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Impaired emotional and behavioural awareness and control in patients with dissociative seizures

Published online by Cambridge University Press:  18 October 2019

Johannes Jungilligens*
Affiliation:
Department of Neurology, University Hospital Knappschaftskrankenhaus Bochum, Ruhr University Bochum, Bochum, Germany Department of Neuropsychology, Faculty of Psychology, Institute of Cognitive Neuroscience, Ruhr University Bochum, Bochum, Germany
Jörg Wellmer
Affiliation:
Ruhr-Epileptology, Department of Neurology, University Hospital Knappschaftskrankenhaus Bochum, Ruhr University Bochum, Bochum, Germany
Uwe Schlegel
Affiliation:
Department of Neurology, University Hospital Knappschaftskrankenhaus Bochum, Ruhr University Bochum, Bochum, Germany
Henrik Kessler
Affiliation:
Department of Psychosomatic Medicine and Psychotherapy, LWL-University Hospital, Ruhr University Bochum, Bochum, Germany
Nikolai Axmacher
Affiliation:
Department of Neuropsychology, Faculty of Psychology, Institute of Cognitive Neuroscience, Ruhr University Bochum, Bochum, Germany
Stoyan Popkirov
Affiliation:
Department of Neurology, University Hospital Knappschaftskrankenhaus Bochum, Ruhr University Bochum, Bochum, Germany
*
Author for correspondence: Johannes Jungilligens, E-mail: johannes.jungilligens@rub.de

Abstract

Background

Dissociative seizures (DS) are brief episodes of disrupted awareness and behavioural control that may resemble epileptic seizures. They are thought to arise in the context of impaired emotion processing and disinhibition. In a multi-perspective neuropsychological study, we aim to assess specific metacognitive traits and behavioural features involved in the affective and cognitive underpinnings of DS (emotion recognition and regulation, inhibition, interoception and sense of agency).

Methods

Twenty prospectively recruited patients with video-EEG-confirmed DS and 20 healthy controls underwent comprehensive neuropsychological and psychiatric testing using validated questionnaires and structured interviews. Behavioural experimental data was obtained using a custom-made emotional go/no-go task, a digital Libet clock setup and a heartbeat counting paradigm.

Results

Emotion recognition, as quantified in the emotional go/no-go task, was impaired in the DS group, and correlated with alexithymic traits. Behavioural inhibition, especially under conditions that would require emotion regulation, was also reduced in the emotional go/no-go task compared to controls and was correlated with neuropsychometric measures of emotion regulation. Data from the Libet clock experiment suggested impaired behavioural awareness in DS patients. No evidence of impaired interoceptive awareness was found in the heartbeat counting task.

Conclusion

These results represent comprehensive experimental evidence for alterations in emotional and behavioural awareness and control in patients with DS that yield empirical evidence for current psychopathological models. Our findings offer a more detailed understanding of key pathogenic factors in DS and provide theoretical support for recently developed cognitive-behavioural therapies for DS.

