Heart and Brain Interaction of Psychiatric Illness: A Review Focused on Heart Rate Variability, Cognitive Function, and Quantitative Electroencephalography

Wookyoung Jung, Kuk-In Jang, Seung-Hwan Lee, Wookyoung Jung, Kuk-In Jang, Seung-Hwan Lee

Abstract

Heart rate variability (HRV) reflects beat-to-beat variability in the heart rate due to the dynamic interplay of the sympathetic and parasympathetic nervous systems. HRV is considered an index of the functional status of the autonomic nervous system. A decrease in HRV is thus observed in individuals with autonomic dysfunction. Abnormal HRV has been reported in a range of mental disorders. In this review, we give an overview of HRV in patients with major depressive disorder (MDD), schizophrenia, and posttraumatic stress disorder (PTSD), one of whose core symptoms is cognitive dysfunction. The association between HRV and cognitive function is highlighted in this review. This review consists of three main sections. In the first section, we examine how HRV in patients with MDD, schizophrenia, and PTSD is characterized, and how it is different when compared to that in healthy controls. In the second section, beyond the heart itself, we discuss the intimate connection between the heart and the brain, focusing on how HRV interacts with quantitative electroencephalography (qEEG) in the context of physiological changes in the sleep cycle. Lastly, we finish the review with the examination of the association between HRV and cognitive function. The overall findings indicate that the reduction in HRV is one of main manifestations in MDD, schizophrenia, and PTSD, and also more generally HRV is closely linked to the change in qEEG and also to individual differences in cognitive performance.

Keywords: Cognition.; Electroencephalography; Heart rate variability; Major depressive disorder; Posttraumatic stress disorder; Schizophrenia.

Conflict of interest statement

Conflicts of Interest

No potential conflict of interest relevant to this article was reported.

Figures

Fig. 1
Fig. 1
Conceptual model of connection of brain (qEEG), heart (HRV), and cognitive function. qEEG, quantitative electroencephalography; MDD, major depressive disorder; PTSD, posttraumatic stress disorder; HRV, heart rate variability.

References

    1. Berntson GG, Bigger JT, Jr, Eckberg DL, Grossman P, Kaufmann PG, Malik M, et al. Heart rate variability: origins, methods, and interpretive caveats. Psychophysiology. 1997;34:623–648. doi: 10.1111/j.1469-8986.1997.tb02140.x.
    1. McCorry LK. Physiology of the autonomic nervous system. Am J Pharm Educ. 2007;71:78. doi: 10.5688/aj710478.
    1. McCraty R, Shaffer F. Heart rate variability: new perspectives on physiological mechanisms, assessment of self-regulatory capacity, and health risk. Glob Adv Health Med. 2015;4:46–61. doi: 10.7453/gahmj.2014.073.
    1. Singer DH, Martin GJ, Magid N, Weiss JS, Schaad JW, Kehoe R, et al. Low heart rate variability and sudden cardiac death. J Electrocardiol. 1988;21( Suppl):S46–S55. doi: 10.1016/0022-0736(88)90055-6.
    1. Thayer JF, Hansen AL, Saus-Rose E, Johnsen BH. Heart rate variability, prefrontal neural function, and cognitive performance: the neurovisceral integration perspective on self-regulation, adaptation, and health. Ann Behav Med. 2009;37:141–153. doi: 10.1007/s12160-009-9101-z.
    1. Sztajzel J. Heart rate variability: a noninvasive electrocardiographic method to measure the autonomic nervous system. Swiss Med Wkly. 2004;134:514–522.
    1. Niskanen JP, Tarvainen MP, Ranta-Aho PO, Karjalainen PA. Software for advanced HRV analysis. Comput Methods Programs Biomed. 2004;76:73–81. doi: 10.1016/j.cmpb.2004.03.004.
    1. Malliani A, Lombardi F, Pagani M. Power spectrum analysis of heart rate variability: a tool to explore neural regulatory mechanisms. Br Heart J. 1994;71:1–2. doi: 10.1136/hrt.71.1.1.
    1. Eckberg DL. Sympathovagal balance: a critical appraisal. Circulation. 1997;96:3224–3232. doi: 10.1161/01.CIR.96.9.3224.
    1. Kuusela T. Methodological aspects of heart rate variability analysis. In: Kamath MV, Watanabe M, Upton A, editors. Heart rate variability (HRV) signal analysis: clinical applications. Boca Raton: CRC Press; 2013. pp. 10–42.
    1. Beckers F, Ramaekers D, Aubert AE. Approximate entropy of heart rate variability: validation of methods and application in heart failure. Cardiovasc Eng. 2001;1:177–182. doi: 10.1023/A:1015212328405.
    1. Malliani A, Pagani M, Lombardi F, Cerutti S. Cardiovascular neural regulation explored in the frequency domain. Circulation. 1991;84:482–492. doi: 10.1161/01.CIR.84.2.482.
    1. Pagani M, Lombardi F, Guzzetti S, Rimoldi O, Furlan R, Pizzinelli P, et al. Power spectral analysis of heart rate and arterial pressure variabilities as a marker of sympathovagal interaction in man and conscious dog. Circ Res. 1986;59:178–193. doi: 10.1161/01.RES.59.2.178.
    1. Reyes del Paso GA, Langewitz W, Mulder LJ, van Roon A, Duschek S. The utility of low frequency heart rate variability as an index of sympathetic cardiac tone: a review with emphasis on a reanalysis of previous studies. Psychophysiology. 2013;50:477–487. doi: 10.1111/psyp.12027.
    1. Houle MS, Billman GE. Low-frequency component of the heart rate variability spectrum: a poor marker of sympathetic activity. Am J Physiol. 1999;276:H215–H223.
