Skip to main content
Log in

Utilizing Heartbeat Evoked Potentials to Identify Cardiac Regulation of Vagal Afferents During Emotion and Resonant Breathing

  • Published:
Applied Psychophysiology and Biofeedback Aims and scope Submit manuscript

Abstract

The importance of the bi-directional communication between the heart and brain has been known for over 100 years (Lane et al. in NeuroImage 44:213–222, 2009a, Psychosom Med 2:117–134, 2009b) and plays an important role in many of the prominent theories of psychophysiology today. Utilizing heartbeat evoked potentials (HEPs), we sought to determine whether heart rate variability (HRV) was related to the strength of the connection between the heart and brain. We also hypothesized that differing emotion states would result in differing amplitudes of HEPs. Participants were induced into emotional states with an autobiographical script of their happiest and saddest memory. HEPs were also recorded during diaphragmatic breathing at six breaths per minute. The evoked potentials during the emotional conditions, especially negative emotion were most attenuated. We believe that the signal from the heart to the brain may be filtered by central limbic structures affecting the level of the signal at the cortex. It also appears that HRV affects the strength of HEPs, especially during resonant breathing. Significant neurocardiac gender differences were also present across all conditions. The results of this study support the theory and speculation of many authors who believe vagal afferents play a role in brain function.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • American Psychiatric Association. (1994). Diagnostic and statistical manual of mental disorders (4th ed.). Washington, DC: American Psychiatric Association.

    Google Scholar 

  • Andrade, P., Noblesse, L., Temel, Y., Ackermans, L., Lim, L., Steinbusch, H., et al. (2010). Neurostimulatory and ablative treatment options in major depressive disorder: A systematic review. Acta Neurochiugica, 152, 565–577.

    Article  Google Scholar 

  • Basco, M. R., Bostic, J. Q., Davies, D., et al. (2000). Methods to improve diagnostic accuracy in a community mental health setting. American Journal of Psychiatry, 157, 1599–1605.

    Article  Google Scholar 

  • Beauchaine, T. (2001). Vagal tone, development, and Gray’s motivational theory: Toward an integrated model of autonomic nervous system functioning in psychopathology. Development and Psychopathology, 13, 183–214.

    Article  PubMed  Google Scholar 

  • Berthoud, H. R., & Neuhuber, W. L. (2000). Functional and chemical anatomy of the afferent vagal system. Autonomic Neuroscience, 85(1–3), 1–17.

    Article  PubMed  Google Scholar 

  • Breiter, H. C., Etcoff, N. L., Whalen, P. J., Kennedy, W. A., Rauch, S. L., Buckner, R. L., et al. (1996). Response and habituation of the human amygdala during visual processing of facial expression. Neuron, 17, 875–887.

    Article  PubMed  Google Scholar 

  • Britton, J. C., Taylor, S. F., Sudheimer, K. D., & Liberzon, I. (2006). Facial expressions and complex IAPS pictures: Common and differential networks. Neuroimage, 31, 906–919.

    Article  PubMed  Google Scholar 

  • Carla, L. H., & Hamann, S. (2006). Neural correlates of regulating negative emotions related to moral violations. NeuroImage, 30, 313–324.

    Article  Google Scholar 

  • Carney, R. M. (2009). Depression and heart rate variability in patients with coronary heart disease. Cleveland Clinic Journal of Medicine, 76(2), 13–17.

    Article  Google Scholar 

  • Carney, R. M., Blumenthal, J. A., Freedland, K. E., Stein, P. K., Howells, W. B., Berkman, L. F., et al. (2005a). Low heart rate variability and the effect of depression on post-myocardial infarction mortality. Archives of Internal Medicine, 165(13), 1486–1491.

    Article  PubMed  Google Scholar 

  • Carney, R. M., Freedland, K. E., & Veith, K. (2005b). Depression, the autonomic nervous system, and coronary heart disease. Psychosomatic Medicine, 67, 29–33.

    Article  Google Scholar 

  • Crawford, L. E., & Cacioppo, J. T. (2002). Learning where to look for danger: Integrating affective and spatial information. Psychological Science, 13, 449–453.

    Article  PubMed  Google Scholar 

  • Crawford, J. R., & Henry, J. D. (2004). The Positive and Negative Affect Schedule (PANAS): Construct validity, measurement properties and normative data in a large non-clinical sample. British Journal of Clinical Psychology, 43, 245–265.