Type
Original Articles
Copyright
Copyright © Cambridge University Press 2019

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References

Abler, B and Kessler, H (2009) Emotion Regulation Questionnaire – Eine deutschsprachige Fassung des ERQ von Gross und John. Diagnostica 55, 144152.CrossRefGoogle Scholar
Baek, K, Doñamayor, N, Morris, LS, Strelchuk, D, Mitchell, S, Mikheenko, Y, Yeoh, SY, Phillips, W, Zandi, M, Jenaway, A, Walsh, C and Voon, V (2017) Impaired awareness of motor intention in functional neurological disorder: implications for voluntary and functional movement. Psychological Medicine 47, 16241636.CrossRefGoogle ScholarPubMed
Bakvis, P, Roelofs, K, Kuyk, J, Edelbroek, PM, Swinkels, WAM and Spinhoven, P (2009) Trauma, stress, and preconscious threat processing in patients with psychogenic nonepileptic seizures. Epilepsia 50, 10011011.CrossRefGoogle ScholarPubMed
Beck, AT, Ward, CH, Mendelson, M, Mock, J and Erbaugh, J (1961) An inventory for measuring depression. Archives of General Psychiatry 4, 561571.CrossRefGoogle ScholarPubMed
Bernstein, DP, Stein, JA, Newcomb, MD, Walker, E, Pogge, D, Ahluvalia, T, Stokes, J, Handelsman, L, Medrano, M, Desmond, D and Zule, W (2003) Development and validation of a brief screening version of the Childhood Trauma Questionnaire. Child Abuse & Neglect 27, 169190.CrossRefGoogle ScholarPubMed
Bernstein Carlson, E and Putnam, FW (1993) An update on the dissociative experiences scale. Dissociation 6, 1627.Google Scholar
Brown, RJ and Reuber, M (2016 a) Psychological and psychiatric aspects of psychogenic non-epileptic seizures (PNES): a systematic review. Clinical Psychology Review 45, 157182.CrossRefGoogle ScholarPubMed
Brown, RJ and Reuber, M (2016 b) Towards an integrative theory of psychogenic non-epileptic seizures (PNES). Clinical Psychology Review 47, 5570.CrossRefGoogle Scholar
Edwards, MJ, Moretto, G, Schwingenschuh, P, Katschnig, P, Bhatia, KP and Haggard, P (2011) Abnormal sense of intention preceding voluntary movement in patients with psychogenic tremor. Neuropsychologia 49, 27912793.CrossRefGoogle ScholarPubMed
Ferentzi, E, Bogdány, T, Szabolcs, Z, Csala, B, Horváth, Á and Köteles, F (2018) Multichannel investigation of interoception: sensitivity is not a generalizable feature. Frontiers in Human Neuroscience 12, 19.CrossRefGoogle Scholar
Fiess, J, Rockstroh, B, Schmidt, R and Steffen, A (2015) Emotion regulation and functional neurological symptoms: does emotion processing convert into sensorimotor activity? Journal of Psychosomatic Research 79, 477483.CrossRefGoogle ScholarPubMed
Garaizar, P, Cubillas, CP and Matute, H (2016) A HTML5 open source tool to conduct studies based on Libet's clock paradigm. Scientific Reports 6, 32689.CrossRefGoogle ScholarPubMed
Goldstein, LH (2006) Ictal symptoms of anxiety, avoidance behaviour, and dissociation in patients with dissociative seizures. Journal of Neurology, Neurosurgery & Psychiatry 77, 616621.CrossRefGoogle ScholarPubMed
Gross, JJ and John, OP (2003) Individual differences in two emotion regulation processes: implications for affect, relationships, and well-being. Journal of Personality and Social Psychology 85, 348362.CrossRefGoogle ScholarPubMed
Gul, A and Ahmad, H (2014) Cognitive deficits and emotion regulation strategies in patients with psychogenic nonepileptic seizures: a task-switching study. Epilepsy & Behavior 32, 108113.CrossRefGoogle ScholarPubMed
Hammond-Tooke, GD, Grajeda, FT, Macrorie, H and Franz, EA (2018) Response inhibition in patients with functional neurological symptom disorder. Journal of Clinical Neuroscience 56, 3843.CrossRefGoogle ScholarPubMed