    1. Levy MN. Autonomic interactions in cardiac control. Ann N Y Acad Sci. 1990;601:209–221. doi: 10.1111/j.1749-6632.1990.tb37302.x.
    1. Malik M, Bigger JT, Camm J, Kleiger RE, Malliani A, Moss AJ, et al. 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. Eur Heart J. 1996;17:354–381. doi: 10.1093/oxfordjournals.eurheartj.a014868.
    1. Nolan J, Batin PD, Andrews R, Lindsay SJ, Brooksby P, Mullen M, et al. 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. 1998;98:1510–1516. doi: 10.1161/01.CIR.98.15.1510.
    1. de Bruyne MC, Kors JA, Hoes AW, Klootwijk P, Dekker JM, Hofman A, et al. Both decreased and increased heart rate variability on the standard 10-second electrocardiogram predict cardiac mortality in the elderly: the Rotterdam Study. Am J Epidemiol. 1999;150:1282–1288. doi: 10.1093/oxfordjournals.aje.a009959.
    1. Dekker JM, Schouten EG, Klootwijk P, Pool J, Swenne CA, Kromhout D. Heart rate variability from short electrocardiographic recordings predicts mortality from all causes in middle-aged and elderly men. The Zutphen Study. Am J Epidemiol. 1997;145:899–908. doi: 10.1093/oxfordjournals.aje.a009049.
    1. Thayer JF, Sternberg E. Beyond heart rate variability: vagal regulation of allostatic systems. Ann N Y Acad Sci. 2006;1088:361–372. doi: 10.1196/annals.1366.014.
    1. Thayer JF, Lane RD. The role of vagal function in the risk for cardiovascular disease and mortality. Biol Psychol. 2007;74:224–242. doi: 10.1016/j.biopsycho.2005.11.013.
    1. La Rovere MT, Pinna GD, Maestri R, Mortara A, Capomolla S, Febo O, et al. Short-term heart rate variability strongly predicts sudden cardiac death in chronic heart failure patients. Circulation. 2003;107:565–570. doi: 10.1161/01.CIR.0000047275.25795.17.
    1. Hillebrand S, Gast KB, de Mutsert R, Swenne CA, Jukema JW, Middeldorp S, et al. Heart rate variability and first cardiovascular event in populations without known cardiovascular disease: meta-analysis and dose-response meta- regression. Europace. 2013;15:742–749. doi: 10.1093/europace/eus341.
    1. Barch D. 7. The neural mechanisms of cognitive control in psychosis. Schizophr Bull. 2017;43(Suppl 1):S9. doi: 10.1093/schbul/sbx021.026.
    1. Zalesky A, Fornito A, Seal ML, Cocchi L, Westin CF, Bullmore ET, et al. Disrupted axonal fiber connectivity in schizophrenia. Biol Psychiatry. 2011;69:80–89. doi: 10.1016/j.biopsych.2010.08.022.
    1. Do J, Woo J. From gut to brain: alteration in inflammation markers in the brain of dextran sodium sulfate-induced colitis model mice. Clin Psychopharmacol Neurosci. 2018;16:422–433. doi: 10.9758/cpn.2018.16.4.422.
    1. Dumont M, Jurysta F, Lanquart JP, Noseda A, van de Borne P, Linkowski P. Scale-free dynamics of the synchronization between sleep EEG power bands and the high frequency component of heart rate variability in normal men and patients with sleep apnea-hypopnea syndrome. Clin Neurophysiol. 2007;118:2752–2764. doi: 10.1016/j.clinph.2007.08.018.
    1. da Silva VP, Ramalho Oliveira BR, Tavares Mello RG, Moraes H, Deslandes AC, Laks J. Heart rate variability indexes in dementia: a systematic review with a quantitative analysis. Curr Alzheimer Res. 2018;15:80–88.
    1. Thayer JF, Lane RD. Claude Bernard and the heart-brain connection: further elaboration of a model of neurovisceral integration. Neurosci Biobehav Rev. 2009;33:81–88. doi: 10.1016/j.neubiorev.2008.08.004.
    1. Shaffer F, McCraty R, Zerr CL. A healthy heart is not a metronome: an integrative review of the heart’s anatomy and heart rate variability. Front Psychol. 2014;5:1040. doi: 10.3389/fpsyg.2014.01040.
    1. Nikolin S, Boonstra TW, Loo CK, Martin D. Combined effect of prefrontal transcranial direct current stimulation and a working memory task on heart rate variability. PLoS One. 2017;12:e0181833. doi: 10.1371/journal.pone.0181833.
    1. Mashin VA, Mashina MN. Analysis of the heart rate variability in negative functional states in the course of psychological relaxation sessions. Hum Physiol. 2000;26:420. doi: 10.1007/BF02760270.
    1. Appelhans BM, Luecken LJ. Heart rate variability and pain: associations of two interrelated homeostatic processes. Biol Psychol. 2008;77:174–182. doi: 10.1016/j.biopsycho.2007.10.004.
    1. Appelhans BM, Luecken LJ. Heart rate variability as an index of regulated emotional responding. Rev Gen Psychol. 2006;10:229–240. doi: 10.1037/1089-2680.10.3.229.
    1. Frazier TW, Strauss ME, Steinhauer SR. Respiratory sinus arrhythmia as an index of emotional response in young adults. Psychophysiology. 2004;41:75–83. doi: 10.1046/j.1469-8986.2003.00131.x.
    1. Urakawa K, Yokoyama K. Music can enhance exercise-induced sympathetic dominancy assessed by heart rate variability. Tohoku J Exp Med. 2005;206:213–218. doi: 10.1620/tjem.206.213.
    1. Chambers AS, Allen JJ. Vagal tone as an indicator of treatment response in major depression. Psychophysiology. 2002;39:861–864. doi: 10.1111/1469-8986.3960861.
