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Decreased heart rate variability during emotion regulation in subjects at risk for psychopathology

Published online by Cambridge University Press:  09 November 2011

M. Di Simplicio ,
G. Costoloni ,
D. Western ,
B. Hanson ,
P. Taggart  and
C. J. Harmer
M. Di Simplicio*
Affiliation:
University Department of Psychiatry, Warneford Hospital, Oxford, UK Neuroscience Department, Psychiatry Section, University of Siena, Siena, Italy
G. Costoloni
Affiliation:
Neuroscience Department, Psychiatry Section, University of Siena, Siena, Italy
D. Western
Affiliation:
Department of Mechanical Engineering, University College London, London, UK
B. Hanson
Affiliation:
Department of Mechanical Engineering, University College London, London, UK
P. Taggart
Affiliation:
Neurocardiology Research Unit, University College London, London, UK
C. J. Harmer
Affiliation:
University Department of Psychiatry, Warneford Hospital, Oxford, UK
*
*Address for correspondence: Dr M. Di Simplicio, Department of Psychiatry, Warneford Hospital, Warneford Lane, Oxford, OX3 7JX, UK. (Email: [email protected])
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Abstract

Background

Dysfunctions in the regulation of emotional responses are related to poor psychological well-being and increased impact of cardiovascular disease. It has been suggested that the relationship between negative affect and higher morbidity could be mediated by a dysregulation of the autonomic nervous system (ANS), for example, of heart rate variability (HRV). Neuroticism is a personality trait associated with a maladaptive emotion regulation and also with alterations in ANS function. However, it is unknown whether subjects with high neuroticism present with specific biases in emotion regulation associated with reduced HRV.

Method

In total, 33 healthy subjects (n=13, highly neurotic) performed an emotion regulation task, during which they were instructed to either passively view negative pictures or attempt to down-regulate the affect elicited by the images. During the task an electrocardiogram was recorded and HRV was measured by calculation of the high frequency spectrum (HF-HRV).

Results

A significant interaction between task condition and personality group was observed on HF-HRV measures (F1,31=6.569, p=0.016). This was driven by subjects with low neuroticism presenting higher HF-HRV during down-regulation compared to passive exposure to negative stimuli, while subjects with high neuroticism reported an opposite tendency.

Conclusions

Our results show reduced HF-HRV during cognitive reappraisal of negative stimuli in high neuroticism and indicate a specific link between loss of flexibility in the parasympathetic cardiovascular tone and emotion regulation, consistent with previous work. Such findings support the importance of exploring the combination of ANS adaptability and emotional dysregulation in neuroticism as different facets of a common psychosomatic vulnerability factor.

Keywords

Emotion regulationheart rate variabilityneuroticism
Type
Original Articles
Information
Psychological Medicine , Volume 42 , Issue 8 , August 2012 , pp. 1775 - 1783
Copyright
Copyright © Cambridge University Press 2011