Hendricks, ML and Testa, RJ (2012) A conceptual framework for clinical work with transgender and gender nonconforming clients: an adaptation of the minority stress model. Professional Psychology: Research and Practice 43, 460467.CrossRefGoogle Scholar
IBM SPSS Statistics for Windows. (2012) Armonk, NY: IBM Corp.Google Scholar
Keynejad, RC, Frodl, T, Kanaan, R, Pariante, C, Reuber, M and Nicholson, TR (2018) Stress and functional neurological disorders: mechanistic insights. Journal of Neurology, Neurosurgery & Psychiatry 90, 813821CrossRefGoogle ScholarPubMed
Kozlowska, K, Brown, KJ, Palmer, DM and Williams, LM (2013) Specific biases for identifying facial expression of emotion in children and adolescents with conversion disorders. Psychosomatic Medicine 75, 272280.CrossRefGoogle ScholarPubMed
Kranick, SM, Moore, JW, Yusuf, N, Martinez, VT, LaFaver, K, Edwards, MJ, Mehta, AR, Collins, P, Harrison, NA, Haggard, P, Hallett, M and Voon, V (2013) Action-effect binding is decreased in motor conversion disorder: implications for sense of agency. Movement Disorders 28, 11101116.CrossRefGoogle ScholarPubMed
Lane, RD, Quinlan, DM, Schwartz, GE, Walker, PA and Zeitlin, SB (1990) The Levels of Emotional Awareness Scale: a cognitive-developmental measure of emotion. Journal of Personality Assessment 55, 124134.CrossRefGoogle ScholarPubMed
Libet, B, Gleason, CA, Wright, EW and Pearl, DK (1983) Time of conscious intention to act in relation to onset of cerebral activity (readiness-potential). The unconscious initiation of a freely voluntary act. Brain 106, 623642.CrossRefGoogle ScholarPubMed
Lowry, R (2001). VassarStats Two Correlation Coefficients. Available at http://vassarstats.net/rdiff.html (Accessed 7 February 2019).Google Scholar
Lundqvist, D, Flykt, A and Öhman, A (1998). The Karolinska Directed Emotional Faces — KDEF, CD ROM. Department of Clinical Neuroscience, Psychology Section. Stockholm: Karolinska Institutet.Google Scholar
Margraf, J (1994). Mini-DIPS. Berlin, Heidelberg: Springer.CrossRefGoogle Scholar
Margraf, J and Ehlers, A (2007). Beck Angst-Inventar (BAI) – Manual. Deutsche Bearbeitung. Frankfurt: Harcourt Test Services.Google Scholar
Mathôt, S, Schreij, D and Theeuwes, J (2012) Opensesame: an open-source, graphical experiment builder for the social sciences. Behavior Research Methods 44, 314324.CrossRefGoogle ScholarPubMed
Melara, RD, Ruglass, LM, Fertuck, EA and Hien, DA (2018) Regulation of threat in post-traumatic stress disorder: associations between inhibitory control and dissociative symptoms. Biological Psychology 133, 8998.CrossRefGoogle ScholarPubMed
Nijenhuis, ER, Spinhoven, P, Van Dyck, R, Van der Hart, O and Vanderlinden, J (1996) The development and psychometric characteristics of the Somatoform Dissociation Questionnaire (SDQ-20). The Journal of Nervous and Mental Disease 184, 688694.CrossRefGoogle Scholar
Pick, S, Mellers, JDC and Goldstein, LH (2016) Explicit facial emotion processing in patients with dissociative seizures. Psychosomatic Medicine 78, 874885.CrossRefGoogle ScholarPubMed
Pick, S, Mellers, JDC and Goldstein, LH (2017) Dissociation in patients with dissociative seizures: relationships with trauma and seizure symptoms. Psychological Medicine 47, 12151229.CrossRefGoogle ScholarPubMed
Pick, S, Goldstein, LH, Perez, DL and Nicholson, TR (2019). Emotional processing in functional neurological disorder: a review, biopsychosocial model and research agenda. Journal of Neurology, Neurosurgery & Psychiatry, 90, 704711.CrossRefGoogle ScholarPubMed
