Rev. Neurosci. 16, 369-402. doi: 10.1146/annurev.ne.16.030193.002101
43. Mermillod, M., Vuilleumier, P., Peyrin, C., Alleysson, D., and Merendaz, C. (2008). The importance of low spatial frequency information for recognizing fearful facial expressions. Conn. Sci. 21, 75-88. doi: 10.1080/09540090802213974
44. Morrison, D. J., and Schyns, P. G. (2001). Usage of spatial scales for the categorization of faces, objects, and scenes. Psychon. Bull. Rev. 8, 454-469. doi: 10.3758/BF03196180
45. Nieuwenhuis, S., Jepma, M., La Fors, S., and Olivers, C. N. L. (2008). The role of the magnocellular and parvocellular pathways in the attentional blink. Brain Cogn. 68, 42-48. doi: 10.1016/j.bandc.2008.02.119
46. Okon-Singer, H., Lichtenstein-Vidne, L., and Cohen, N. (2013). Dynamic modulation of emotional processing. Biol. Psychol. 92, 480-491. doi: 10.1016/j.biopsycho.2012.05.010
47. Park, G., Moon, E., Kim, D., and Lee, S. (2012a). Individual differences in cardiac vagal tone are related to neural responses to facial expressions at different spatial frequencies: an ERP and sLORETA study. Cogn. Affect. Behav. Neurosci. 12, 777-793. doi: 10.3758/s13415-012-0111-0
48. Park, G., Van Bavel, J. J., Egan, E. J. L., Vasey, M., and Thayer, J. F. (2012b). From the heart to the mind's eye: cardiac vagal tone is related to visual perception of fearful faces at high spatial frequency. Biol. Psychol. 90, 171-178. doi: 10.1016/j.biopsycho.2012.02.012
49. Park, G., Van Bavel, J. J., Vasey, M. W., and Thayer, J. F. (2012c). Cardiac vagal tone predicts inhibited attention to fearful faces. Emotion 12, 1292-1302. doi: 10.1037/a0028528
50. Park, G., Vasey, M., Van Bavel, J. J., and Thayer, J. F. (2013a). Cardiac vagal tone is correlated with selective attention to neutral distractors under load. Psychophysiology 50, 398-406. doi: 10.1111/psyp.12029
51. Park, G., Van Bavel, J. J., Vasey, M., and Thayer, J. F. (2013b). Cardiac vagal tone predicts attentional engagement to and disengagement from fearful faces. Emotion 13, 645-656. doi: 10.1037/a0032971
52. Park, G., Vasey, M., Van Bavel, J. J., and Thayer, J. F. (2014). When tonic cardiac vagal tone predicts changes in phasic vagal tone: the role of fear and perceptual load. Psychophysiology doi: 10.1111/psyp.12186 [Epub ahead of print].
53. Parker, D. M., Lishman, J. R., and Hughes, J. (1996). Role of course and fine spatial information in face and object processing. J. Exp. Psychol. Hum. Percept. Perform. 22, 1448-1466. doi: 10.1037/0096-1523.22.6.1448
54. Pessoa, L., and Adolphs, R. (2011). Emotion and the brain: multiple roads are better than one. Nat. Rev. Neurosci. 12, 425. doi: 10.1038/nrn2920-c2
55. Pittig, A., Arch, J. J., Lam, C. W., and Craske, M. G. (2013). Heart rate and heart rate variability in panic, social anxiety, obsessive-compulsive, and generalized anxiety disorders at baseline and in response to relaxation and hyperventilation. Int. J. Psychophysiol. 87, 19-20. doi: 10.1016/j.ijpsycho.2012.10.012
56. Posner, M. I., and Cohen, Y. A. (1984). "Components of visual orienting," in Attention and Performance, eds H. Bouma and D. G. Bouwhuis (Hillsdale, NJ: Erlbaum), 531-554.
