Reduced Responsiveness to Social Provocation in Autism Spectrum Disorder
Corresponding Author
Isabella Schneider
Department of Psychiatry, Psychotherapy and Psychosomatics, Medical School, RWTH Aachen University, Aachen, Germany
JARA Translational Brain Medicine, Forschungszentrum Jülich, Jülich, Germany
Address for correspondence and reprints: Isabella Schneider, Department of Psychiatry, Psychotherapy and Psychosomatics, Medical School, RWTH Aachen University, Pauwelsstr. 30, D-52074 Aachen, Germany. E-mail: [email protected]Search for more papers by this authorChristina Regenbogen
Department of Psychiatry, Psychotherapy and Psychosomatics, Medical School, RWTH Aachen University, Aachen, Germany
Department of Clinical Neuroscience, Karolinska Institutet, Stockholm, Sweden
Search for more papers by this authorNils Kohn
Department of Psychiatry, Psychotherapy and Psychosomatics, Medical School, RWTH Aachen University, Aachen, Germany
JARA Translational Brain Medicine, Forschungszentrum Jülich, Jülich, Germany
Search for more papers by this authorFlorian D. Zepf
JARA Translational Brain Medicine, Forschungszentrum Jülich, Jülich, Germany
Department of Child and Adolescent Psychiatry, Psychosomatics and Psychotherapy, Medical School, RWTH Aachen University, Aachen, Germany
Department of Child and Adolescent Psychiatry, School of Paediatrics and Child Health & School of Psychiatry and Clinical Neurosciences, Faculty of Medicine, Dentistry and Health Sciences, The University of Western Australia, Perth, Australia
Specialised Child and Adolescent Mental Health Services (CAMHS), Department of Health in Western Australia, Perth, WA, Australia
Search for more papers by this authorSarah Bubenzer-Busch
JARA Translational Brain Medicine, Forschungszentrum Jülich, Jülich, Germany
Department of Child and Adolescent Psychiatry, Psychosomatics and Psychotherapy, Medical School, RWTH Aachen University, Aachen, Germany
Search for more papers by this authorFrank Schneider
Department of Psychiatry, Psychotherapy and Psychosomatics, Medical School, RWTH Aachen University, Aachen, Germany
JARA Translational Brain Medicine, Forschungszentrum Jülich, Jülich, Germany
Department of Psychiatry, University of Pennsylvania, Philadelphia, Pennsylvania
Search for more papers by this authorRuben C. Gur
Department of Psychiatry, University of Pennsylvania, Philadelphia, Pennsylvania
Search for more papers by this authorUte Habel
Department of Psychiatry, Psychotherapy and Psychosomatics, Medical School, RWTH Aachen University, Aachen, Germany
JARA Translational Brain Medicine, Forschungszentrum Jülich, Jülich, Germany
Search for more papers by this authorCorresponding Author
Isabella Schneider
Department of Psychiatry, Psychotherapy and Psychosomatics, Medical School, RWTH Aachen University, Aachen, Germany
JARA Translational Brain Medicine, Forschungszentrum Jülich, Jülich, Germany
Address for correspondence and reprints: Isabella Schneider, Department of Psychiatry, Psychotherapy and Psychosomatics, Medical School, RWTH Aachen University, Pauwelsstr. 30, D-52074 Aachen, Germany. E-mail: [email protected]Search for more papers by this authorChristina Regenbogen
Department of Psychiatry, Psychotherapy and Psychosomatics, Medical School, RWTH Aachen University, Aachen, Germany
Department of Clinical Neuroscience, Karolinska Institutet, Stockholm, Sweden
Search for more papers by this authorNils Kohn
Department of Psychiatry, Psychotherapy and Psychosomatics, Medical School, RWTH Aachen University, Aachen, Germany
JARA Translational Brain Medicine, Forschungszentrum Jülich, Jülich, Germany
Search for more papers by this authorFlorian D. Zepf
JARA Translational Brain Medicine, Forschungszentrum Jülich, Jülich, Germany
Department of Child and Adolescent Psychiatry, Psychosomatics and Psychotherapy, Medical School, RWTH Aachen University, Aachen, Germany
Department of Child and Adolescent Psychiatry, School of Paediatrics and Child Health & School of Psychiatry and Clinical Neurosciences, Faculty of Medicine, Dentistry and Health Sciences, The University of Western Australia, Perth, Australia