    1. Riganello F, Dolce G, Garbarino S, Sannita W. Heart rate variability and the two-way interaction between CNS and the central autonomic network. Exp Clin Cardiol. 2014;20:5584–5595.
    1. Carney RM, Rich MW, Tevelde A, Saini J, Clark K, Jaffe AS. Major depressive disorder in coronary artery disease. Am J Cardiol. 1987;60:1273–1275. doi: 10.1016/0002-9149(87)90607-2.
    1. Gonzalez MB, Snyderman TB, Colket JT, Arias RM, Jiang JW, O’Connor CM, et al. Depression in patients with coronary artery disease. Depression. 1996;4:57–62. doi: 10.1002/(SICI)1522-7162(1996)4:2<57::AID-DEPR3>;2-C.
    1. Pratt LA, Ford DE, Crum RM, Armenian HK, Gallo JJ, Eaton WW. Depression, psychotropic medication, and risk of myocardial infarction. Prospective data from the Baltimore ECA follow-up. Circulation. 1996;94:3123–3129. doi: 10.1161/01.CIR.94.12.3123.
    1. Anda R, Williamson D, Jones D, Macera C, Eaker E, Glassman A, et al. Depressed affect, hopelessness, and the risk of ischemic heart disease in a cohort of U.S. adults. Epidemiology. 1993;4:285–294. doi: 10.1097/00001648-199307000-00003.
    1. Barefoot JC, Helms MJ, Mark DB, Blumenthal JA, Califf RM, Haney TL, et al. Depression and long-term mortality risk in patients with coronary artery disease. Am J Cardiol. 1996;78:613–617. doi: 10.1016/S0002-9149(96)00380-3.
    1. Penninx BW, Beekman AT, Honig A, Deeg DJ, Schoevers RA, van Eijk JT, et al. Depression and cardiac mortality: results from a community-based longitudinal study. Arch Gen Psychiatry. 2001;58:221–227. doi: 10.1001/archpsyc.58.3.221.
    1. Agelink MW, Boz C, Ullrich H, Andrich J. Relationship between major depression and heart rate variability. Clinical consequences and implications for antidepressive treatment. Psychiatry Res. 2002;113:139–149. doi: 10.1016/S0165-1781(02)00225-1.
    1. Hon EH, Lee ST. Electronic evaluation of the fetal heart rate. Viii. Patterns preceding fetal death, further observations. Am J Obstet Gynecol. 1963;87:814–826.
    1. Reynard A, Gevirtz R, Berlow R, Brown M, Boutelle K. Heart rate variability as a marker of self-regulation. Appl Psychophysiol Biofeedback. 2011;36:209–215. doi: 10.1007/s10484-011-9162-1.
    1. Segerstrom SC, Nes LS. Heart rate variability reflects self-regulatory strength, effort, and fatigue. Psychol Sci. 2007;18:275–281. doi: 10.1111/j.1467-9280.2007.01888.x.
    1. Kemp AH, Quintana DS, Gray MA, Felmingham KL, Brown K, Gatt JM. Impact of depression and antidepressant treatment on heart rate variability: a review and meta-analysis. Biol Psychiatry. 2010;67:1067–1074. doi: 10.1016/j.biopsych.2009.12.012.
    1. Rottenberg J. Cardiac vagal control in depression: a critical analysis. Biol Psychol. 2007;74:200–211. doi: 10.1016/j.biopsycho.2005.08.010.
    1. Koenig J, Kemp AH, Beauchaine TP, Thayer JF, Kaess M. Depression and resting state heart rate variability in children and adolescents - a systematic review and meta-analysis. Clin Psychol Rev. 2016;46:136–150. doi: 10.1016/j.cpr.2016.04.013.
    1. Dalack GW, Roose SP. Perspectives on the relationship between cardiovascular disease and affective disorder. J Clin Psychiatry. 1990;51( Suppl):4–9. discussion 10–11.
    1. Rechlin T, Weis M, Claus D. Heart rate variability in depressed patients and differential effects of paroxetine and amitriptyline on cardiovascular autonomic functions. Pharmacopsychiatry. 1994;27:124–128. doi: 10.1055/s-2007-1014291.
    1. Guinjoan SM, Bernabó JL, Cardinali DP. Cardiovascular tests of autonomic function and sympathetic skin responses in patients with major depression. J Neurol Neurosurg Psychiatry. 1995;59:299–302. doi: 10.1136/jnnp.59.3.299.
    1. Tulen JH, Bruijn JA, de Man KJ, van der Velden E, Pepplinkhuizen L, Man in ’t Veld AJ. Anxiety and autonomic regulation in major depressive disorder: an exploratory study. J Affect Disord. 1996;40:61–71. doi: 10.1016/0165-0327(96)00042-0.
    1. Stein PK, Carney RM, Freedland KE, Skala JA, Jaffe AS, Kleiger RE, et al. Severe depression is associated with markedly reduced heart rate variability in patients with stable coronary heart disease. J Psychosom Res. 2000;48:493–500. doi: 10.1016/S0022-3999(99)00085-9.
    1. Yeragani VK, Pohl R, Balon R, Ramesh C, Glitz D, Jung I, et al. Heart rate variability in patients with major depression. Psychiatry Res. 1991;37:35–46. doi: 10.1016/0165-1781(91)90104-W.
    1. Moser M, Lehofer M, Hoehn-Saric R, McLeod DR, Hildebrandt G, Steinbrenner B, et al. Increased heart rate in depressed subjects in spite of unchanged autonomic balance? J Affect Disord. 1998;48:115–124. doi: 10.1016/S0165-0327(97)00164-X.
    1. Moon E, Lee SH, Kim DH, Hwang B. Comparative study of heart rate variability in patients with schizophrenia, bipolar disorder, post-traumatic stress disorder, or major depressive disorder. Clin Psychopharmacol Neurosci. 2013;11:137–143. doi: 10.9758/cpn.2013.11.3.137.
