Higher cardiovascular activation, but normal heartbeat-evoked potentials and cardiac interoceptive accuracy in somatoform disorders and major depressive disorder
[en] The perception-filter model posits that the generation of medically-unexplained symptoms is associated with (I.) more intense afferent bodily signals, (II.) impaired filter system activity to differentiate relevant from irrelevant signals, and (III.) altered perception of bodily signals. We tested these assumptions for cardiac perception in patients with somatoform disorders (SFD), patients with major depressive disorder (MDD) and healthy control (HC) individuals. Heart rate (variability; HR/HRV) and blood pressure served as indicators of bodily signals (I.); heartbeat-evoked potentials (HEPs) assessed during a heartbeat counting task (HCT) and a distraction task indicated filter system activity (II.); interoceptive accuracy (IAc) in the HCT was interpreted as an index of perception (III.). All indicators were assessed before and after a socially-evaluated cold pressor stress task (SECPT) and a control intervention. SFD patients (n = 24) showed higher average HR and diastolic blood pressure, as well as lower HRV than HC individuals (n = 22), but there were no differences in HEPs or IAc. Neither were there significant differences between the SFD and the MDD groups (n = 24), nor any stress effect on HEPs or IAc. Our findings suggest that increased intensity of bodily signals (I.) is the only model assumption that could be supported for patients with fully-developed SFD.
Disciplines :
Neurosciences & behavior
Author, co-author :
Schulz, André ; University of Luxembourg > Faculty of Humanities, Education and Social Sciences (FHSE) > Department of Behavioural and Cognitive Sciences (DBCS)
Dierolf, Angelika ; University of Luxembourg > Faculty of Humanities, Education and Social Sciences (FHSE) > Department of Behavioural and Cognitive Sciences (DBCS)
Lutz, Annika ; University of Luxembourg > Faculty of Humanities, Education and Social Sciences (FHSE) > Department of Behavioural and Cognitive Sciences (DBCS)
Voderholzer, Ulrich
Koch, Stefan
Bach, Michael
Asenstorfer, Carina
Michaux, Gilles
Mertens, Vera-Christina
Vögele, Claus ; University of Luxembourg > Faculty of Humanities, Education and Social Sciences (FHSE) > Department of Behavioural and Cognitive Sciences (DBCS)
External co-authors :
yes
Language :
English
Title :
Higher cardiovascular activation, but normal heartbeat-evoked potentials and cardiac interoceptive accuracy in somatoform disorders and major depressive disorder
Ainley, V., Tsakiris, M., Pollatos, O., Schulz, A., Herbert, B.M., 2020. Comment on "Zamariola et al. Interoceptive Accuracy Scores are Problematic: evidence from Simple Bivariate Correlations"-The empirical data base, the conceptual reasoning and the analysis behind this statement are misconceived and do not support the authors' conclusions. Biol. Psychol., 152, 2018, 107870, 10.1016/j.biopsycho.2020.107870.
American-Psychiatric-Association. Diagnostic and Statistical Manual of Mental Disorders: DSM-IV. 2000, American Psychiatric Publishing, Inc., Arlington, VA.
American-Psychiatric-Association. Diagnostic and Statistical Manual of Mental Disorders: DSM-5. 2013, American Psychiatric Publishing, Inc., Arlington, VA.
Barsky, A.J., Orav, E.J., Bates, D.W., Somatization increases medical utilization and costs independent of psychiatric and medical comorbidity. Arch. Gen. Psychiatr. 62:8 (2005), 903–910, 10.1001/archpsyc.62.8.903.
Baumeister, H., Harter, M., Prevalence of mental disorders based on general population surveys. Soc. Psychiatr. Psychiatr. Epidemiol. 42:7 (2007), 537–546, 10.1007/s00127-007-0204-1.
Beck, A.T., Steer, R., Brown, G.K., Beck Depression Inventory (BDI-II). 1996, Psychological Corporation, San Antonio (TX).
Chatrian, G.E., Lettich, E., Nelson, P.L., Modified nomenclature for the “10%” electrode system. J. Clin. Neurophysiol. 5:2 (1988), 183–186, 10.1097/00004691-198804000-00005.
Coll, M.P., Hobson, H., Bird, G., Murphy, J., Systematic review and meta-analysis of the relationship between the heartbeat-evoked potential and interoception. Neurosci. Biobehav. Rev., 2021, 10.1016/j.neubiorev.2020.12.012.