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References

Åhs, F, Sollers, JJ III, Furmark, T, Fredrikson, M, Thayer, JF (2009). High-frequency heart rate variability and cortico-striatal activity in men and women with social phobia. NeuroImage 47, 815–820.CrossRefGoogle ScholarPubMed
Akaike, H (1974). A new look at the statistical model identification. IEEE Transactions on Automatic Control 19, 716–723.CrossRefGoogle Scholar
Beck, AT, Ward, CH, Mendelson, M, Mock, J, Erbaugh, J (1961). An inventory for measuring depression. Archives of General Psychiatry 4, 561–571.CrossRefGoogle ScholarPubMed
Bleil, ME, Gianaros, PJ, Jennings, JR, Flory, JD, Manuck, SB (2008). Trait negative affect: toward an integrated model of understanding psychological risk for impairment in cardiac autonomic function. Psychosomatic Medicine 70, 328–337.CrossRefGoogle ScholarPubMed
Bruyne, MCD, Kors, JA, Hoes, AW, Klootwijk, P, Dekker, JM, Hofman, A, van Bemmel, JH, Grobbee, DE (1999). Both decreased and increased heart rate variability on the standard 10-second electrocardiogram predict cardiac mortality in the elderly. American Journal of Epidemiology 150, 1282–1288.CrossRefGoogle Scholar
Butler, EA, Wilhelm, FH, Gross, JJ (2006). Respiratory sinus arrhythmia, emotion, and emotion regulation during social interaction. Psychophysiology 43, 612–622.CrossRefGoogle ScholarPubMed
Canli, T (2008). Toward a neurogenetic theory of neuroticism. Annals of the New York Academy of Sciences 1129, 153–174.CrossRefGoogle Scholar
Chan, SW, Goodwin, GM, Harmer, CJ (2007). Highly neurotic never-depressed students have negative biases in information processing. Psychological Medicine 37, 1281–1291.CrossRefGoogle ScholarPubMed
Chan, SW, Harmer, CJ, Goodwin, GM, Norbury, R (2008). Risk for depression is associated with neural biases in emotional categorisation. Neuropsychologia 46, 2896–2903.CrossRefGoogle ScholarPubMed
Chan, SW, Norbury, R, Goodwin, GM, Harmer, CJ (2009). Risk for depression and neural responses to fearful facial expressions of emotion. British Journal of Psychiatry 194, 139–145.CrossRefGoogle ScholarPubMed
Critchley, H, Taggart, P, Suttom, PM, Holdright, D, Batchvarov, V, Hnatkova, K, Malik, M, Dolan, R (2005). Mental stress and sudden cardiac death: asymetric midbrain activity as a linking mechanism. Brain 128, 75–85.CrossRefGoogle Scholar
Critchley, HD, Mathias, CJ, Josephs, O, O'Doherty, J, Zanini, S, Dewar, BK, Cipolotti, L, Shallice, T, Dolan, RJ (2003). Human cingulate cortex and autonomic control: converging neuroimaging and clinical evidence. Brain 126, 2139–2152.CrossRefGoogle ScholarPubMed
de Jonge, P, Rosmalen, JGM, Kema, IP, Doornbos, B, vVan Melle, JP, Pouwer, F, Kupper, N (2010). Psychophysiological biomarkers explaining the association between depression and prognosis in coronary artery patients: a critical review of the literature. Neuroscience & Biobehavioral Reviews 35, 84–90.CrossRefGoogle Scholar
Dekker, JM, Schouten, EG, Klootwijk, P, Pool, J, Swenne, CA, Kromhout, D (1997). Heart rate variability from short electrocardiographic recordings predicts mortality from all causes in middle-aged and elderly men. American Journal of Epidemiology 145, 899–908.CrossRefGoogle ScholarPubMed
Eysenck, SBG, Eysenck, HJ (1975). Manual of the EPQ (Eysenck Personality Questionnaire). University of London Press: London.Google Scholar
Friedman, BH (2007). An autonomic flexibility-neurovisceral integration model of anxiety and cardiac vagal tone. Biological Psychology 74, 185–199.CrossRefGoogle ScholarPubMed
Gentzler, AL, Santucci, AK, Kovacs, M, Fox, NA (2009). Respiratory sinus arrhythmia reactivity predicts emotion regulation and depressive symptoms in at-risk and control children. Biological Psychology 82, 156–163.CrossRefGoogle ScholarPubMed
Gianaros, PJ, van der Veen, FM, Jennings, JR (2004). Regional cerebral blood flow correlates with heart period and high-frequency heart period variability during working-memory tasks: implications for the cortical and subcortical regulation of cardiac autonomic activity. Psychophysiology 41, 521–530.CrossRefGoogle ScholarPubMed
Gramer, M, Saria, K (2007). Effects of social anxiety and evaluative threat on cardiovascular responses to active performance situations. Biological Psychology 74, 67–74.CrossRefGoogle Scholar
Grippo, AJ, Johnson, AK (2009). Stress, depression, and cardiovascular dysregulation: a review of neurobiological mechanisms and the integration of research from preclinical disease models. Stress 12, 1–21.CrossRefGoogle ScholarPubMed
Gross, JJ, John, OP (2003). Individual differences in two emotion regulation processes: implications for affect, relationships, and well-being. Journal of Personality and Social Psychology 85, 348–362.CrossRefGoogle ScholarPubMed
