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Cold Face Test-Induced Increases in Heart Rate Variability Are Abolished by Engagement in a Social Cognition Task

Published Online:September 15, 2015https://doi.org/10.1027/0269-8803/a000152

Abstract

Abstract. The vagus nerve is a major constituent in the bidirectional relationship between the heart and the prefrontal cortex. This study investigated the role of the vagus in social cognition using the cold face test (facial cooling) to stimulate the vagus nerve and increase prefrontal inhibitory control. Heart Rate Variability (HRV) was measured to index parasympathetic outflow while social cognition ability was tested using the Reading the Mind in the Eyes Test (RMET). Healthy males (n = 25) completed the RMET under two conditions: with and without facial cooling. Results indicated that although facial cooling increased HRV at rest, there was no improvement in the RMET during the facial cooling condition. Interestingly, completing the RMET with facial cooling abolished this increase in HRV, suggesting interference along the vagal reflex arc. These results are consistent with the involvement of a common cortico-subcortical circuit in autonomic and cognitive processes, important for emotion recognition.

References

  • Akselrod, S., Gordon, D., Ubel, F. A., Shannon, D. C., Berger, A. & Cohen, R. J. (1981). Power spectrum analysis of heart rate fluctuation: A quantitative probe of beat-to-beat cardiovascular control. Science, 213, 220–222. First citation in articleCrossref, Google Scholar

  • Allen, M. T., Shelley, K. S. & Boquet, A. J. Jr. (1992). A comparison of cardiovascular and autonomic adjustments to three types of cold stimulation tasks. International Journal of Psychophysiology, 13, 59–69. First citation in articleCrossref, Google Scholar

  • Alvares, G. A., Quintana, D. S., Kemp, A. H., Van Zwieten, A., Balleine, B. W., Hickie, I. B. & Guastella, A. J. (2013). Reduced heart rate variability in social anxiety disorder: Associations with gender and symptom severity. PLoS One, 8, e70468. doi: 10.1371/journal.pone.0070468 First citation in articleCrossref, Google Scholar

  • Amodio, D. M. & Frith, C. D. (2006). Meeting of minds: The medial frontal cortex and social cognition. Nature Reviews Neuroscience, 7, 268–277. First citation in articleCrossref, Google Scholar

  • Appelhans, B. M. & Luecken, L. J. (2006). Heart rate variability as an index of regulated emotional responding. Review of general psychology, 10, 229. First citation in articleCrossref, Google Scholar

  • Appelhans, B. M. & Luecken, L. J. (2008). Heart rate variability and pain: Associations of two interrelated homeostatic processes. Biological Psychology, 77, 174–182. doi: 10.1016/j.biopsycho.2007.10.004 First citation in articleCrossref, Google Scholar

  • Babor, T. F., Korner, P., Wilber, C. & Good, S. P. (1987). Screening and early intervention strategies for harmful drinkers: Initial lessons from the Amethyst project. Drug and Alcohol Review, 6, 325–339. First citation in articleCrossref, Google Scholar

  • Bannister, R. & Oppenheimer, D. (1972). Degenerative diseases of the nervous system associated with autonomic failure. Brain, 95, 457–474. First citation in articleCrossref, Google Scholar

  • Baron‐Cohen, S., Wheelwright, S., Hill, J., Raste, Y. & Plumb, I. (2001). The “Reading the mind in the eyes” test revised version: A study with normal adults, and adults with Asperger syndrome or high‐functioning autism. Journal of Child Psychology and Psychiatry, 42, 241–251. First citation in articleCrossref, Google Scholar

  • Barutcu, I., Esen, A. M., Kaya, D., Turkmen, M., Karakaya, O., Melek, M., … Basaran, Y. (2005). Cigarette smoking and heart rate variability: Dynamic influence of parasympathetic and sympathetic maneuvers. Annals of Noninvasive Electrocardiology, 10, 324–329. First citation in articleCrossref, Google Scholar