Craig, A.D., How do you feel? Interoception: the sense of the physiological condition of the body. Nat. Rev. Neurosci. 3:8 (2002), 655–666, 10.1038/nrn894.
Desmedt, O., Corneille, O., Luminet, O., Murphy, J., Bird, G., Maurage, P., Contribution of time estimation and knowledge to heartbeat counting task performance under original and adapted instructions. Biol. Psychol., 154, 2020, 107904, 10.1016/j.biopsycho.2020.107904.
Desmedt, O., Luminet, O., Corneille, O., The heartbeat counting task largely involves non-interoceptive processes: evidence from both the original and an adapted counting task. Biol. Psychol. 138 (2018), 185–188, 10.1016/j.biopsycho.2018.09.004.
Dirlich, G., Vogl, L., Plaschke, M., Strian, F., Cardiac field effects on the EEG. Electroencephalogr. Clin. Neurophysiol. Suppl. 102:4 (1997), 307–315, 10.1016/S0013-4694(96)96506-2.
Dressendorfer, R.A., Kirschbaum, C., Rohde, W., Stahl, F., Strasburger, C.J., Synthesis of a cortisol-biotin conjugate and evaluation as a tracer in an immunoassay for salivary cortisol measurement. J. Steroid Biochem. Mol. Biol. 43:7 (1992), 683–692, 10.1016/0960-0760(92)90294-S.
Dunn, B.D., Stefanovitch, I., Evans, D., Oliver, C., Hawkins, A., Dalgleish, T., Can you feel the beat? Interoceptive awareness is an interactive function of anxiety- and depression-specific symptom dimensions. Behav. Res. Ther. 48:11 (2010), 1133–1138, 10.1016/j.brat.2010.07.006.
Flasinski, T., Dierolf, A.M., Rost, S., Lutz, A.P.C., Voderholzer, U., Koch, S., Bach, M., Asenstorfer, C., Münch, E.E., Mertens, V.C., Vögele, C., Schulz, A., Altered interoceptive awareness in high habitual symptom reporters and patients with somatoform disorders. Front. Psychol., 11, 2020, 1859, 10.3389/fpsyg.2020.01859.
Fröhlich, C., Jacobi, F., Wittchen, H.U., DSM-IV pain disorder in the general population. An exploration of the structure and threshold of medically unexplained pain symptoms. Eur. Arch. Psychiatr. Clin. Neurosci. 256:3 (2006), 187–196, 10.1007/s00406-005-0625-3.
Garfinkel, S.N., Seth, A.K., Barrett, A.B., Suzuki, K., Critchley, H.D., Knowing your own heart: distinguishing interoceptive accuracy from interoceptive awareness. Biol. Psychol. 104 (2015), 65–74, 10.1016/j.biopsycho.2014.11.004.
Gratton, G., Coles, M.G., Donchin, E., A new method for off-line removal of ocular artifact. Electroencephalogr. Clin. Neurophysiol. 55:4 (1983), 468–484, 10.1016/0013-4694(83)90135-9.
Gray, M.A., Taggart, P., Sutton, P.M., Groves, D., Holdright, D.R., Bradbury, D., Brull, D., Critchley, H.D., A cortical potential reflecting cardiac function. Proc. Natl. Acad. Sci. U. S. A. 104:16 (2007), 6818–6823, 10.1073/pnas.0609509104.
Harris, A.M., Orav, E.J., Bates, D.W., Barsky, A.J., Somatization increases disability independent of comorbidity. J. Gen. Intern. Med. 24:2 (2009), 155–161, 10.1007/s11606-008-0845-0.
Janssens, K.A., Oldehinkel, A.J., Verhulst, F.C., Hunfeld, J.A., Ormel, J., Rosmalen, J.G., Symptom-specific associations between low cortisol responses and functional somatic symptoms: the TRAILS study. Psychoneuroendocrinology 37:3 (2012), 332–340, 10.1016/j.psyneuen.2011.06.016.
Knapp-Kline, K., Kline, J.P., Heart rate, heart rate variability, and heartbeat detection with the method of constant stimuli: slow and steady wins the race. Biol. Psychol. 69:3 (2005), 387–396.
Lieb, R., Pfister, H., Mastaler, M., Wittchen, H.U., Somatoform syndromes and disorders in a representative population sample of adolescents and young adults: prevalence, comorbidity and impairments. Acta Psychiatr. Scand. 101:3 (2000), 194–208.