    1. van Zyl LT, Hasegawa T, Nagata K. Effects of antidepressant treatment on heart rate variability in major depression: a quantitative review. Biopsychosoc Med. 2008;2:12. doi: 10.1186/1751-0759-2-12.
    1. Lederbogen F, Gernoth C, Weber B, Colla M, Kniest A, Heuser I, et al. Antidepressive treatment with amitriptyline and paroxetine: comparable effects on heart rate variability. J Clin Psychopharmacol. 2001;21:238–239. doi: 10.1097/00004714-200104000-00018.
    1. Khaykin Y, Dorian P, Baker B, Shapiro C, Sandor P, Mironov D, et al. Autonomie correlates of antidepressant treatment using heart-rate variability analysis. Can J Psychiatry. 1998;43:183–186. doi: 10.1177/070674379804300209.
    1. Licht CM, de Geus EJ, Zitman FG, Hoogendijk WJ, van Dyck R, Penninx BW. Association between major depressive disorder and heart rate variability in the Netherlands Study of Depression and Anxiety (NESDA) Arch Gen Psychiatry. 2008;65:1358–1367. doi: 10.1001/archpsyc.65.12.1358.
    1. Licht CM, de Geus EJ, van Dyck R, Penninx BW. Longitudinal evidence for unfavorable effects of antidepressants on heart rate variability. Biol Psychiatry. 2010;68:861–868. doi: 10.1016/j.biopsych.2010.06.032.
    1. O’Regan C, Kenny RA, Cronin H, Finucane C, Kearney PM. Antidepressants strongly influence the relationship between depression and heart rate variability: findings from the Irish Longitudinal Study on Ageing (TILDA) Psychol Med. 2015;45:623–636. doi: 10.1017/S0033291714001767.
    1. Bär KJ, Letzsch A, Jochum T, Wagner G, Greiner W, Sauer H. Loss of efferent vagal activity in acute schizophrenia. J Psychiatr Res. 2005;39:519–527. doi: 10.1016/j.jpsychires.2004.12.007.
    1. Chang JS, Yoo CS, Yi SH, Hong KH, Oh HS, Hwang JY, et al. Differential pattern of heart rate variability in patients with schizophrenia. Prog Neuropsychopharmacol Biol Psychiatry. 2009;33:991–995. doi: 10.1016/j.pnpbp.2009.05.004.
    1. Jindal R, MacKenzie EM, Baker GB, Yeragani VK. Cardiac risk and schizophrenia. J Psychiatry Neurosci. 2005;30:393–395.
    1. Clamor A, Lincoln TM, Thayer JF, Koenig J. Resting vagal activity in schizophrenia: meta-analysis of heart rate variability as a potential endophenotype. Br J Psychiatry. 2016;208:9–16. doi: 10.1192/bjp.bp.114.160762.
    1. Valkonen-Korhonen M, Tarvainen MP, Ranta-Aho P, Karjalainen PA, Partanen J, Karhu J, et al. Heart rate variability in acute psychosis. Psychophysiology. 2003;40:716–726. doi: 10.1111/1469-8986.00072.
    1. Hempel RJ, Tulen JH, van Beveren NJ, Röder CH, Hengeveld MW. Cardiovascular variability during treatment with haloperidol, olanzapine or risperidone in recent-onset schizophrenia. J Psychopharmacol. 2009;23:697–707. doi: 10.1177/0269881108091254.
    1. Kim JH, Ann JH, Lee J. Relationship between heart rate variability and the severity of psychotic symptoms in schizophrenia. Acta Neuropsychiatr. 2011;23:161–166. doi: 10.1111/j.1601-5215.2011.00549.x.
    1. Chung MS, Yang AC, Lin YC, Lin CN, Chang FR, Shen SH, et al. Association of altered cardiac autonomic function with psychopathology and metabolic profiles in schizophrenia. Psychiatry Res. 2013;210:710–715. doi: 10.1016/j.psychres.2013.07.034.
    1. Cohen H, Loewenthal U, Matar M, Kotler M. Association of autonomic dysfunction and clozapine. Heart rate variability and risk for sudden death in patients with schizophrenia on long-term psychotropic medication. Br J Psychiatry. 2001;179:167–171. doi: 10.1192/bjp.179.2.167.
    1. Mueck-Weymann M, Rechlin T, Ehrengut F, Rauh R, Acker J, Dittmann RW, et al. Effects of olanzapine and clozapine upon pulse rate variability. Depress Anxiety. 2002;16:93–99. doi: 10.1002/da.10037.
    1. Rechlin T, Beck G, Weis M, Kaschka WP. Correlation between plasma clozapine concentration and heart rate variability in schizophrenic patients. Psychopharmacology (Berl) 1998;135:338–341. doi: 10.1007/s002130050520.
    1. Mujica-Parodi LR, Yeragani V, Malaspina D. Nonlinear complexity and spectral analyses of heart rate variability in medicated and unmedicated patients with schizophrenia. Neuropsychobiology. 2005;51:10–15. doi: 10.1159/000082850.
    1. Malaspina D, Dalack G, Leitman D, Corcoran C, Amador XF, Yale S, et al. Low heart rate variability is not caused by typical neuroleptics in schizophrenia patients. CNS Spectr. 2002;7:53–57. doi: 10.1017/S1092852900022264.
    1. Alvares GA, Quintana DS, Hickie IB, Guastella AJ. Autonomic nervous system dysfunction in psychiatric disorders and the impact of psychotropic medications: a systematic review and meta-analysis. J Psychiatry Neurosci. 2016;41:89–104. doi: 10.1503/jpn.140217.