Haas, BW, Constable, RT, Canli, T (2008). Stop the sadness: neuroticism is associated with sustained medial prefrontal cortex response to emotional facial expressions. NeuroImage 42, 385–392.CrossRefGoogle ScholarPubMed
Haas, BW, Omura, K, Constable, RT, Canli, T (2007). Emotional conflict and neuroticism: personality-dependent activation in the amygdala and subgenual anterior cingulate. Behavioural Neuroscience 121, 249–256.CrossRefGoogle ScholarPubMed
Hughes, JW, Stoney, CM (2000). Depressed mood is related to high-frequency heart rate variability during stressors. Psychosomatic Medicine 62, 796–803.CrossRefGoogle ScholarPubMed
Ingjaldsson, JT, Laberg, JC, Thayer, JF (2003). Reduced heart rate variability in chronic alcohol abuse: relationship with negative mood, chronic thought suppression, and compulsive drinking. Biological Psychiatry 54, 1427–1436.CrossRefGoogle ScholarPubMed
Kay, SM (1999). Modern Spectral Estimation: Theory and Application. Prentice Hall PTR: New Jersey.Google Scholar
Kendler, KS, Myers, J (2010). The genetic and environmental relationship between major depression and the five-factor model of personality. Psychological Medicine 40, 801–806.CrossRefGoogle ScholarPubMed
Khan, AA, Jacobson, KC, Gardner, CO, Prescott, CA, Kendler, KS (2005). Personality and comorbidity of common psychiatric disorders. British Journal of Psychiatry 186, 190–196.CrossRefGoogle ScholarPubMed
Lahey, BB (2009). Public health significance of neuroticism. American Psychologist 64, 241–256.CrossRefGoogle ScholarPubMed
Lane, RD, McRae, K, Reiman, EM, Chen, K, Ahern, GL, Thayer, JF (2009). Neural correlates of heart rate variability during emotion. NeuroImage 44, 213–222.CrossRefGoogle ScholarPubMed
Lang, PJ, Bradley, MM, Cuthbert, BN (1997). International Affective Picture System (IAPS): Technical Manual and Affective Ratings. NIMH Center for the Study of Emotion and Attention, University of Florida: Gainesville, FL.Google Scholar
Levy, MN (1990). Autonomic interactions in cardiac control. Annals of the New York Academy of Sciences 601, 209–221.CrossRefGoogle ScholarPubMed
Malik, M (1996). Task Force of the European Society of Cardiology the North American Society of pacing electrophysiology – heart rate variability: standards of measurement, physiological interpretation, and clinical use. Circulation 93, 1043–1065.Google Scholar
Malliani, A (2000). Principles of Cardiac Neuroregulation in Health and Disease. Kluwer Academic Publishers: Dordrecht/Boston/London.CrossRefGoogle Scholar
Malouff, JM, Thorsteinsson, EB, Schutte, NS (2005). The relationship between the five-factor model of personality and symptoms of clinical disorders: a meta-analysis. Journal of Psychopathology and Behavioral Assessment 27, 101–114.CrossRefGoogle Scholar
Mauss, IB, Wilhelm, FH, Gross, JJ (2003). Autonomic recovery and habituation in social anxiety. Psychophysiology 40, 648–653.CrossRefGoogle ScholarPubMed
Mujica-Parodi, LR, Korgaonkar, M, Ravindranath, B, Greenberg, T, Tomasi, D, Wagshul, M, Ardekani, B, Guilfoyle, D, Khan, S, Zhong, Y, Chon, K, Malaspina, D (2009). Limbic dysregulation is associated with lowered heart rate variability and increased trait anxiety in healthy adults. Human Brain Mapping 30, 47–58.CrossRefGoogle ScholarPubMed
Napadow, V, Dhond, R, Conti, G, Makris, N, Brown, EN, Barbieri, R (2008). Brain correlates of autonomic modulation: combining heart rate variability with fMRI. NeuroImage 42, 169–177.CrossRefGoogle ScholarPubMed
Nolan, J, Batin, PD, Andrews, R, Lindsay, SJ, Brooksby, P, Mullen, M, Baig, W, Flapan, AD, Cowley, A, Prescott, RJ, Neilson, JMM, Fox, KAA (1998). Prospective study of heart rate variability and mortality in chronic heart failure: results of the United Kingdom Heart Failure Evaluation and Assessment of Risk Trial (UK-Heart). Circulation 98, 1510–1516.CrossRefGoogle ScholarPubMed
Norman, GJ, Cacioppo, JT, Morris, JS, Malarkey, WB, Berntson, GG, Devries, AC (2011). Oxytocin increases autonomic cardiac control: moderation by loneliness. Biological Psychology 86, 174–180.CrossRefGoogle ScholarPubMed
Nugent, AC, Bain, EE, Thayer, JF, Sollers, JJ III, Drevets, WC (2011). Heart rate variability during motor and cognitive tasks in females with major depressive disorder. Psychiatry Research: Neuroimaging 191, 1–8.CrossRefGoogle ScholarPubMed
Ode, S, Hilmert, CJ, Zielke, DJ, Robinson, MD (2010). Neuroticism's importance in understanding the daily life correlates of heart rate variability. Emotion 10, 536–543.CrossRefGoogle ScholarPubMed