  • Baumert, M. & Sacre, J. W. (2013). Heart rate complexity and cardiac sympathetic dysinnervation in patients with type 2 diabetes mellitus, Paper presented at the Engineering in Medicine and Biology Society (EMBC) 2013 35th Annual International Conference of the IEEE, Osaka, Japan. First citation in articleGoogle Scholar

  • Bauminger, N. (2002). The facilitation of social-emotional understanding and social interaction in high-functioning children with autism: Intervention outcomes. Journal of Autism and Developmental Disorders, 32, 283–298. First citation in articleCrossref, Google Scholar

  • Benarroch, E. E. (1993). The central autonomic network: Functional organization, dysfunction, and perspective, Paper presented at the Mayo Clinic Proceedings, Rochester, NY. First citation in articleGoogle Scholar

  • Benarroch, E. E. & Parisi, J. E. (2000). Involvement of the ventrolateral medulla in parkinsonism with autonomic failure. Neurology, 54, 963–968. First citation in articleCrossref, Google Scholar

  • Berntson, G. G., Bigger, J. T. Jr., Eckberg, D. L., Grossman, P., Kaufmann, P. G., Malik, M., … van der Molen, M. W. (1997). Heart rate variability: Origins, methods, and interpretive caveats. Psychophysiology, 34, 623–648. First citation in articleCrossref, Google Scholar

  • Berntson, G. G., Cacioppo, J. T. & Quigley, K. S. (1993). Respiratory sinus arrhythmia: autonomic origins, physiological mechanisms, and psychophysiological implications. Psychophysiology, 30, 183–196. First citation in articleCrossref, Google Scholar

  • Brick, I. (1966). Circulatory responses to immersing the face in water. Journal of Applied Physiology, 21, 33–36. First citation in articleCrossref, Google Scholar

  • Butler, P. J. & Jones, D. R. (1997). Physiology of diving of birds and mammals. Physiological Reviews, 77, 837. First citation in articleCrossref, Google Scholar

  • Camm, A., Malik, M., Bigger, J., Breithardt, G., Cerutti, S., Kleiger, R., … Kleiger, R. (1996). Heart rate variability: standards of measurement, physiological interpretation and clinical use. Task Force of the European Society of Cardiology and the North American Society of Pacing and Electrophysiology. Circulation, 93, 1043–1065. First citation in articleCrossref, Google Scholar

  • Carney, R. M., Blumenthal, J. A., Stein, P. K., Watkins, L., Catellier, D., Berkman, L. F., … Freedland, K. E. (2001). Depression, heart rate variability, and acute myocardial infarction. Circulation, 104, 2024–2028. First citation in articleCrossref, Google Scholar

  • Cohen, J. (1973). Eta-squared and partial eta-squared in fixed factor ANOVA designs. Educational and Psychological Measurement, 33, 107–112. First citation in articleCrossref, Google Scholar

  • Couture, S. M., Penn, D. L. & Roberts, D. L. (2006). The functional significance of social cognition in schizophrenia: A review. Schizophrenia Bulletin, 32, S44–S63. First citation in articleGoogle Scholar

  • Davis, M. & Whalen, P. J. (2001). The amygdala: Vigilance and emotion. Molecular Psychiatry, 6, 13–34. First citation in articleCrossref, Google Scholar

  • Dishman, R. K., Nakamura, Y., Garcia, M. E., Thompson, R. W., Dunn, A. L. & Blair, S. N. (2000). Heart rate variability, trait anxiety, and perceived stress among physically fit men and women. International Journal of Psychophysiology, 37, 121–133. First citation in articleCrossref, Google Scholar

  • Duncan, G. H., Bushnell, M. C. & Lavigne, G. J. (1989). Comparison of verbal and visual analogue scales for measuring the intensity and unpleasantness of experimental pain. Pain, 37, 295–303. First citation in articleCrossref, Google Scholar