57. Posner, M. I., and Peterson, S. E. (1990). The attention system of the human brain. Annu. Rev. Neurosci. 13, 25-42. doi: 10.1146/annurev.ne.13.030190.000325
58. Posner, M. I., Rafal, R. D., Choate, L. S., and Vaughan, J. (1985). Inhibition of return: neural basis and function. Cogn. Neuropsychol. 2, 211-228. doi: 10.1080/02643298508252866
59. Posner, M. I., and Rothbart, M. K. (2007). Networks as a model for the integration of psychological science. Annu. Rev. Psychol. 58, 1-23. doi: 10.1146/annurev.psych.58.110405.085516
60. Pourtois, G., Dan, E. S., Grandjean, D., Sander, D., and Vuilleumier, P. (2005). Two electrophysiological stages of spatial orienting towards fear faces: early temporo-parietal activation preceding gain control in extrastriate visual cortex. Neuroimage 26, 149-163. doi: 10.1016/j.neuroimage.2005.01.015
61. Pourtois, G., and Vuilleumier, P. (2006). Dynamics of emotional effects on spatial attention in the human visual cortex. Prog. Brain Res. 156, 67-91. doi: 10.1016/S0079-6123(06)56004-2
62. Rottenberg, J., Kasch, K. L., Gross, J. J., and Gotlib, I. H. (2002). Sadness and amusement reactivity differentially predict concurrent and prospective functioning in major depressive disorder. Emotion 2, 135-146. doi: 10.1037/1528-3542.2.2.135
63. Ruiz-Padial, E., Sollers, J. J., Vila, J., and Thayer, J. F. (2003). The rhythm of the heart in the blink of an eye: emotion-modulated startle magnitude covaries with heart rate variability. Psychophysiology 40, 306-313. doi: 10.1111/1469-8986.00032
64. Schyns, P. G., and Oliva, A. (1999). Dr. Angry and Mr. Smile: when categorization flexibly modifies the perception of faces in rapid visual presentations. Cognition 69, 243-265. doi: 10.1016/S0010-0277(98)00069-9
65. Segerstrom, S. C., and Nes, L. S. (2007). Heart rate variability reflects self-regulatory strength, effort, and fatigue. Psychol. Sci. 18, 275-281. doi: 10.1111/j.1467-9280.2007.01888.x
66. Stoyanova, R. S., Pratt, J., and Anderson, A. K. (2007). Inhibition of return to social signals of fear. Emotion 7, 49-56. doi: 10.1037/1528-3542.7.1.49
67. Sumner, P. (2006). Inhibition versus attentional momentum in cortical and collicular mechanisms of IOR. Cogn. Neuropsychol. 23, 1035-1048.
68. Task Force of the European Society of Cardiology, and the North American Society of Pacing, and Electrophysiology. (1996). Heart rate variability: standards of measurement, physiology interpretation, and clinical use. Circulation 93, 1043-1065. doi: 10.1080/02643290600588350
69. Taylor, T. L., and Therrien, M. E. (2005). Inhibition of return for faces. Percept. Psychophys. 67, 1414-1422. doi: 10.3758/BF03193646
70. Thayer, J. F., Åhs, F., Fredrikson, M., Sollers, J. J. III, and Wager, T. D. (2012). A meta-analysis of heart rate variability and neuroimaging studies: implications for heart rate variability as a marker of stress and health. Neurosci. Biobehav. Rev. 36, 747-756. doi: 10.1016/j.neubiorev.2011.11.009
71. Thayer, J. F., Friedman, B. H., and Borkovec, T. D. (1996). Autonomic characteristics of generalized anxiety disorder and worry. Biol. Psychiatry 39, 255-266. doi: 10.1016/0006-3223(95)00136-0
72. Thayer, J. F., Hansen, A. L., Saus-Rose, E., and Johnsen, B. H. (2009). Heart rate variability, prefrontal neural function and cognitive performance: the neurovisceral integration perspective on self-regulation, adaptation, and health. Ann. Behav. Med. 37, 141-153. doi: 10.1007/s12160-009-9101-z
73. Thayer, J. F., and Lane, R. D. (2000). A model of neurovisceral integration in emotion regulation and dysregulation. J. Affect. Disord. 61, 201-216. doi: 10.1016/S0165-0327(00)00338-4
74. Thayer, J. F., and Lane, R. D. (2002). Perseverative thinking and health: neurovisceral concomitants. Psychol. Health 17, 685-695. doi: 10.1080/08870440290025867
75. Verkuil, B., Brosschot, J. E., Putman, P., and Thayer, J. F. (2009). Interacting effects of worry and anxiety on attentional disengagement from threat. Behav. Res. Ther. 47, 146-152. doi: 10.1016/j.brat.2008.11.003
76. Vuilleumier, P. (2005). How brains beware: neutral mechanisms of emotional attention. Trends Cogn. Sci. 9, 585-594. doi: 10.1016/j.tics.2005.10.011
77. Vuilleumier, P., Armony, J. L., Driver, J., and Dolan, R. J. (2003). Distinct spatial frequency sensitivities for processing faces and emotional expressions. Nat. Neurosci. 6, 624-631. doi: 10.1038/nn1057
78. Vuilleumier, P., and Brosch, T. (2009). "Interactions of emotion and attention," in The Cognitive Neurosciences IV, ed. M. S. Gazzaniga (Cambridge, MA MIT Press), 925-934.
79. Weber, C. S., Thayer, J. F., Rudat, M., Wirtz, P. H., Zimmermann-Viehoff, F., Thomas, A., et al. (2010). Low vagal tone is associated with impaired post stress recovery of cardiovascular, endocrine, and immune markers. Eur. J. Appl. Physiol. 109, 201-211. doi: 10.1007/s00421-009-1341-x
80. Winston, J. S., Vuilleumier, P., and Dolan, R. (2003). Effects of low-spatial frequency components of fearful faces on fusiform cortex activity. Curr. Biol. 13, 1824-1829. doi: 10.1016/j.cub.2003.09.038