Pick, S, Mellers, JDC and Goldstein, LH (2018 b) Implicit attentional bias for facial emotion in dissociative seizures: additional evidence. Epilepsy & Behavior 80, 296302.CrossRefGoogle ScholarPubMed
Popkirov, S, Grönheit, W, Schlegel, U and Wellmer, J (2014) Recurrent loss of consciousness despite DDD pacing: psychogenic pseudosyncope in a 19-year-old man. Clinical Research in Cardiology 103, 755757.CrossRefGoogle ScholarPubMed
Popkirov, S, Grönheit, W and Wellmer, J (2015) A systematic review of suggestive seizure induction for the diagnosis of psychogenic nonepileptic seizures. Seizure 31, 124132.CrossRefGoogle Scholar
Popkirov, S, Jungilligens, J, Grönheit, W and Wellmer, J (2017) Diagnosing psychogenic nonepileptic seizures: video-EEG monitoring, suggestive seizure induction and diagnostic certainty. Epilepsy & Behavior 73, 5458.CrossRefGoogle ScholarPubMed
Popkirov, S, Carson, AJ and Stone, J (2018) Scared or scarred: could ‘dissociogenic’ lesions predispose to nonepileptic seizures after head trauma? Seizure 58, 127132.CrossRefGoogle ScholarPubMed
Popkirov, S, Flasbeck, V, Schlegel, U, Juckel, G and Brüne, M (2019) Childhood trauma and dissociative symptoms predict frontal EEG asymmetry in borderline personality disorder. Journal of Trauma & Dissociation 20, 3247.CrossRefGoogle ScholarPubMed
Ricciardi, L, Demartini, B, Crucianelli, L, Krahé, C, Edwards, MJ and Fotopoulou, A (2016) Interoceptive awareness in patients with functional neurological symptoms. Biological Psychology 113, 6874.CrossRefGoogle ScholarPubMed
Schandry, R (1981) Heart beat perception and emotional experience. Psychophysiology 18, 483488.CrossRefGoogle ScholarPubMed
Steptoe, A and Noll, A (1997) The perception of bodily sensations, with special reference to hypochondriasis. Behaviour Research and Therapy 35, 901910.CrossRefGoogle ScholarPubMed
Stone, J and Carson, AJ (2013) The unbearable lightheadedness of seizing: wilful submission to dissociative (non-epileptic) seizures. Journal of Neurology, Neurosurgery & Psychiatry 84, 822824.CrossRefGoogle ScholarPubMed
Subic-Wrana, C, Beutel, ME, Brähler, E, Stöbel-Richter, Y, Knebel, A, Lane, RD and Wiltink, J (2014) How is emotional awareness related to emotion regulation strategies and self-reported negative affect in the general population? PLoS ONE 9, e91846.CrossRefGoogle Scholar
Szaflarski, JP, Allendorfer, JB, Nenert, R, LaFrance, WC, Barkan, HI, DeWolfe, J, Pati, S, Thomas, AE and Ver Hoef, L (2018) Facial emotion processing in patients with seizure disorders. Epilepsy & Behavior 79, 193204.CrossRefGoogle ScholarPubMed
Taylor, GJ, Michael Bagby, R and Parker, JDA (1991) The alexithymia construct: a potential paradigm for psychosomatic medicine. Psychosomatics 32, 153164.CrossRefGoogle ScholarPubMed
Tottenham, N, Hare, TA and Casey, BJ (2011) Behavioral assessment of emotion discrimination, emotion regulation, and cognitive control in childhood, adolescence, and adulthood. Frontiers in Psychology 2, 19.CrossRefGoogle Scholar
Van den Bergh, O, Witthöft, M, Petersen, S and Brown, RJ (2017) Symptoms and the body: taking the inferential leap. Neuroscience & Biobehavioral Reviews 74, 185203.CrossRefGoogle ScholarPubMed
Voon, V, Ekanayake, V, Wiggs, E, Kranick, S, Ameli, R, Harrison, NA and Hallett, M (2013) Response inhibition in motor conversion disorder. Movement Disorders 28, 612618.CrossRefGoogle ScholarPubMed
Williams, IA, Levita, L and Reuber, M (2018) Emotion dysregulation in patients with psychogenic nonepileptic seizures: a systematic review based on the extended process model. Epilepsy & Behavior 86, 3748.CrossRefGoogle ScholarPubMed
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