    1. Cohen H, Kotler M, Matar MA, Kaplan Z, Miodownik H, Cassuto Y. Power spectral analysis of heart rate variability in posttraumatic stress disorder patients. Biol Psychiatry. 1997;41:627–629. doi: 10.1016/S0006-3223(96)00525-2.
    1. Cohen H, Kotler M, Matar MA, Kaplan Z, Loewenthal U, Miodownik H, et al. Analysis of heart rate variability in post-traumatic stress disorder patients in response to a trauma-related reminder. Biol Psychiatry. 1998;44:1054–1059. doi: 10.1016/S0006-3223(97)00475-7.
    1. Cohen H, Kotler M, Matar M, Kaplan Z. Normalization of heart rate variability in post-traumatic stress disorder patients following fluoxetine treatment: preliminary results. Isr Med Assoc J. 2000;2:296–301.
    1. Cohen H, Benjamin J, Geva AB, Matar MA, Kaplan Z, Kotler M. Autonomic dysregulation in panic disorder and in post- traumatic stress disorder: application of power spectrum analysis of heart rate variability at rest and in response to recollection of trauma or panic attacks. Psychiatry Res. 2000;96:1–13. doi: 10.1016/S0165-1781(00)00195-5.
    1. Blechert J, Michael T, Grossman P, Lajtman M, Wilhelm FH. Autonomic and respiratory characteristics of posttraumatic stress disorder and panic disorder. Psychosom Med. 2007;69:935–943. doi: 10.1097/PSY.0b013e31815a8f6b.
    1. Hauschildt M, Peters MJ, Moritz S, Jelinek L. Heart rate variability in response to affective scenes in posttraumatic stress disorder. Biol Psychol. 2011;88:215–222. doi: 10.1016/j.biopsycho.2011.08.004.
    1. Hopper JW, Spinazzola J, Simpson WB, van der Kolk BA. Preliminary evidence of parasympathetic influence on basal heart rate in posttraumatic stress disorder. J Psychosom Res. 2006;60:83–90. doi: 10.1016/j.jpsychores.2005.06.002.
    1. Tan G, Fink B, Dao TK, Hebert R, Farmer LS, Sanders A, et al. Associations among pain, PTSD, mTBI, and heart rate variability in veterans of Operation Enduring and Iraqi Freedom: a pilot study. Pain Med. 2009;10:1237–1245. doi: 10.1111/j.1526-4637.2009.00712.x.
    1. Keary TA, Hughes JW, Palmieri PA. Women with post-traumatic stress disorder have larger decreases in heart rate variability during stress tasks. Int J Psychophysiol. 2009;73:257–264. doi: 10.1016/j.ijpsycho.2009.04.003.
    1. Sahar T, Shalev AY, Porges SW. Vagal modulation of responses to mental challenge in posttraumatic stress disorder. Biol Psychiatry. 2001;49:637–643. doi: 10.1016/S0006-3223(00)01045-3.
    1. Kamkwalala A, Norrholm SD, Poole JM, Brown A, Donley S, Duncan E, et al. Dark-enhanced startle responses and heart rate variability in a traumatized civilian sample: putative sex-specific correlates of posttraumatic stress disorder. Psychosom Med. 2012;74:153–159. doi: 10.1097/PSY.0b013e318240803a.
    1. Ballenger JC, Davidson JR, Lecrubier Y, Nutt DJ, Foa EB, Kessler RC, et al. Consensus statement on posttraumatic stress disorder from the International Consensus Group on Depression and Anxiety. J Clin Psychiatry. 2000;61( Suppl 5):60–66.
    1. Dennis PA, Watkins LL, Calhoun PS, Oddone A, Sherwood A, Dennis MF, et al. Posttraumatic stress, heart rate variability, and the mediating role of behavioral health risks. Psychosom Med. 2014;76:629–637. doi: 10.1097/PSY.0000000000000110.
    1. Chang HA, Chang CC, Tzeng NS, Kuo TB, Lu RB, Huang SY. Decreased cardiac vagal control in drug-naïve patients with posttraumatic stress disorder. Psychiatry Investig. 2013;10:121–130. doi: 10.4306/pi.2013.10.2.121.
    1. Sack M, Hopper JW, Lamprecht F. Low respiratory sinus arrhythmia and prolonged psychophysiological arousal in posttraumatic stress disorder: heart rate dynamics and individual differences in arousal regulation. Biol Psychiatry. 2004;55:284–290. doi: 10.1016/S0006-3223(03)00677-2.
    1. Buckley TC, Kaloupek DG. A meta-analytic examination of basal cardiovascular activity in posttraumatic stress disorder. Psychosom Med. 2001;63:585–594. doi: 10.1097/00006842-200107000-00011.
    1. Pole N. The psychophysiology of posttraumatic stress disorder: a meta-analysis. Psychol Bull. 2007;133:725–746. doi: 10.1037/0033-2909.133.5.725.
    1. Malik M, Farrell T, Camm AJ. Circadian rhythm of heart rate variability after acute myocardial infarction and its influence on the prognostic value of heart rate variability. Am J Cardiol. 1990;66:1049–1054. doi: 10.1016/0002-9149(90)90503-S.
    1. Huikuri HV, Niemelä MJ, Ojala S, Rantala A, Ikäheimo MJ, Airaksinen KE. Circadian rhythms of frequency domain measures of heart rate variability in healthy subjects and patients with coronary artery disease. Effects of arousal and upright posture. Circulation. 1994;90:121–126. doi: 10.1161/01.CIR.90.1.121.
    1. Vanoli E, Adamson PB, Ba-Lin, Pinna GD, Lazzara R, Orr WC. Heart rate variability during specific sleep stages. A comparison of healthy subjects with patients after myocardial infarction. Circulation. 1995;91:1918–1922. doi: 10.1161/01.CIR.91.7.1918.