    Article  PubMed  Google Scholar 

  • DiPietro, J. A., Porges, S. W., & Uhly, B. (1992). Reactivity and developmental competence in preterm and full term infants. Developmental Psychology, 28, 831–841.

    Article  Google Scholar 

  • Dougherty, D. D., Shin, L. M., Alpert, N. M., Pitman, R. K., Orr, S. P., Lasko, M., et al. (1999). Anger in healthy men: A PET study using script-driven imagery. Biological Psychiatry, 46, 466–472.

    Article  PubMed  Google Scholar 

  • Dufey, M., Hurtado, E., Fernandez, A. M., Manes, F., & Ibanez, A. (2010). Exploring the relationship between vagal tone and event related potentials in response to an affective picture task. Social Neuroscience, 1, 1–15.

    Google Scholar 

  • Fennig, S., Craig, T., Lavelle, J., Kovasznay, B., & Bromet, E. J. (1994). Best-estimate versus structured interview-based diagnosis in first-admission psychosis. Comprehensive Psychiatry, 35(5), 341–348.

    Article  PubMed  Google Scholar 

  • Fennig, S., Naisberg-Fennig, S., Craig, T. J., et al. (1996). Comparison of clinical and research diagnoses of substance use disorders in a first-admission psychotic sample. American Journal of Addiction, 5(1), 40–48.

    Google Scholar 

  • Fernandez-Carriba, S., Loeches, A., Morcillo, A., & Hopkins, W. D. (2002). Functional asymmetry of emotions in primates: New findings in chimpanzees. Brain Research Bulletin, 57, 561–564.

    Article  PubMed  Google Scholar 

  • First, M. B., Spitzer, R. L., Gibbon, M., & Williams, J. B. (2002). Structured clinical interview for DSM-IV-TR Axis I disorders, research version, non-patient edition (SCID-I/NP). New York: Biometrics Research, New York State Psychiatric Institute.

    Google Scholar 

  • Garcia–Garcia, M., Dominguez-Borras, J., SanMiguel, I., & Escera, C. (2008). Electrophysiological and behavioral evidence of gender differences in the modulation of distraction by the emotional context. Biological Psychology, 79, 307–316.

    Article  PubMed  Google Scholar 

  • Gevirtz, R. (2000). Resonant frequency training to restore homeostasis for treatment of psychophysiological disorders. Biofeedback, 27, 7–9.

    Google Scholar 

  • Gruber, J., Oveis, C., Keltner, D., & Johnson, S. L. (2008). Risk for mania and positive emotional responding: Too much of a good thing? Emotion, 8(1), 23–33.

    Article  PubMed  Google Scholar 

  • Hassett, A. L., Radvanski, D. C., Vaschillo, E. G., Vaschillo, B., Sigal, L. H., et al. (2007). A pilot study of the efficacy of heart rate variability (HRV) biofeedback in patients with fibromyalgia. Applied Psychophysiology and Biofeedback, 32, 1–10.

    Article  PubMed  Google Scholar 

  • Hofer, A., Siedentopf, C. M., Ischenbeck, A., Rettenbacher, M. A., Verius, M., Felber, S., et al. (2007). Sex differences in brain activation patterns during processing of positively and negatively valenced emotional words. Psychological Medicine, 37(1), 109–119.

    Article  PubMed  Google Scholar 

  • Karavidas, M., Lehrer, P. M., Vaschillo, E., Vaschillo, B., Marin, H., Buyske, S., et al. (2007). Preliminary results of an open label study of heart rate variability biofeedback for the treatment of major depression. Applied Psychophysiology and Biofeedback, 32(1), 19–30.

    Article  PubMed  Google Scholar 

  • Kemp, A. H., Quintana, D. S., Gray, M. A., Felmingham, K. L., Brown, K., & Gatt, J. (2010). Impact of depression and antidepressant treatment on heart rate variability: A review and meta-analysis. Biological Psychiatry, 67(11), 1067–1074.

    Article  PubMed  Google Scholar 

  • Kemp, A. H., Silberstein, R. B., Armstrong, S. M., & Nathan, P. J. (2004). Gender differences in the cortical electrophysiological processing of visual emotional stimuli. NeuroImage, 16, 632–646.

    Article  Google Scholar 

  • Kessler, R. C. (2004). Epidemiology of women and depression. Journal of Affective Disorders, 74, 5–13.

    Article  Google Scholar 

  • Kranzler, R., Kadden, R., Burleson, J., et al. (1995). Validity of psychiatric diagnoses in patients with substance use disorders—is the interview more important than the interviewer. Comprehensive Psychiatry, 36(4), 278–288.