Lind, A.B., Delmar, C., Nielsen, K., Struggling in an emotional avoidance culture: a qualitative study of stress as a predisposing factor for somatoform disorders. J. Psychosom. Res. 76:2 (2014), 94–98, 10.1016/j.jpsychores.2013.11.019.
Lowe, B., Levenson, J., Depping, M., Husing, P., Kohlmann, S., Lehmann, M., Shedden-Mora, M., Toussaint, A., Uhlenbusch, N., Weigel, A., Somatic symptom disorder: a scoping review on the empirical evidence of a new diagnosis. Psychol. Med., 2021, 1–17, 10.1017/S0033291721004177.
Meyer, C., Rumpf, H.J., Hapke, U., Dilling, H., John, U., [Lifetime prevalence of mental disorders in general adult population. Results of TACOS study]. Nervenarzt 71:7 (2000), 535–542, 10.1007/s001150050623.
Michal, M., Reuchlein, B., Adler, J., Reiner, I., Beutel, M.E., Vögele, C., Schächinger, H., Schulz, A., Striking discrepancy of anomalous body experiences with normal interoceptive accuracy in depersonalization-derealization disorder. PLoS One, 9(2), 2014, e89823, 10.1371/journal.pone.0089823.
Müller, L.E., Schulz, A., Andermann, M., Gabel, A., Gescher, D.M., Spohn, A., Herpertz, S.C., Bertsch, K., Cortical representation of afferent bodily signals in borderline personality disorder: neural correlates and relationship to emotional dysregulation. JAMA Psychiatr. 72:11 (2015), 1077–1086, 10.1001/jamapsychiatry.2015.1252.
Murphy, J., Millgate, E., Geary, H., Ichijo, E., Coll, M.P., Brewer, R., Catmur, C., Bird, G., Knowledge of resting heart rate mediates the relationship between intelligence and the heartbeat counting task. Biol. Psychol. 133 (2018), 1–3, 10.1016/j.biopsycho.2018.01.012.
Mussgay, L., Klinkenberg, N., Rüddel, H., Heart beat perception in patients with depressive, somatoform, and personality disorders. J. Psychophysiol. 13:1 (1999), 27–36.
Park, H.D., Blanke, O., Heartbeat-evoked cortical responses: underlying mechanisms, functional roles, and methodological considerations. Neuroimage 197 (2019), 502–511, 10.1016/j.neuroimage.2019.04.081.
Paulus, M.P., Stein, M.B., Interoception in anxiety and depression. Brain Struct. Funct. 214:5–6 (2010), 451–463, 10.1007/s00429-010-0258-9.
Petrak, F., Hardt, J., Kappis, B., Nickel, R., Tiber Egle, U., Determinants of health-related quality of life in patients with persistent somatoform pain disorder. Eur. J. Pain 7:5 (2003), 463–471, 10.1016/S1090-3801(03)00014-4.
Pollatos, O., Dietel, A., Herbert, B.M., Wankner, S., Wachsmuth, C., Henningsen, P., Sack, M., Blunted autonomic reactivity and increased pain tolerance in somatoform patients. Pain 152:9 (2011), 2157–2164, 10.1016/j.pain.2011.05.024.
Pollatos, O., Herbert, B.M., Wankner, S., Dietel, A., Wachsmuth, C., Henningsen, P., Sack, M., Autonomic imbalance is associated with reduced facial recognition in somatoform disorders. J. Psychosom. Res. 71:4 (2011), 232–239, 10.1016/j.jpsychores.2011.03.012.
Pollatos, O., Traut-Mattausch, E., Schandry, R., Differential effects of anxiety and depression on interoceptive accuracy. Depress. Anxiety 26:2 (2009), 167–173, 10.1002/da.20504.
Pruessner, J.C., Kirschbaum, C., Meinlschmid, G., Hellhammer, D.H., Two formulas for computation of the area under the curve represent measures of total hormone concentration versus time-dependent change. Psychoneuroendocrinology 28:7 (2003), 916–931, 10.1016/S0306-4530(02)00108-7.
Reid, S., Crayford, T., Patel, A., Wessely, S., Hotopf, M., Frequent attenders in secondary care: a 3-year follow-up study of patients with medically unexplained symptoms. Psychol. Med. 33:3 (2003), 519–524, 10.1017/s003329170200658x.