    1. Tsunoda M, Endo T, Hashimoto S, Honma S, Honma KI. Effects of light and sleep stages on heart rate variability in humans. Psychiatry Clin Neurosci. 2001;55:285–286. doi: 10.1046/j.1440-1819.2001.00862.x.
    1. Bonnet MH, Arand DL. Heart rate variability: sleep stage, time of night, and arousal influences. Electroencephalogr Clin Neurophysiol. 1997;102:390–396. doi: 10.1016/S0921-884X(96)96070-1.
    1. Scholz UJ, Bianchi AM, Cerutti S, Kubicki S. Vegetative background of sleep: spectral analysis of the heart rate variability. Physiol Behav. 1997;62:1037–1043. doi: 10.1016/S0031-9384(97)00234-5.
    1. Kupfer DJ, Foster FG, Coble P, McPartland RJ, Ulrich RF. The application of EEG sleep for the differential diagnosis of affective disorders. Am J Psychiatry. 1978;135:69–74. doi: 10.1176/ajp.135.1.69.
    1. Feinberg M, Gillin JC, Carroll BJ, Greden JF, Zis AP. EEG studies of sleep in the diagnosis of depression. Biol Psychiatry. 1982;17:305–316.
    1. Shagass C, Roemer RA, Straumanis JJ. Relationships between psychiatric diagnosis and some quantitative EEG variables. Arch Gen Psychiatry. 1982;39:1423–1435. doi: 10.1001/archpsyc.1982.04290120053011.
    1. Boutros NN, Arfken C, Galderisi S, Warrick J, Pratt G, Iacono W. The status of spectral EEG abnormality as a diagnostic test for schizophrenia. Schizophr Res. 2008;99:225–237. doi: 10.1016/j.schres.2007.11.020.
    1. Ford MR, Goethe JW, Dekker DK. EEG coherence and power in the discrimination of psychiatric disorders and medication effects. Biol Psychiatry. 1986;21:1175–1188. doi: 10.1016/0006-3223(86)90224-6.
    1. Shagass C, Roemer RA, Straumanis JJ, Josiassen RC. Psychiatric diagnostic discriminations with combinations of quantitative EEG variables. Br J Psychiatry. 1984;144:581–592. doi: 10.1192/bjp.144.6.581.
    1. Pollock VE, Schneider LS. Quantitative, waking EEG research on depression. Biol Psychiatry. 1990;27:757–780. doi: 10.1016/0006-3223(90)90591-O.
    1. Nusslock R, Shackman AJ, McMenamin BW, Greischar LL, Davidson RJ, Kovacs M. Comorbid anxiety moderates the relationship between depression history and prefrontal EEG asymmetry. Psychophysiology. 2018;55:e12953. doi: 10.1111/psyp.12953.
    1. Loo SK, McGough JJ, McCracken JT, Smalley SL. Parsing heterogeneity in attention-deficit hyperactivity disorder using EEG-based subgroups. J Child Psychol Psychiatry. 2018;59:223–231. doi: 10.1111/jcpp.12814.
    1. Shim M, Im CH, Kim YW, Lee SH. Altered cortical functional network in major depressive disorder: a resting-state electroencephalogram study. Neuroimage Clin. 2018;19:1000–1007. doi: 10.1016/j.nicl.2018.06.012.
    1. Swatzyna RJ, Tarnow JD, Turner RP, Roark AJ, MacInerney EK, Kozlowski GP. Integration of EEG into psychiatric practice: a step toward precision medicine for autism spectrum disorder. J Clin Neurophysiol. 2017;34:230–235. doi: 10.1097/WNP.0000000000000365.
    1. Kim JW, Kim SY, Choi JW, Kim KM, Nam SH, Min KJ, et al. Differences in resting-state quantitative electroencephalography patterns in attention deficit/hyperactivity disorder with or without comorbid symptoms. Clin Psychopharmacol Neurosci. 2017;15:138–145. doi: 10.9758/cpn.2017.15.2.138.
    1. Miyashita T, Ogawa K, Itoh H, Arai Y, Ashidagawa M, Uchiyama M, et al. Spectral analyses of electroencephalography and heart rate variability during sleep in normal subjects. Auton Neurosci. 2003;103:114–120. doi: 10.1016/S1566-0702(02)00259-X.
    1. Barlow JS. Rhythmic activity induced by photic stimulation in relation to intrinsic alpha activity of the brain in man. Electroencephalogr Clin Neurophysiol. 1960;12:317–326. doi: 10.1016/0013-4694(60)90005-5.
    1. Laufs H, Kleinschmidt A, Beyerle A, Eger E, Salek-Haddadi A, Preibisch C, et al. EEG-correlated fMRI of human alpha activity. Neuroimage. 2003;19:1463–1476. doi: 10.1016/S1053-8119(03)00286-6.
    1. Boly M, Phillips C, Tshibanda L, Vanhaudenhuyse A, Schabus M, Dang-Vu TT, et al. Intrinsic brain activity in altered states of consciousness: how conscious is the default mode of brain function? Ann N Y Acad Sci. 2008;1129:119–129. doi: 10.1196/annals.1417.015.
    1. Rothenberger SD, Krafty RT, Taylor BJ, Cribbet MR, Thayer JF, Buysse DJ, et al. Time-varying correlations between delta EEG power and heart rate variability in midlife women: the SWAN Sleep Study. Psychophysiology. 2015;52:572–584. doi: 10.1111/psyp.12383.
    1. Chang JS, Yoo CS, Yi SH, Her JY, Choi HM, Ha TH, et al. An integrative assessment of the psychophysiologic alterations in young women with recurrent major depressive disorder. Psychosom Med. 2012;74:495–500. doi: 10.1097/PSY.0b013e31824d0da0.