  • Durel, L. A., Kus, L. A., Anderson, N. B., Mcneilly, M., Llabre, M. M., Spitzer, S., … Schneiderman, N. (1993). Patterns and stability of cardiovascular responses to variations of the cold pressor test. Psychophysiology, 30, 39–46. First citation in articleCrossref, Google Scholar

  • Elstad, M., Walløe, L., Chon, K. H. & Toska, K. (2011). Low-frequency fluctuations in heart rate, cardiac output and mean arterial pressure in humans: What are the physiological relationships? Journal of Hypertension, 29, 1327–1336. First citation in articleCrossref, Google Scholar

  • First, M. B., Spitzer, R. L., Gibbon, M. & Williams, J. B. (2007). Structured clinical interview for DSM-IV-TR axis I disorders, research version, Non- patient edition (SCID-I/NP), New York, NY: Biometrics Research, New York State Psychiatric Institute. First citation in articleGoogle Scholar

  • Fiske, S. T. & Taylor, S. E. (2013). Social cognition: From brains to culture (2nd ed.). Thousand Oaks, CA: Sage. First citation in articleCrossref, Google Scholar

  • Goldie, J., McGregor, C. & Murphy, B. (2010). Determining levels of arousal using electrocardiography: A study of HRV during transcranial magnetic stimulation, Paper presented at the Engineering in Medicine and Biology Society (EMBC), 2010 Annual International Conference of the IEEE, Buenos Aires. First citation in articleGoogle Scholar

  • Guastella, A. J., Hickie, I. B., McGuinness, M. M., Otis, M., Woods, E. A., Disinger, H. M., … Banati, R. B. (2013). Recommendations for the standardisation of oxytocin nasal administration and guidelines for its reporting in human research. Psychoneuroendocrinology, 38, 612–625. First citation in articleCrossref, Google Scholar

  • Hansen, A., Johnsen, B., Sollers, J. III, Stenvik, K. & Thayer, J. (2004). Heart rate variability and its relation to prefrontal cognitive function: The effects of training and detraining. European Journal of Applied Physiology, 93, 263–272. doi: 10.1007/s00421-004-1208-0 First citation in articleCrossref, Google Scholar

  • Hayashi, N., Ishihara, M., Tanaka, A., Osumi, T. & Yoshida, T. (1997). Face immersion increases vagal activity as assessed by heart rate variability. European Journal of Applied Physiology and Occupational Physiology, 76, 394–399. First citation in articleCrossref, Google Scholar

  • Hirsch, J. A. & Bishop, B. (1981). Respiratory sinus arrhythmia in humans: How breathing pattern modulates heart rate. American Journal of Physiology: Heart and Circulatory Physiology, 241, H620–H629. First citation in articleGoogle Scholar

  • Ieda, M., Miyaoka, T., Wake, R., Liaury, K., Tsuchie, K., Fukushima, M., … Horiguchi, J. (2014). Evaluation of autonomic nervous system by salivary alpha-amylase level and heart rate variability in patients with schizophrenia. European Archives of Psychiatry and Clinical Neuroscience, 264, 83–87. doi: 10.1007/s00406-013-0411-6 First citation in articleCrossref, Google Scholar

  • Kawakami, Y., Natelson, B. H. & DuBois, A. (1967). Cardiovascular effects of face immersion and factors affecting diving reflex in man. Journal of Applied Physiology, 23, 964–970. First citation in articleCrossref, Google Scholar

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

  • Khurana, R. K., Watabiki, S., Hebel, J., Toro, R. & Nelson, E. (1980). Cold face test in the assessment of trigeminal‐brainstem‐vagal function in humans. Annals of Neurology, 7, 144–149. First citation in articleCrossref, Google Scholar

  • Khurana, R. K. & Wu, R. (2006). The cold face test: A non-baroreflex mediated test of cardiac vagal function. Clinical Autonomic Research, 16, 202–207. doi: 10.1007/s10286-006-0332-9 First citation in articleCrossref, Google Scholar