Specialised Child and Adolescent Mental Health Services (CAMHS), Department of Health in Western Australia, Perth, WA, Australia
Search for more papers by this authorSarah Bubenzer-Busch
JARA Translational Brain Medicine, Forschungszentrum Jülich, Jülich, Germany
Department of Child and Adolescent Psychiatry, Psychosomatics and Psychotherapy, Medical School, RWTH Aachen University, Aachen, Germany
Search for more papers by this authorFrank Schneider
Department of Psychiatry, Psychotherapy and Psychosomatics, Medical School, RWTH Aachen University, Aachen, Germany
JARA Translational Brain Medicine, Forschungszentrum Jülich, Jülich, Germany
Department of Psychiatry, University of Pennsylvania, Philadelphia, Pennsylvania
Search for more papers by this authorRuben C. Gur
Department of Psychiatry, University of Pennsylvania, Philadelphia, Pennsylvania
Search for more papers by this authorUte Habel
Department of Psychiatry, Psychotherapy and Psychosomatics, Medical School, RWTH Aachen University, Aachen, Germany
JARA Translational Brain Medicine, Forschungszentrum Jülich, Jülich, Germany
Search for more papers by this authorAbstract
Deficits in emotion processing and social interaction are prominent symptoms of autism spectrum disorder (ASD). ASD has also been associated with aggressive tendencies towards self and others. The prevalence of aggressive behavior in this disorder, its etiology and its impact on social life are still unclear. This study investigated behavioral and physiological effects of social provocation in patients with ASD and healthy controls. We used a modified Taylor Aggression Paradigm in 24 high-functioning patients with ASD and 24 healthy controls. Participants were instructed to play against a fictitious human opponent. Money withdrawals toward the participant represented provocation and money deduction by the participant denoted aggressive behavior. Throughout the measurement, electrodermal activity (EDA) was recorded. Healthy controls showed higher aggressive responses to high provocation compared to low provocation, which demonstrated the effectiveness of the used procedure in eliciting aggression. Patients' responses were not influenced by the level of social provocation, although in both groups aggression was higher after lost compared to won trials. Physiologically, controls showed fewer but higher EDA amplitudes when responding aggressively, whereas patients displayed the opposite pattern of more but lower EDA amplitudes. The modified Taylor Aggression Paradigm successfully elicited aggression and revealed different behavioral and neurophysiological responses in patients and healthy controls. Patients' aggressive behavior as well as their physiological responses were less modulated by level of provocation compared to controls. Therapeutic attempts for patients might concentrate on improving empathic abilities and the understanding of social situations, including provocation and aggressive behavior. Autism Res 2015, 8: 297–306. © 2015 International Society for Autism Research, Wiley Periodicals, Inc.
References
- Adolphs, R., Sears, L., & Piven, J. (2001). Abnormal processing of social information from faces in autism. Journal of Cognitive Neuroscience, 13, 232–240.
- American Psychiatric Association. (2000). Diagnostic and statistical manual of mental disorders ( 4th ed., pp. 70−75), Text Revision. Washington, DC: American Psychiatric Association.
- Anckarsäter, H. (2006). Central nervous changes in social dysfunction: Autism, aggression, and psychopathology. Brain Research Bulletin, 69, 259–265.
- Anderson, C.A. & Bushman, B.J. (2002). Human aggression. Annual Review of Psychology, 53, 27–51.
- Anderson, C.A., Deuser, W.E., & DeNeve, K.M. (1995). Hot temperatures, hostile affect, hostile cognition, and arousal: Tests of a general model of affective aggression. Personality and Social Psychology Bulletin, 21, 434–448.
- Aschenbrenner, S., & Tucha, O. (2000). Regensburger word fluency test. Göttingen, Germany: Hogrefe.