Rief, W., Barsky, A.J., Psychobiological perspectives on somatoform disorders. Psychoneuroendocrinology 30:10 (2005), 996–1002, 10.1016/j.psyneuen.2005.03.018.
Rief, W., Broadbent, E., Explaining medically unexplained symptoms-models and mechanisms. Clin. Psychol. Rev. 27:7 (2007), 821–841, 10.1016/j.cpr.2007.07.005.
Rief, W., Hennings, A., Riemer, S., Euteneuer, F., Psychobiological differences between depression and somatization. J. Psychosom. Res. 68:5 (2010), 495–502, 10.1016/j.jpsychores.2010.02.001.
Rief, W., Hiller, W., Screening für Somatoforme Störungen. 2008, Hogrefe, Göttingen.
Ring, C., Brener, J., Knapp, K., Mailloux, J., Effects of heartbeat feedback on beliefs about heart rate and heartbeat counting: a cautionary tale about interoceptive awareness. Biol. Psychol. 104 (2015), 193–198, 10.1016/j.biopsycho.2014.12.010.
Schaefer, M., Egloff, B., Gerlach, A.L., Witthoft, M., Improving heartbeat perception in patients with medically unexplained symptoms reduces symptom distress. Biol. Psychol. 101 (2014), 69–76, 10.1016/j.biopsycho.2014.05.012.
Schaefer, M., Egloff, B., Witthoft, M., Is interoceptive awareness really altered in somatoform disorders? Testing competing theories with two paradigms of heartbeat perception. J. Abnorm. Psychol. 121:3 (2012), 719–724, 10.1037/a0028509.
Schandry, R., Heart beat perception and emotional experience. Psychophysiology 18:4 (1981), 483–488, 10.1111/j.1469-8986.1981.tb02486.x.
Schandry, R., Montoya, P., Event-related brain potentials and the processing of cardiac activity. Biol. Psychol. 42:1–2 (1996), 75–85, 10.1016/0301-0511(95)05147-3.
Schandry, R., Sparrer, B., Weitkunat, R., From the heart to the brain: a study of heartbeat contingent scalp potentials. Int. J. Neurosci. 30:4 (1986), 261–275, 10.3109/00207458608985677.
Schandry, R., Specht, G., The influence of psychological and physical stress on the perception of heartbeats. [Abstract]. Psychophysiology, 18(2), 1981, 154, 10.1111/j.1469-8986.1981.tb02929.x.
Schenk, L., Fischbach, J.T.M., Müller, R., Vögele, C., Witthoft, M., Van Diest, I., Schulz, A., High blood pressure responders show largest increase in heartbeat perception accuracy after post-learning stress following a cardiac interoceptive learning task. Biol. Psychol., 154, 2020, 107919, 10.1016/j.biopsycho.2020.107919.
Schulz, A., Back, S.N., Schaan, V.K., Bertsch, K., Vögele, C., On the construct validity of interoceptive accuracy based on heartbeat counting: cardiovascular determinants of absolute and tilt-induced change scores. Biol. Psychol., 164, 2021, 108168, 10.1016/j.biopsycho.2021.108168.
Schulz, A., Deuter, C.E., Breden, I.H., Vogele, C., Wingenfeld, K., Otte, C., Kuehl, L.K., Noradrenergic activation induced by yohimbine decreases interoceptive accuracy in healthy individuals with childhood adversity. Dev. Psychopathol., 2021, 1–12, 10.1017/S0954579420001613.
Schulz, A., Ferreira de Sá, D.S., Dierolf, A.M., Lutz, A., van Dyck, Z., Vögele, C., Schächinger, H., Short-term food deprivation increases amplitudes of heartbeat-evoked potentials. Psychophysiology 52:5 (2015), 695–703, 10.1111/psyp.12388.
Schulz, A., Köster, S., Beutel, M.E., Schächinger, H., Vögele, C., Rost, S., Rauh, M., Michal, M., Altered patterns of heartbeat-evoked potentials in depersonalization/derealization disorder: neurophysiological evidence for impaired cortical representation of bodily signals. Psychosom. Med. 77:5 (2015), 506–516, 10.1097/PSY.0000000000000195.
Schulz, A., Lass-Hennemann, J., Sütterlin, S., Schächinger, H., Vögele, C., Cold pressor stress induces opposite effects on cardioceptive accuracy dependent on assessment paradigm. Biol. Psychol. 93:1 (2013), 167–174, 10.1016/j.biopsycho.2013.01.007.