  • Kristensson, K., Olsson, Y. & Sourander, P. (1971). Changes in the vagus nerve in diabetes mellttus. Acta Pathologica Microbiologica Scandinavica Section A Pathology, 79, 684–685. First citation in articleGoogle Scholar

  • Kruyen, P. M., Emons, W. H. & Sijtsma, K. (2013). Shortening the S-STAI: Consequences for research and clinical practice. Journal of Psychosomatic Research. First citation in articleGoogle Scholar

  • La Marca, R., Waldvogel, P., Thorn, H., Tripod, M., Wirtz, P. H., Pruessner, J. C. & Ehlert, U. (2011). Association between Cold Face Test-induced vagal inhibition and cortisol response to acute stress. Psychophysiology, 48, 420–429. doi: 10.1111/j.1469-8986.2010.01078.x First citation in articleCrossref, Google Scholar

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

  • Lee, L., Harkness, K. L., Sabbagh, M. A. & Jacobson, J. A. (2005). Mental state decoding abilities in clinical depression. Journal of Affective Disorders, 86, 247–258. First citation in articleCrossref, Google Scholar

  • Lovibond, P. F. & Lovibond, S. H. (1995). The structure of negative emotional states: Comparison of the Depression Anxiety Stress Scales (DASS) with the Beck Depression and Anxiety Inventories. Behaviour Research and Therapy, 33, 335–343. First citation in articleCrossref, Google Scholar

  • Malpas, S. C., Whiteside, E. A. & Maling, T. J. (1991). Heart rate variability and cardiac autonomic function in men with chronic alcohol dependence. British Heart Journal, 65, 84–88. First citation in articleCrossref, Google Scholar

  • Marteau, T. M. & Bekker, H. (1992). The development of a six‐item short‐form of the state scale of the Spielberger State – Trait Anxiety Inventory (STAI). The British Journal of Clinical Psychology, 31, 301–306. First citation in articleCrossref, Google Scholar

  • Mehnert, U., Knapp, P. A., Mueller, N., Reitz, A. & Schurch, B. (2009). Heart rate variability: An objective measure of autonomic activity and bladder sensations during urodynamics. Neurourology and urodynamics, 28, 313–319. First citation in articleCrossref, Google Scholar

  • Mizuno, K., Tanaka, M., Yamaguti, K., Kajimoto, O., Kuratsune, H. & Watanabe, Y. (2011). Mental fatigue caused by prolonged cognitive load associated with sympathetic hyperactivity. Behavioral and Brain Functions, 7, 17. First citation in articleCrossref, Google Scholar

  • Porges, S. W. (2003). The polyvagal theory: Phylogenetic contributions to social behavior. Physiology & Behavior, 79, 503–513. First citation in articleCrossref, Google Scholar

  • Quintana, D. S., Guastella, A. J., Outhred, T., Hickie, I. B. & Kemp, A. H. (2012). Heart rate variability is associated with emotion recognition: Direct evidence for a relationship between the autonomic nervous system and social cognition. International Journal of Psychophysiology, 86, 168–172. doi: 10.1016/j.ijpsycho.2012.08.012 First citation in articleCrossref, Google Scholar

  • Quintana, D. S. & Heathers, J. A. (2014). Considerations in the assessment of heart rate variability in biobehavioral research. Frontiers in Psychology, 5, 805. First citation in articleCrossref, Google Scholar

  • Quintana, D. S., Kemp, A. H., Alvares, G. A. & Guastella, A. J. (2013). A role for autonomic cardiac control in the effects of oxytocin on social behavior and psychiatric illness. Frontiers in Neuroscience, 7, 48. doi: 10.3389/fnins.2013.00048 First citation in articleCrossref, Google Scholar

  • Quintana, D. S., McGregor, I. S., Guastella, A. J., Malhi, G. S. & Kemp, A. H. (2013). A meta‐analysis on the impact of alcohol dependence on short‐term resting‐state heart rate variability: Implications for cardiovascular risk. Alcoholism: Clinical and Experimental Research, 37, E23–E29. First citation in articleGoogle Scholar