    Article  PubMed  Google Scholar 

  • Kranzler, H. R., Kadden, R. M., Babor, T. F., et al. (1996). Validity of the SCID in substance abuse patients. Addiction, 91(6), 859–868.

    Article  PubMed  Google Scholar 

  • Lane, R. D., McRae, K., Reiman, E. M., Ahern, G. L., & Thayer, J. F. (2007). Neural correlates of vagal tone during emotion. Psychosomatic Medicine, 69, A-8.

    Google Scholar 

  • Lane, R. D., Weidenbacher, H., Fort, C. L., Thayer, J. F., & Allen, J. B. (2008). Subgenual anterior cingulate (BA25) activity correlates with changes in cardiac vagal tone during affective set shifting in healthy adults. Psychosomatic Medicine, 70, A-42.

    Article  Google Scholar 

  • Lane, R. D., McRae, K., Reiman, E. M., Chen, K., Ahern, G. L., & Thayer, J. F. (2009a). Neural correlates of heart rate variability during emotion. NeuroImage, 44, 213–222.

    Article  PubMed  Google Scholar 

  • Lane, R. D., Waldstein, S. R., Chesney, M. A., Jennings, R., Lovallo, W. R., Kozel, P. J., et al. (2009b). The rebirth of neuroscience in psychosomatic medicine, part I: Historical context, methods, and relevant basic science. Psychosomatic Medicine, 71(2), 117–134.

    Article  PubMed  Google Scholar 

  • Lazar, S. W., Kerr, C. E., Wasserman, R. H., Gray, J. R., Greve, D. N., & Treadway, M. T. (2005). Meditation experience is associated with increased cortical thickness. NeuroReport, 16(17), 1893–1897.

    Article  PubMed  Google Scholar 

  • Lehrer, P. M., Vaschillo, E., & Vaschillo, B. (2000). Resonant frequency biofeedback training to increase cardiac variability: rationale and manual for training. Applied Psychophysiology and Biofeedback, 25(3), 177–191.

    Article  PubMed  Google Scholar 

  • Lehrer, P., Vaschillo, E., Vaschillo, B., Lu, S., Eckberg, D. L., Edelberg, R., et al. (2003). Heart rate variability biofeedback increases baroreflex gain and peak expiratory flow. Psychosomatic Medicine, 65, 796–805.

    Article  PubMed  Google Scholar 

  • Levy, M. N. (1990). Autonomic interactions in cardiac control. Annals of the New York Academy of Sciences, 601, 209–221.

    Article  PubMed  Google Scholar 

  • Lithari, C., Frantzidis, C. A., Papadelis, C., Vivas, A. B., Klados, M. A., Kourtidou-Papadeli, C., et al. (2010). Are females more responsive to emotional stimuli? A neurophysiological study across arousal and valence dimensions. Brain Topography, 23, 27–40.

    Article  PubMed  Google Scholar 

  • Lobbestael, J., Leurgans, M., & Arntz, A. (2010). Inter-rater reliability of the Structured Clinical Interview for DSM-IV Axis I Disorders (SCID I) and Axis II Disorders (SCID II). Clinical Psychology Psychotherapy, 3, 21.

    Google Scholar 

  • Lyonfields, J., Borkevec, T., & Thayer, J. (1995). Vagal tone in generalized anxiety disorder and the effect of aversive imagery and worrisome thinking. Behavior Therapy, 26, 257–266.

    Article  Google Scholar 

  • Manta, S., Dong, J., & Debonnel, G. (2009). Enhancement of the function of rat serotonin and norepinephrine neurons by sustained vagus nerve stimulation. Journal of Psychiatry and Neuroscience, 34(4), 272–280.

    PubMed  Google Scholar 

  • Mayberg, H. S., Liotti, M., Brannan, S. K., McGinnis, S., Mahurin, R. K., Jerabek, P. A., et al. (1999). Reciprocal limbic-cortical function and negative mood: Converging PET findings in depression and normal sadness. American Journal of Psychiatry, 156, 675–682.

    PubMed  Google Scholar 

  • McCraty, R. (2003). Heart-brain neurodynamics: The making of emotions. HeartMath Research Center, Institute of HeartMath, Publication Number 03-015. Boulder Creek, CA.

  • McCraty, R., Atkinson, M., Tomasino, D., & Bradley, R. T. (2009). The coherent heart heart-brain interactions, psychophysiological coherence and the emergence of a system-wide order. Integral Review, 5(2), 10–115.

