Trait and state interoceptive abnormalities are associated with dissociation and seizure frequency in patients with functional seizures

Akihiro Koreki, Sarah N Garfkinel, Marco Mula, Niruj Agrawal, Sarah Cope, Talia Eilon, Cassandra Gould Van Praag, Hugo D Critchley, Mark Edwards, Mahinda Yogarajah, Akihiro Koreki, Sarah N Garfkinel, Marco Mula, Niruj Agrawal, Sarah Cope, Talia Eilon, Cassandra Gould Van Praag, Hugo D Critchley, Mark Edwards, Mahinda Yogarajah

Abstract

Objective: Dissociative traits represent a disturbance in selfhood that may predispose to, and trigger, functional seizures (FSs). The predictive representation and control of the internal physiological state of the body (interoception) are proposed to underpin the integrity of the sense of self ("minimal selfhood"). Therefore, discrepancies between objective and subjective aspects of interoception may relate to symptom expression in patients with FSs. Here, we tested whether individual differences in trait measures of interoception relate to dissociative symptoms, and whether state interoceptive deficits predict FS occurrence.

Methods: Forty-one participants with FSs and 30 controls completed questionnaire ratings of dissociation, and measures of (1) interoceptive accuracy (IA)-objective performance on heartbeat detection tasks; (2) trait interoceptive sensibility-subjective sensitivity to internal sensations (using the Porges Body Perception Questionnaire); and (3) state interoceptive sensibility-subjective trial-by-trial measures of confidence in heartbeat detection. Interoceptive trait prediction error (ITPE) was calculated from the discrepancy between IA and trait sensibility, and interoceptive state prediction error (ISPE) from the discrepancy between IA and state sensibility.

Results: Patients with FSs had significantly lower IA and greater trait interoceptive sensibility than healthy controls. ITPE was the strongest predictor of dissociation after controlling for trait anxiety and depression in a regression model. ISPE correlated significantly with FS frequency after controlling for state anxiety.

Significance: Patients with FSs have disturbances in interoceptive processing that predict both dissociative traits reflecting the disrupted integrity of self-representation, and the expression of FSs. These findings provide insight into the pathophysiology of functional neurological disorder, and could lead to novel diagnostic and therapeutic approaches.

Keywords: dissociation; dissociative seizures; functional seizures; interoception; nonepileptic attack disorder; psychogenic nonepileptic seizures.

Conflict of interest statement

None of the authors has any conflict of interest to disclose. We confirm that we have read the Journal's position on issues involved in ethical publication and affirm that this report is consistent with those guidelines.

© 2020 The Authors. Epilepsia published by Wiley Periodicals LLC on behalf of International League Against Epilepsy.

Figures

FIGURE 1
FIGURE 1
Interoceptive trait prediction error (ITPE) derived from the heartbeat tacking task (HTT) and heartbeat discrimination task (HDT) plotted against Somatoform Dissociation Questionnaire (SDQ‐20) and depersonalization subscore of the Multiscale Dissociation Inventory (MDI‐DP) scores
FIGURE 2
FIGURE 2
Seizure frequency rank plotted against 1/interoceptive state prediction error (ISPE) rank. Note that the bigger the value for seizure frequency rank, the smaller seizure frequency in the patient population. The bigger the 1/ISPE rank, the bigger the ISPE value. 1/ISPE is equivalent to heartbeat discrimination task (HDT) awareness