    1. Yoon BW, Morillo CA, Cechetto DF, Hachinski V. Cerebral hemispheric lateralization in cardiac autonomic control. Arch Neurol. 1997;54:741–744. doi: 10.1001/archneur.1997.00550180055012.
    1. Hilz MJ, Dütsch M, Perrine K, Nelson PK, Rauhut U, Devinsky O. Hemispheric influence on autonomic modulation and baroreflex sensitivity. Ann Neurol. 2001;49:575–584. doi: 10.1002/ana.1006.
    1. Hannesdóttir DK, Doxie J, Bell MA, Ollendick TH, Wolfe CD. A longitudinal study of emotion regulation and anxiety in middle childhood: associations with frontal EEG asymmetry in early childhood. Dev Psychobiol. 2010;52:197–204.
    1. Wahbeh H, Oken BS. Peak high-frequency HRV and peak alpha frequency higher in PTSD. Appl Psychophysiol Biofeedback. 2013;38:57–69. doi: 10.1007/s10484-012-9208-z.
    1. Begić D, Hotujac L, Jokić-Begić N. Electroencephalographic comparison of veterans with combat-related post-traumatic stress disorder and healthy subjects. Int J Psychophysiol. 2001;40:167–172. doi: 10.1016/S0167-8760(00)00153-7.
    1. Jokić-Begić N, Begić D. Quantitative electroencephalogram (qEEG) in combat veterans with post-traumatic stress disorder (PTSD) Nord J Psychiatry. 2003;57:351–355. doi: 10.1080/08039480310002688.
    1. Bechara A, Naqvi N. Listening to your heart: interoceptive awareness as a gateway to feeling. Nat Neurosci. 2004;7:102–103. doi: 10.1038/nn0204-102.
    1. Critchley HD, Wiens S, Rotshtein P, Ohman A, Dolan RJ. Neural systems supporting interoceptive awareness. Nat Neurosci. 2004;7:189–195. doi: 10.1038/nn1176.
    1. McCraty R. Heart–brain neurodynamics: the making of emotions. Boulder Creek, CA: Institute of Heart Math Publication; 2003. pp. 3–15.
    1. Jin MJ, Kim JS, Kim S, Hyun MH, Lee SH. An integrated model of emotional problems, beta power of electroencephalography, and low frequency of heart rate variability after childhood trauma in a non-clinical sample: a path analysis study. Front Psychiatry. 2018;8:314. doi: 10.3389/fpsyt.2017.00314.
    1. Laborde S, Furley P, Schempp C. The relationship between working memory, reinvestment, and heart rate variability. Physiol Behav. 2015;139:430–436. doi: 10.1016/j.physbeh.2014.11.036.
    1. Friedman BH. An autonomic flexibility-neurovisceral integration model of anxiety and cardiac vagal tone. Biol Psychol. 2007;74:185–199. doi: 10.1016/j.biopsycho.2005.08.009.
    1. Thayer JF, Brosschot JF. Psychosomatics and psychopathology: looking up and down from the brain. Psychoneuroendocrinology. 2005;30:1050–1058. doi: 10.1016/j.psyneuen.2005.04.014.
    1. Thayer JF, Friedman BH. Stop that! Inhibition, sensitization, and their neurovisceral concomitants. Scand J Psychol. 2002;43:123–130. doi: 10.1111/1467-9450.00277.
    1. Jeon H, Lee SH. From neurons to social beings: short review of the mirror neuron system research and its socio-psychological and psychiatric implications. Clin Psychopharmacol Neurosci. 2018;16:18–31. doi: 10.9758/cpn.2018.16.1.18.
    1. Lane RD, McRae K, Reiman EM, Chen K, Ahern GL, Thayer JF. Neural correlates of heart rate variability during emotion. Neuroimage. 2009;44:213–222. doi: 10.1016/j.neuroimage.2008.07.056.
    1. Gianaros PJ, Van Der Veen FM, Jennings JR. 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. 2004;41:521–530. doi: 10.1111/1469-8986.2004.00179.x.
    1. Lane RD, Weidenbacher H, Fort CL, Thayer JF, Allen JJB. Subgenual anterior cingulate (BA25) activity covaries with changes in cardiac vagal tone during affective set shifting in healthy adults. Psychosom Med. 2008;70:A–42.
    1. Nugent AC, Bain EE, Thayer JF, Drevets WC. Anatomical correlates of autonomic control during a motor task. Psychosom Med. 2007;69:A–74.
    1. Nugent AC, Bain EE, Sollers JJ, Thaye rJF, Drevets WC. Alterations in neural correlates of autonomic control in females with major depressive disorder. Psychosom Med. 2008;70:A–99.
    1. Goldman-Rakic PS. Regional and cellular fractionation of working memory. Proc Natl Acad Sci U S A. 1996;93:13473–13480. doi: 10.1073/pnas.93.24.13473.
    1. Nagahama Y, Okada T, Katsumi Y, Hayashi T, Yamauchi H, Sawamoto N, et al. Transient neural activity in the medial superior frontal gyrus and precuneus time locked with attention shift between object features. Neuroimage. 1999;10:193–199. doi: 10.1006/nimg.1999.0451.
    1. Milham MP, Banich MT, Webb A, Barad V, Cohen NJ, Wszalek T, et al. The relative involvement of anterior cingulate and prefrontal cortex in attentional control depends on nature of conflict. Brain Res Cogn Brain Res. 2001;12:467–473. doi: 10.1016/S0926-6410(01)00076-3.
    1. Henson RN, Shallice T, Dolan RJ. Right prefrontal cortex and episodic memory retrieval: a functional MRI test of the monitoring hypothesis. Brain. 1999;122:1367–1381. doi: 10.1093/brain/122.7.1367.
    1. Gehring WJ, Willoughby AR. The medial frontal cortex and the rapid processing of monetary gains and losses. Science. 2002;295:2279–2282. doi: 10.1126/science.1066893.