    Google Scholar 

  • Montoya, P., Schandry, R., & Muller, A. (1993). Heartbeat evoked potentials (HEP): Topography and influence of cardiac awareness and focus of attention. Electroencephalography and Clinical Neurophysiology, 88, 163–172.

    Article  PubMed  Google Scholar 

  • Morris, J. S., Frith, C. D., Perrett, D. I., Rowland, D., Young, A. W., Calder, A. J., et al. (1996). A differential neural response in the human amygdala to fearful and happy facial expressions. Nature, 383, 812–815.

    Article  PubMed  Google Scholar 

  • Morris, J. S., Öhman, A., & Dolan, R. J. (1998). Conscious and unconscious emotional learning in the human amygdala. Nature, 393, 467–470.

    Article  PubMed  Google Scholar 

  • Movius, H., & Allen, J. (2004). Cardiac vagal tone, defensiveness, and motivational style. Biological Psychology, 68, 147–162.

    Article  Google Scholar 

  • Nolan, R. P., Kamath, M. V., Floras, J. S., Stanley, J., Pang, C., Picton, P., et al. (2005). Heart rate variability biofeedback as a behavioral neurocardiac intervention to enhance vagal heart rate control. American Heart Journal, 149(6), 1137.e1–1137.e7.

    Article  Google Scholar 

  • Nugent, A. C., Bain, E. E., Thayer, J. F., & Drevets, W. C. (2007). Anatomical correlates of autonomic control during a motor task. Psychosomatic Medicine, 69, A-74.

    Google Scholar 

  • Olofsson, J. K., Nordin, S., Sequeira, H., & Polich, J. (2008). Affective picture processing: An integrative review of ERP findings. Biological Psychology, 77(3), 247–265.

    Article  PubMed  Google Scholar 

  • Orozco, S., & Ehlers, C. L. (1998). Gender differences in electrophysiological responses to facial stimuli. Society of Biological Psychiatry, 44(4), 281–289.

    Article  Google Scholar 

  • Pitman, R. K., Orr, S. P., Forgue, D. F., Altman, B., & de Jong, J. B. (1990). Psychophysiologic responses to combat imagery of Vietnam veterans with posttraumatic stress disorder versus other anxiety disorders. Journal of Abnormal Psychology, 99, 49–54.

    Article  PubMed  Google Scholar 

  • Pollatos, O., & Schandry, R. (2004). Accuracy of heartbeat perception is reflected in the amplitude of the heartbeat-evoked brain potential. Psychophysiology, 41, 476–482.

    Article  PubMed  Google Scholar 

  • Porges, S. W. (1995). Cardiac vagal tone: A physiological index of stress. Neuroscience and Biobehavioral Reviews, 19, 225–233.

    Article  PubMed  Google Scholar 

  • Pretz, J. E., Totz, K. S., & Kaufman, S. B. (2010). The effects of mood, cognitive style, and cognitive ability on implicit learning. doi:10.1016/j.lindif.2009.12.003.

  • Pu, J., Schmeichel, B. J., & Demaree, H. A. (2010). Cardiac vagal control predicts spontaneous regulation of negative emotional expression and subsequent cognitive performance. Biological Psychology, 84, 531–540.

    Article  Google Scholar 

  • Rechlin, T., Weis, M., Spitzer, A., & Kaschka, W. (1994). Are affective disorders associated with alterations of heart rate variability? Journal of Affective Disorders, 32, 271–275.

    Article  PubMed  Google Scholar 

  • Reiman, E. M., Lane, R. D., Ahern, G. L., Schwartz, G. E., Davidson, R. J., Friston, K. J., et al. (1997). Neuroanatomical correlates of externally and internally generated emotion. American Journal of Psychiatry, 154, 918–925.

    PubMed  Google Scholar 

  • Rush, A. J., George, M. S., Sackeim, H. A., Marangell, L. B., Husain, M. M., Giller, C., et al. (2000). Vagus nerve stimulation (VNS) for treatment-resistant depressions: A multicenter study. Biological Psychiatry, 47(4), 276–286.

    Article  PubMed  Google Scholar 

  • Schandry, R., & Montoya, P. (1996). Event-related brain potentials and the processing of cardiac activity. Biological Psychology, 42, 75–85.

    Article  PubMed  Google Scholar 

  • Schandry, R., Sparrer, B., & Weitkunat, R. (1986). From the heart to the brain: A study of heartbeat contingent scalp potentials. International Journal of Neuroscience, 30, 261–275.