Parati, G, Saul, JP, di Rienzo, M, Mancia, G (1995). Spectral analysis of blood pressure and heart rate variability in evaluating cardiovascular regulation. A critical appraisal. Hypertension 25, 1276–1286.CrossRefGoogle ScholarPubMed
Penninx, BW, Beekman, AT, Honig, A, Deeg, DJ, Schoevers, RA, van Eijk, JT, van Tilburg, W (2001). Depression and cardiac mortality: results from a community-based longitudinal study. Archives of General Psychiatry 58, 221–227.CrossRefGoogle ScholarPubMed
Phan, KL, Fitzgerald, DA, Nathan, PJ, Moore, GJ, Uhde, TW, Tancer, ME (2005). Neural substrates for voluntary suppression of negative affect: a functional magnetic resonance imaging study. Biological Psychiatry 57, 210–219.CrossRefGoogle Scholar
Shinba, T, Kariya, N, Matsui, Y, Ozawa, N, Matsuda, Y, Yamamoto, K (2008). Decrease in heart rate variability response to task is related to anxiety and depressiveness in normal subjects. Psychiatry and Clinical Neuroscience 62, 603–609.CrossRefGoogle ScholarPubMed
Smith, TW, Glazer, K, Ruiz, JM, Gallo, LC (2004). Hostility, anger, aggressiveness, and coronary heart disease: an interpersonal perspective on personality, emotion, and health. Journal of Personality 72, 1217–1270.CrossRefGoogle ScholarPubMed
Smith, TW, Mackenzie, J (2006). Personality and risk of physical illness. Annual Review of Clinical Psychology 2, 435–467.CrossRefGoogle ScholarPubMed
Spielberger, CD, Gorsuch, RL, Lushene, RD (1983). Manual for the State-Trait Anxiety Inventory (STAI). Consulting Psychologists Press: Palo Alto, CA.Google Scholar
Spitzer, RL, Williams, GB, Gibbon, M (2002). Structured Clinical Interview for the DSM-IV. New York State Psychiatric Institute: New York.Google Scholar
Suls, J, Bunde, J (2005). Anger, anxiety, and depression as risk factors for cardiovascular disease: the problems and implications of overlapping affective dispositions. Psychological Bulletin 131, 260–300.CrossRefGoogle ScholarPubMed
Taylor, CB (2010). Depression, heart rate related variables and cardiovascular disease. International Journal of Psychophysiology 78, 80–88.CrossRefGoogle ScholarPubMed
Thayer, JF, Brosschot, JF (2005). Psychosomatics and psychopathology: looking up and down from the brain. Psychoneuroendocrinology 30, 1050–1058.CrossRefGoogle ScholarPubMed
Thayer, JF, Lane, RD (2007). The role of vagal function in the risk for cardiovascular disease and mortality. Biological Psychology 74, 224–242.CrossRefGoogle ScholarPubMed
Thayer, JF, Lane, RD (2009). Claude Bernard and the heart-brain connection: further elaboration of a model of neurovisceral integration. Neurosciences and Biobehavioural Reviews 33, 81–88.CrossRefGoogle Scholar
Thayer, JF, Sternberg, E (2006). Beyond heart rate variability: vagal regulation of allostatic systems. Annals of the New York Academy of Sciences 1088, 361–372.CrossRefGoogle ScholarPubMed
Verkuil, B, Brosschot, JF, de Beurs, DP, Thayer, JF (2009). Effects of explicit and implicit perseverative cognition on cardiac recovery after cognitive stress. International Journal of Psychophysiology 74, 220–228.CrossRefGoogle ScholarPubMed
Volokhov, RN, Demaree, HA (2010). Spontaneous emotion regulation to positive and negative stimuli. Brain and Cognition 73, 1–6.CrossRefGoogle ScholarPubMed
Wager, TD, van Ast, VA, Hughes, BL, Davidson, ML, Lindquist, MA, Ochsner, KN (2009 a). Brain mediators of cardiovascular responses to social threat. Part II: Prefrontal-subcortical pathways and relationship with anxiety. NeuroImage 47, 836–851.CrossRefGoogle ScholarPubMed
Wager, TD, Waugh, CE, Lindquist, M, Noll, DC, Fredrickson, BL, Taylor, SF (2009 b). 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 47, 821–835.CrossRefGoogle ScholarPubMed
Wallentin, M, Nielsen, AH, Vuust, P, Dohn, A, Roepstorff, A, Lund, TE (2011). Amygdala and heart rate variability responses from listening to emotionally intense parts of a story. NeuroImage 58, 963–973.CrossRefGoogle ScholarPubMed
Watkins, LL, Blumenthal, JA, Babyak, MA, Davidson, JRT, McCants, Jr. CB, O'Connor, C, Sketch, MH Jr. (2010). Phobic anxiety and increased risk of mortality in coronary heart disease. Psychosomatic Medicine 72, 664–671.CrossRefGoogle ScholarPubMed
Waugh, CE, Panage, S, Mendes, WB, Gotlib, IH (2010). Cardiovascular and affective recovery from anticipatory threat. Biological Psychology 84, 169–175.CrossRefGoogle ScholarPubMed
Weisman, AN, Beck, AT (1978). Development and Validation of the Dysfunctional Attitudes Scale: A Preliminary Investigation. American Education Research Association: Toronto, Canada.Google Scholar
Western, D, Taggart, P, Hanson, B (2010). Real-Time Feedback of Dynamic Cardiac Repolarization Properties. Engineering in Medicine and Biology, EMBC: Buenos Aires, Argentina.CrossRefGoogle ScholarPubMed
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