    1. Sanfey AG, Rilling JK, Aronson JA, Nystrom LE, Cohen JD. The neural basis of economic decision-making in the Ultimatum Game. Science. 2003;300:1755–1758. doi: 10.1126/science.1082976.
    1. Mulert C, Seifert C, Leicht G, Kirsch V, Ertl M, Karch S, et al. Single-trial coupling of EEG and fMRI reveals the involvement of early anterior cingulate cortex activation in effortful decision making. Neuroimage. 2008;42:158–168. doi: 10.1016/j.neuroimage.2008.04.236.
    1. Rigoni D, Polezzi D, Rumiati R, Guarino R, Sartori G. When people matter more than money: an ERPs study. Brain Res Bull. 2010;81:445–452. doi: 10.1016/j.brainresbull.2009.12.003.
    1. Etkin A, Egner T, Kalisch R. Emotional processing in anterior cingulate and medial prefrontal cortex. Trends Cogn Sci. 2011;15:85–93. doi: 10.1016/j.tics.2010.11.004.
    1. Coles MG. Cardiac and respiratory activity during visual search. J Exp Psychol. 1972;96:371–379. doi: 10.1037/h0033603.
    1. Porges SW, Raskin DC. Respiratory and heart rate components of attention. J Exp Psychol. 1969;81:497–503. doi: 10.1037/h0027921.
    1. Porges SW, Humphrey MM. Cardiac and respiratory responses during visual search in nonretarded children and retarded adolescents. Am J Ment Defic. 1977;82:162–169.
    1. Porges SW, Arnold WR, Forbes EJ. Heart rate variability: an index of attentional responsivity in human newborns. Dev Psychol. 1973;8:85–92. doi: 10.1037/h0033793.
    1. Porges SW, Stamps LE, Walter GF. Heart rate variability and newborn heart rate responses to illumination changes. Dev Psychol. 1974;10:507–513. doi: 10.1037/h0036560.
    1. Hansen AL, Johnsen BH, Thayer JF. Vagal influence on working memory and attention. Int J Psychophysiol. 2003;48:263–274. doi: 10.1016/S0167-8760(03)00073-4.
    1. Thayer JF, Lane RD. A model of neurovisceral integration in emotion regulation and dysregulation. J Affect Disord. 2000;61:201–216. doi: 10.1016/S0165-0327(00)00338-4.
    1. Hansen AL, Johnsen BH, Thayer JF. Relationship between heart rate variability and cognitive function during threat of shock. Anxiety Stress Coping. 2009;22:77–89. doi: 10.1080/10615800802272251.
    1. Johnsen BH, Thayer JF, Laberg JC, Wormnes B, Raadal M, Skaret E, et al. Attentional and physiological characteristics of patients with dental anxiety. J Anxiety Disord. 2003;17:75–87. doi: 10.1016/S0887-6185(02)00178-0.
    1. Johnsen BH, Hansen AL, Murison R, Eid J, Thayer JF. Heart rate variability and cortisol responses during attentional and working memory tasks in naval cadets. Int Marit Health. 2012;63:181–187.
    1. Britton A, Singh-Manoux A, Hnatkova K, Malik M, Marmot MG, Shipley M. The association between heart rate variability and cognitive impairment in middle-aged men and women. Neuroepidemiology. 2008;31(2):115–21. doi: 10.1159/000148257.
    1. Jennings JR, Allen B, Gianaros PJ, Thayer JF, Manuck SB. Focusing neurovisceral integration: cognition, heart rate variability, and cerebral blood flow. Psychophysiology. 2015;52:214–224. doi: 10.1111/psyp.12319.
    1. Duschek S, Muckenthaler M, Werner N, del Paso GA. Relationships between features of autonomic cardiovascular control and cognitive performance. Biol Psychol. 2009;81:110–117. doi: 10.1016/j.biopsycho.2009.03.003.
    1. Kimhy D, Crowley OV, McKinley PS, Burg MM, Lachman ME, Tun PA, et al. The association of cardiac vagal control and executive functioning--findings from the MIDUS study. J Psychiatr Res. 2013;47:628–635. doi: 10.1016/j.jpsychires.2013.01.018.
    1. Mann SL, Selby EA, Bates ME, Contrada RJ. Integrating affective and cognitive correlates of heart rate variability: a structural equation modeling approach. Int J Psychophysiol. 2015;98:76–86. doi: 10.1016/j.ijpsycho.2015.07.003.
    1. Sandrone G, Mortara A, Torzillo D, La Rovere MT, Malliani A, Lombardi F. Effects of beta blockers (atenolol or metoprolol) on heart rate variability after acute myocardial infarction. Am J Cardiol. 1994;74:340–345. doi: 10.1016/0002-9149(94)90400-6.
    1. Stein PK, Ehsani AA, Domitrovich PP, Kleiger RE, Rottman JN. Effect of exercise training on heart rate variability in healthy older adults. Am Heart J. 1999;138:567–576. doi: 10.1016/S0002-8703(99)70162-6.
    1. Luft CD, Takase E, Darby D. Heart rate variability and cognitive function: effects of physical effort. Biol Psychol. 2009;82:164–168. doi: 10.1016/j.biopsycho.2009.07.007.
    1. Luque-Casado A, Zabala M, Morales E, Mateo-March M, Sanabria D. Cognitive performance and heart rate variability: the influence of fitness level. PLoS One. 2013;8:e56935. doi: 10.1371/journal.pone.0056935.
    1. Hansen AL, Johnsen BH, Sollers JJ, 3rd, Stenvik K, Thayer JF. Heart rate variability and its relation to prefrontal cognitive function: the effects of training and detraining. Eur J Appl Physiol. 2004;93:263–272. doi: 10.1007/s00421-004-1208-0.

Source: PubMed

3
S'abonner