- Baron-Cohen, S., Wheelwright, S., Skinner, R., Martin, J., & Clubley E. (2001). The autism-spectrum quotient (AQ): Evidence from asperger syndrome/high-functioning autism, males and females, scientists and mathematicians. Journal of Autism and Developmental Disorders, 31, 5–17.
- Barry-Walsh, J.B., & Mullen, P.E. (2004). Forensic aspects of asperger's syndrome. Journal of Forensic Psychiatry and Psychology, 15, 96–107.
- Beck, A.T., Steer, R.A., & Brown, G.K. ( 1996). Manual for the Beck depression inventory-II. San Antonio, TX: Psychological Corporation.
- Berkowitz, L. (1993). Aggression: It causes, consequences, and control, (p. 485). New York: McGraw Hill.
- Boucsein, W. (2012). Electrodermal activity ( 2nd ed.). New York: Springer.
- Bouhlel, S., Jones, Y., Khelifa, E., Msolly, M., Melki, W., & El-Hechmi, Z. (2012). Prodromal symptoms in schizophrenic relapse: A descriptive and comparative study. Encephale, 38, 397–403.
- Buss, A.H., & Perry, M. (1992). The aggression questionnaire. Journal of Personality and Social Psychology, 63, 452–459.
- Decety, J. (2011). Dissecting the neural mechanisms mediating empathy. Emotional Review, 3, 92–108.
- De Vignemont, F., & Singer, T. (2006). The empathic brain: How, when and why? Trend in Cognitive Science, 10, 435–441.
- Dougherty, D.M., Bjork, J.M., Huckabee, H.C.G., Moeller, F.G., & Swann, A.C. (1999). Laboratory measures of aggression and impulsivity in women with borderline personality disorder. Psychiatry Research, 85, 315–326.
- Falkenberg, I., Kohn, N., Schoepker, R., & Habel, U. (2012). Mood induction in depressive patients: A comparative multidimensional approach. PLoS ONE 7: e30016.
- Fowels, D.C., Christie, M.J., Edelberg, R., Grings, W.W., Lykken, D.T., & Venables, P.H. (1981). Publication recommendations for electrodermal measurements. Psychophysiology, 18, 232–239.
- Frith, U. (2001). Mind blindness and the brain in autism. Neuron, 32, 969–979.
- Giancola, P.R., & Chermack, S.T. (1998). Construct validity of laboratory aggression paradigms: A response to Tedeschi and Quigley (1996). Aggression and Violent Behavior, 3, 237–253.
-
Gunasekaran, S., &
Chaplin, E. (2012). Autism spectrum disorders and offending. Advances in Mental Health and Intellectual Disabilities, 6, 308–313.
10.1108/20441281211285955 Google Scholar
- Gur, R.C., Sara, R., Hagendoorn, M., Marom, O., Hughett, P., Macy, L., et al. (2002). A method for obtaining 3-dimensional facial expressions and its standardization for use in neurocognitive studies. Journal of Neuroscience Methods, 115, 137–143.
- Härting, C., Markowitsch, H.J., Neufeld, H., Calabrese, P., Deisinge, K., & Kessler, J. (2002). Wechsler Gedächtnis Test-Revidierte Fassung (WMS-R): Deutsche Adaptation der revidierten Fassung der Wechsler Memory Scale. Bern, Switzerland: Verlag Hans Huber.
- Hartley, S.L., Sikora, D.M., & McCoy, R. (2008). Prevalence and risk factors of maladaptive behaviour in young children with autistic disorder. Journal of Intellectual Disability Research, 52, 819–829.
- Haskins, B.G., & Silva, J.A. (2006). Asperger's disorder and criminal behavior: Forensic-psychiatric considerations. Journal of the American Academy of Psychiatry and the Law, 34, 374–384.
- Hubert, B.E., Wicker, B., Monfardini, E., & Deruelle, C. (2009). Electrodermal reactivity to emotion processing in adults with autistic spectrum disorders. Autism, 13, 9–19.
- Ickes, W. (2003). Everyday mind reading. New York: Prometheus Books.
- Krippl, M., & Karim, A.A. (2011). “Theory of Mind “and its neuronal correlates in forensically relevant disorders. Nervenarzt, 82, 843–852.