References

    1. LaFrance WC, Baker GA, Duncan R, Goldstein LH, Reuber M. Minimum requirements for the diagnosis of psychogenic nonepileptic seizures: a staged approach: a report from the International League Against Epilepsy Nonepileptic Seizures Task Force. Epilepsia. 2013;54:2005–18.
    1. Asadi‐Pooya AA, Sperling MR. Epidemiology of psychogenic nonepileptic seizures. Epilepsy Behav. 2015;46:60–5.
    1. LaFrance WC, Benbadis SR. Avoiding the costs of unrecognized psychological nonepileptic seizures. Neurology. 2006;66:1620–1.
    1. Angus‐Leppan H. Diagnosing epilepsy in neurology clinics: a prospective study. Seizure. 2008;17:431–6.
    1. Jennum P, Ibsen R, Kjellberg J. Morbidity and mortality of nonepileptic seizures (NES): a controlled national study. Epilepsy Behav. 2019;96:229–33.
    1. Kerr MP, Mensah S, Besag F, et al. International consensus clinical practice statements for the treatment of neuropsychiatric conditions associated with epilepsy. Epilepsia. 2011;52:2133–8.
    1. Bowman ES. Why conversion seizures should be classified as a dissociative disorder. Psychiatr Clin North Am. 2006;29:185–211.
    1. Nijenhuis ERS. Somatoform dissociation: major symptoms of dissociative disorders. J Trauma Dissoc. 2001;1:7–32.
    1. Brown RJ. Dissociation and functional neurologic disorders. Handb Clin Neurol. 2016;139:85–94.
    1. Nijenhuis ER, Spinhoven P, Van dyck R, Der hart OV, Vanderlinden J. The development and psychometric characteristics of the Somatoform Dissociation Questionnaire (SDQ‐20). J Nerv Ment Dis. 1996;184:688–94.
    1. Goldstein LH, Mellers JDC. Ictal symptoms of anxiety, avoidance behaviour, and dissociation in patients with dissociative seizures. J Neurol Neurosurg Psychiatr. 2006;77:616–21.
    1. Briere J. Multiscale Dissociation Inventory: Professional Manual. Odessa, FL: Psychological Assessment Resources; 2002.
    1. Picard F, Friston K. Predictions, perception, and a sense of self. Neurology. 2014;83:1112–8.
    1. Seth AK, Tsakiris M. Being a beast machine: the somatic basis of selfhood. Trends Cogn Sci. 2018;22:969–81.
    1. Seth AK, Suzuki K, Critchley HD. An interoceptive predictive coding model of conscious presence. Front Psychol. 2011;2:395.
    1. Schäflein E, Sattel HC, Pollatos O, Sack M. Disconnected—impaired interoceptive accuracy and its association with self‐perception and cardiac vagal tone in patients with dissociative disorder. Front Psychol. 2018;9:897.
    1. Garfinkel SN, Tiley C, O'Keeffe S, Harrison NA, Seth AK, Critchley HD. Discrepancies between dimensions of interoception in autism: implications for emotion and anxiety. Biol Psychol. 2016;114:117–26.
    1. Ainley V, Apps MAJ, Fotopoulou A, Tsakiris M. 'Bodily precision': a predictive coding account of individual differences in interoceptive accuracy. Philos Trans R Soc B Biol Sci. 2016;371(1708):20160003.
    1. Heart SR, Perception B, Experience E. Heart beat perception and emotional experience. Psychophysiology. 1981;18:483–8.
    1. Whitehead WE, Drescher VM, Heiman P, Blackwell B. Relation of heart rate control to heartbeat perception. Biofeedback Self Regul. 1977;2:371–92.
    1. Porges S. Body Perception Questionnaire. Baltimore, MD: Laboratory of Developmental Assessment, University of Maryland; 1993.
    1. Spielberger C, Gorsuch R, Lushene R. Manual for the State‐Trait Anxiety Inventory. Palo Alto, CA: Consulting Psychologists Press; 1983.
    1. Beck A, Steer R, Brown G. Manual for the Beck Depression Inventory‐II. San Antonio, TX: Psychological Corporation; 1996.
    1. Garfinkel SN, Seth AK, Barrett AB, Suzuki K, Critchley HD. Knowing your own heart: distinguishing interoceptive accuracy from interoceptive awareness. Biol Psychol. 2015;104:65–74.
    1. Glickman ME, Rao SR, Schultz MR. False discovery rate control is a recommended alternative to Bonferroni‐type adjustments in health studies. J Clin Epidemiol. 2014;67:850–7.