Schulz, A., Plein, D.E., Richter, S., Blumenthal, T.D., Schächinger, H., Cold pressor stress affects cardiac attenuation of startle. Int. J. Psychophysiol. 79:3 (2011), 385–391, 10.1016/j.ijpsycho.2010.12.008.
Schulz, A., Rost, S., Flasinski, T., Dierolf, A.M., Lutz, A.P.C., Münch, E.E., Mertens, V.C., Witthöft, M., Vögele, C., Higher responsiveness of heartbeat-evoked potentials to attention focused on heartbeats in high than in low symptom reporters: a neurophysiological explanation for medically-unexplained symptoms. J. Psychosom. Res., 137, 2020, 110223, 10.1016/j.jpsychores.2020.110223.
Schulz, A., Schultchen, D., Vögele, C., Interoception, stress, and physical symptoms in stress-associated diseases. European Journal of Health Psychology 27 (2020), 132–153.
Schulz, A., Stammet, P., Dierolf, A.M., Vögele, C., Beyenburg, S., Werer, C., Devaux, Y., Late heartbeat-evoked potentials are associated with survival after cardiac arrest. Resuscitation 126 (2018), 7–13, 10.1016/j.resuscitation.2018.02.009.
Schulz, A., Strelzyk, F., Ferreira de Sa, D.S., Naumann, E., Vögele, C., Schächinger, H., Cortisol rapidly affects amplitudes of heartbeat-evoked brain potentials-Implications for the contribution of stress to an altered perception of physical sensations?. Psychoneuroendocrinology 38:11 (2013), 2686–2693, 10.1016/j.psyneuen.2013.06.027.
Schulz, A., Vögele, C., Interoception and stress. Front. Psychol., 6, 2015, 993, 10.3389/fpsyg.2015.00993.
Schulz, P., Schlotz, W., Becker, P., TICS. Trierer Inventar zu chronischem Stress. 2004, Hogrefe, Göttingen.
Schwabe, L., Haddad, L., Schächinger, H., HPA axis activation by a socially evaluated cold-pressor test. Psychoneuroendocrinology 33:6 (2008), 890–895, 10.1016/j.psyneuen.2008.03.001.
Shao, S., Shen, K., Wilder-Smith, E.P., Li, X., Effect of pain perception on the heartbeat evoked potential. Clin. Neurophysiol. 122:9 (2011), 1838–1845, 10.1016/j.clinph.2011.02.014.
Spielberger, C.D., Gorsuch, R.L., Lushene, R.E., Manual for the State-Trait Anxiety Inventory. 1970, Consulting Psychologists Press, Palo Alto (CA).
Terhaar, J., Viola, F.C., Bar, K.J., Debener, S., Heartbeat evoked potentials mirror altered body perception in depressed patients. Clin. Neurophysiol. 123:10 (2012), 1950–1957, 10.1016/j.clinph.2012.02.086.
Weiss, S., Sack, M., Henningsen, P., Pollatos, O., On the interaction of self-regulation, interoception and pain perception. Psychopathology 47:6 (2014), 377–382, 10.1159/000365107.
Wittchen, H.U., Zaudig, M., Fydrich, T., SKID: Strukturiertes Klinisches Interview für DSM-IV; Achse I und II. Achse II : Persönlichkeitsstörungen. SKID-II. Hogrefe, 1997 Göttingen.
Wittkamp, M.F., Bertsch, K., Vögele, C., Schulz, A., A latent state-trait analysis of interoceptive accuracy. Psychophysiology, 55(6), 2018, e13055, 10.1111/psyp.13055.
Ying-Chih, C., Yu-Chen, H., Wei-Lieh, H., Heart rate variability in patients with somatic symptom disorders and functional somatic syndromes: a systematic review and meta-analysis. Neurosci. Biobehav. Rev. 112 (2020), 336–344, 10.1016/j.neubiorev.2020.02.007.
Zamariola, G., Maurage, P., Luminet, O., Corneille, O., Interoceptive accuracy scores from the heartbeat counting task are problematic: evidence from simple bivariate correlations. Biol. Psychol., 2018, 10.1016/j.biopsycho.2018.06.006.
Zimprich, D., Nusser, L., Pollatos, O., Are interoceptive accuracy scores from the heartbeat counting task problematic? A comment on Zamariola et al. 2018 Biol. Psychol., 152, 2020, 107868, 10.1016/j.biopsycho.2020.107868.