  • Ryan, C., Hollenberg, M., Harvey, D. B. & Gwynn, R. (1976). Impaired parasympathetic responses in patients after myocardial infarction. The American journal of cardiology, 37, 1013–1018. First citation in articleCrossref, Google Scholar

  • Shahrestani, S., Stewart, E. M., Quintana, D. S., Hickie, I. B. & Guastella, A. J. (2014). Heart rate variability during social interactions in children with and without psychopathology: A meta‐analysis. Journal of Child Psychology and Psychiatry. First citation in articleGoogle Scholar

  • Spielberger, C. D., Gorsuch, R. L., Lushene, R. E. & Vagg, P. R. (1983). State-Trait Anxiety Inventory (STAI). BiB, 2010, 180. First citation in articleGoogle Scholar

  • Stemper, B., Hilz, M., Rauhut, U. & Neundörfer, B. (2002). Evaluation of cold face test bradycardia by means of spectral analysis. Clinical Autonomic Research, 12, 78–83. First citation in articleCrossref, Google Scholar

  • Tanaka, M., Mizuno, K., Tajima, S., Sasabe, T. & Watanabe, Y. (2009). Central nervous system fatigue alters autonomic nerve activity. Life Sciences, 84, 235–239. First citation in articleCrossref, Google Scholar

  • Thayer, J. F., Åhs, F., Fredrikson, M., Sollers, J. J. III & 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. Neuroscience & Biobehavioral Reviews, 36, 747–756. First citation in articleCrossref, Google Scholar

  • Thayer, J. F., Friedman, B. H. & Borkovec, T. D. (1996). Autonomic characteristics of generalized anxiety disorder and worry. Biological Psychiatry, 39, 255–266. First citation in articleCrossref, Google Scholar

  • Thayer, J. F., Hall, M., Sollers, J. J. III & Fischer, J. E. (2006). Alcohol use, urinary cortisol, and heart rate variability in apparently healthy men: Evidence for impaired inhibitory control of the HPA axis in heavy drinkers. International Journal of Psychophysiology, 59, 244–250. First citation in articleCrossref, Google Scholar

  • Thayer, J. F., Hansen, A. L., Saus-Rose, E. & Johnsen, B. H. (2009). Heart rate variability, prefrontal neural function, and cognitive performance: The neurovisceral integration perspective on self-regulation, adaptation, and health. Annals of Behavioral Medicine, 37, 141–153. First citation in articleCrossref, Google Scholar

  • Thayer, J. F. & Lane, R. D. (2000). A model of neurovisceral integration in emotion regulation and dysregulation. Journal of Affective Disorders, 61, 201–216. First citation in articleCrossref, 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 & Biobehavioral Reviews, 33, 81–88. First citation in articleCrossref, Google Scholar

  • Van Breukelen, G. J. & Van Dijk, K. R. (2007). Use of covariates in randomized controlled trials. Journal of the International Neuropsychological Society, 13, 903–904. First citation in articleCrossref, Google Scholar

  • Vellante, M., Baron-Cohen, S., Melis, M., Marrone, M., Petretto, D. R., Masala, C. & Preti, A. (2013). The “Reading the Mind in the Eyes” test: Systematic review of psychometric properties and a validation study in Italy. Cognitive Neuropsychiatry, 18, 326–354. First citation in articleCrossref, Google Scholar

  • Weippert, M., Kumar, M., Kreuzfeld, S., Arndt, D., Rieger, A. & Stoll, R. (2010). Comparison of three mobile devices for measuring R-R intervals and heart rate variability: Polar S810i, Suunto t6 and an ambulatory ECG system. European Journal of Applied Physiology, 109, 779–786. First citation in articleCrossref, Google Scholar

  • Zbrożyna, A. W. & Westwood, D. M. (1992). Cardiovascular responses elicited by simulated diving and their habituation in man. Clinical Autonomic Research, 2, 225–233. First citation in articleCrossref, Google Scholar