    1. Pick S, Mellers JDC, Goldstein LH. Dissociation in patients with dissociative seizures: relationships with trauma and seizure symptoms. Psychol Med. 2017;47:1215–29.
    1. Demartini B, Goeta D, Barbieri V, et al. Psychogenic non‐epileptic seizures and functional motor symptoms: a common phenomenology? J Neurol Sci. 2016;368:49–54.
    1. Ricciardi L, Demartini B, Crucianelli L, Krahé C, Edwards MJ, Fotopoulou A. Interoceptive awareness in patients with functional neurological symptoms. Biol Psychol. 2016;113:68–74.
    1. Parees I, Saifee TA, Kassavetis P, Kojovic M, Rubio‐Agusti I, Rothwell JC. Believing is perceiving: mismatch between self‐report and actigraphy in psychogenic tremor. Brain. 2012;135(Pt 1):117–23.
    1. Ricciardi L, Demartini B, Morgante F, Parees I, Nielsen G, Edwards MJ. Symptom severity in patients with functional motor symptoms: patient’s perception and doctor’s clinical assessment. Parkinsonism Relat Disord. 2015;21:529–32.
    1. Apazoglou K, Mazzola V, Wegrzyk J, Frasca Polara G, Aybek S. Biological and perceived stress in motor functional neurological disorders. Psychoneuroendocrinology. 2017;85:142–50.
    1. Seth AK, Friston KJ. Active interoceptive inference and the emotional brain. Philos Trans R Soc B Biol Sci. 2016;371(1708):20160007.
    1. Tsakiris M, Jiménez AT, Just CM. A heartbeat away from one’s body: interoceptive sensitivity predicts malleability of body‐representations. Proc R Soc B Biol Sci. 2011;278:2470–6.
    1. Medford N. Dissociative symptoms and epilepsy. Epilepsy Behav. 2014;30:10–3.
    1. Schulz A, Köster S, Beutel ME, et al. Altered patterns of heartbeat‐evoked potentials in depersonalization/derealization disorder: neurophysiological evidence for impaired cortical representation of bodily signals. Psychosom Med. 2015;77:506–16.
    1. Schaefer M, Egloff B, Witthöft M. Is interoceptive awareness really altered in somatoform disorders? Testing competing theories with two paradigms of heartbeat perception. J Abnorm Psychol. 2012;121:719–24.
    1. Seth AK. Interoceptive inference, emotion, and the embodied self. Trends Cogn Sci. 2013;17:565–73.
    1. Barrett LF. The theory of constructed emotion: an active inference account of interoception and categorization. Soc Cogn Affect Neurosci. 2017;12(1):1–23.
    1. Quadt L, Critchley HD, Garfinkel SN. The neurobiology of interoception in health and disease: neuroscience of interoception. Ann N Y Acad Sci. 2018;1428(1):112–28.
    1. Paulus MP, Feinstein JS, Khalsa SS. An active inference approach to interoceptive psychopathology. Annu Rev Clin Psychol. 2019;15:97–122.
    1. Van den Bergh O, Witthöft M, Petersen S, Brown RJ. Symptoms and the body: taking the inferential leap. Neurosci Biobehav Rev. 2017;74(Pt A):185–203.
    1. Hendrickson R, Popescu A, Dixit R, Ghearing G, Bagic A. Panic attack symptoms differentiate patients with epilepsy from those with psychogenic nonepileptic spells (PNES). Epilepsy Behav. 2014;37:210–4.
    1. Kleckner IR, Wormwood JB, Simmons WK, Barrett LF, Quigley KS. Methodological recommendations for a heartbeat detection‐based measure of interoceptive sensitivity: recommended methods for heartbeat detection. Psychophysiology. 2015;52:1432–40.
    1. Mussgay L, Klinkenberg N, Rüddel H. Heart beat perception in patients with depressive, somatoform, and personality disorders. J Psychophysiol. 1999;13:27–36.
    1. Terhaar J, Viola FC, Bär K‐J, Debener S. Heartbeat evoked potentials mirror altered body perception in depressed patients. Clin Neurophysiol. 2012;123:1950–7.
    1. Ring C, Brener J. Influence of beliefs about heart rate and actual heart rate on heartbeat counting. Psychophysiology. 1996;33:541–6.
    1. 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. 2015;104:193–8.
    1. Lanius RA, Vermetten E, Loewenstein RJ, Brand B, Schmahl C, Bremner JD. Emotion modulation in PTSD: clinical and neurobiological evidence for a dissociative subtype. Am J Psychiatry. 2010;167:640–7.

Source: PubMed

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