- Lai, M.L., Lombardo, M.V., & Baron-Cohen, S. (2014). Autism. The Lancet, 383, 896–910.
- Lehrl, S. (2005). Mehrfachwahl-Wortschatz-Intelligenztest MWT-B. Balingen, Germany: Spitta Verlag.
-
Leibetseder, M.,
Laieiter, A.R.,
Riepler, A., &
Köller, T. (2001). E-Skala: Fragebogen zur Erfassung von Empathie: Beschreibung und psychometrische Eigenschaften. Zeitschrift für Differentielle und Diagnostische Psychologie, 22, 70–85.
10.1024//0170-1789.22.1.70 Google Scholar
- Lorber, M.F. (2004). Psychophysiology of aggression, psychopathy, and conduct problems: A meta-analysis. Psychological Bulletin, 130, 531–552.
- Lord, C., Rutter, M., DiLavore, P.C., & Risi, S. (1999). Autism diagnostic observation schedule. Los Angeles, CA: Western Psychological Services.
-
Patton, J.H.,
Standford, M.S., &
Barratt, E.S. (1995).
Factor structure of the Barratt impulsiveness scale. Journal of Clinical Psychology, 51, 768–774.
10.1002/1097-4679(199511)51:6<768::AID-JCLP2270510607>3.0.CO;2-1 CAS PubMed Web of Science® Google Scholar
- Paulus, C. (2006). The Saarbrueck personality questionnaire on empathy: Psychometric evaluation of the German version of the Interpersonal Reactivity Index. Available at http://psydok.sulb.uni-saarland.de/volltexte/2009/2363/. Accessed on July 14, 2013.
- Reitan, R.M. (1992). Trail making test: Manual for administration and scoring. South Tucson, AZ: Reitan Neuropsychology Laboratory.
- Shattuck, P.T., Seltzer, M.M., Greenberg, J.S., Orsmond, G.I., Bolt, D., Kring, S., et al. (2007). Change in autism symptoms and maladaptive behaviors in adolescents and adults with autism spectrum disorder. Journal of Autism and Developmental Disorders, 37, 1735–1747.
- Siever, L.J. (2008). Neurobiology of aggression and violence. American Journal of Psychiatry, 165, 429–442.
- Society for Psychophysiological Research Ad Hoc Committee on Electrodermal Measures. (2012). Publication recommendations for electrodermal measurements. Psychophysiology, 49, 1017–1034.
- Söderström Anckarsäter, H. (2005). Clinical neuropsychiatric symptoms in perpetrators of severe crimes against persons. Nordic Journal of Psychiatry, 59, 246–252.
- Taylor, S.P. (1967). Aggressive behavior and physiological arousal as a function of provocation and the tendency to inhibit aggression. Journal of Personality, 35, 297–310.
- Von Aster, M., Neubauer, A., & Horn, R. (2006). Wechsler-Intelligenztest für Erwachsene, WIE Manual. Übersetzung und Adaptation der WAIS-III von David Wechsler. Frankfurt/Main: Harcourt Test Services GmbH.
- Wittchen, H.U., Wunderlich, U., Gruschitz, S., & Zaudig, M. (1997). Strukturiertes Klinisches Interview für DSM IV, Achse I (SKID-I). Goettingen, Germany: Hogrefe.
- Woodbury-Smith, M.R., Clare, I.C.H., Holland, A.J., Kearns, A., Staufenberg, E., & Watson, P. (2005). A case-control study of offenders with high functioning autistic spectrum disorders. Journal of Forensic Psychiatry & Psychology, 16, 747–763.
- World Health Organization, Dilling, H., Mombour, W., & Schmidt, M.H. (2011). Internationale Klassifikation psychischer Störungen. ICD-10 Kapitel V (F). Klinisch-diagnostische Leitlinien. Bern, Göttingen, Toronto: Huber.
- Zepf, F.D., Stadler, C., Demisch, L., Schmitt, M., Landgraf, M., & Poustka, F. (2008). Serotonergic funtioning and trait-impulsivity in attention-deficit/hyperactivity-disordered boys (ADHD): Influence of rapid tryptophan depletion. Human Psychopharmacology, 23, 43–51.