    Article  PubMed  Google Scholar 

  • Schupp, H. T., Junghofer, M., Welke, A. I., & Hamm, A. O. (2003). Attention and emotion: an ERP Analysis of facilitated emotional stimulus processing. Neuroreport, 14(8), 1107–1110.

    Article  PubMed  Google Scholar 

  • Shear, M. K., Greeno, C., Kang, J., et al. (2000). Diagnosis of nonpsychotic patients in community clinics. American Journal of Psychiatry, 157, 581–587.

    Article  PubMed  Google Scholar 

  • Siepmann, M., Aykac, V., Unterdorfer, J., Petrowski, K., & Mueck-Weymann, M. (2008). A pilot study on the effects of heart rate variability biofeedback in patients with depression and in healthy subjects. Applied Psychophysiology and Biofeedback, 33(4), 195–201.

    Article  PubMed  Google Scholar 

  • Smith, D. P., Hillman, C. H., & Duley, A. R. (2005). Influences of age on emotional reactivity during picture processing. Journal of Gerontology Series B: Psychological Sciences and Social Sciences, 60, 49–56.

    Article  Google Scholar 

  • Steiner, J. L., Tebes, J. K., Sledge, W. H., et al. (1995). A comparison of the structured clinical interview for DSM-III-R and clinical diagnoses. Journal of Nervous Mental Disorders, 183(6), 365–369.

    Article  Google Scholar 

  • Tarvainen, M. P. & Niskanen, J. P. (2008). Kubios HRV version 2.0 user’s guide. Biosignal Analysis and Medical Imaging Group (BSAMIG). Department of Physics, University of Kuopio, Kuopio Finland. Matlab, MathWorks, Inc.

  • Task Force of the European Society of Cardiology the North American Society of Pacing Electrophysiology. (1996). Heart rate variability: Standards of measurement, physiological interpretation, and clinical use. Circulation, 93, 1043–1065.

    Article  Google Scholar 

  • Terhaar, J., Viola, C. F., Bar, K., & Debener, S. (2012). Heartbeat evoked potentials mirror altered body perception in depressed patients. Clinical Neurophysiology. doi:10.1016/j.clinph.2012.02.086.

  • Thayer, J. F., & Lane, R. D. (2000). A model of neurovisceral integration in emotion regulation and dysregulation. Journal of Affective Disorders, 61(3), 201–216.

    Article  PubMed  Google Scholar 

  • Thayer, J. F., & Lane, R. D. (2009). Claude Bernard and the heart-brain connection: Further elaboration of a model of neurovisceral integration. Neuroscience and Behavioral Reviews, 33(2), 81–88.

    Article  Google Scholar 

  • Tortora, G. J., & Grabowski, S. R. (1996). Principles of anatomy and physiology (8th ed.). New York: Harper Collins.

    Google Scholar 

  • Undem, B. J., & Weinreich, D. (Eds.). (2005). Advances in vagal afferent neurobiology. Boca Raton, FL: CRC Press.

    Google Scholar 

  • Vytal, K., & Hamann, S. (2010). Neuroimaging support for discrete neural correlates of basic emotions: A voxel-based meta-analysis. Journal of Cognitive Neuroscience, 22(12), 2864–2885.

    Article  PubMed  Google Scholar 

  • Watson, D., Clarke, L. A., & Tellegen, A. (1988). Development and validation of brief Brief measures of positive and negative affect: The PANAS Scales. Journal of Personality and Social Psychology, 47, 1063–1070.

    Article  Google Scholar 

  • Wrase, J., Klein, S., Gruesser, S. M., Hermann, D., Flor, H., Mann, K., et al. (2003). Gender differences in the processing of standardized emotional visual stimuli in humans: A functional magnetic resonance imaging study. Neu-roscience Letters, 348, 41–45.

    Article  Google Scholar 

Download references

Conflict of interest

None.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Starr MacKinnon.

Additional information

This data has been previously published as the first author’s dissertation with UMI Dissertation Publishing.

Rights and permissions

Reprints and permissions

About this article

Cite this article

MacKinnon, S., Gevirtz, R., McCraty, R. et al. Utilizing Heartbeat Evoked Potentials to Identify Cardiac Regulation of Vagal Afferents During Emotion and Resonant Breathing. Appl Psychophysiol Biofeedback 38, 241–255 (2013). https://doi.org/10.1007/s10484-013-9226-5

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10484-013-9226-5

Keywords

Navigation