Age-dependent changes in the neural substrates of empathy in autism spectrum disorder

Martin Schulte-Rüther; Ellen Greimel; Martina Piefke; Inge Kamp-Becker; Helmut Remschmidt; Gereon R Fink; Beate Herpertz-Dahlmann; Kerstin Konrad

doi:10.1093/scan/nst088

Age-dependent changes in the neural substrates of empathy in autism spectrum disorder

Soc Cogn Affect Neurosci. 2014 Aug;9(8):1118-26. doi: 10.1093/scan/nst088. Epub 2013 Jun 18.

Authors

Martin Schulte-Rüther¹, Ellen Greimel¹, Martina Piefke², Inge Kamp-Becker³, Helmut Remschmidt³, Gereon R Fink², Beate Herpertz-Dahlmann², Kerstin Konrad¹

Affiliations

¹ Child Neuropsychology Section, Department of Child and Adolescent Psychiatry, Psychosomatics, and Psychotherapy, University Hospital RWTH Aachen, Aachen, Germany, Cognitive Neuroscience, Institute of Neuroscience and Medicine (INM-3), Research Center Jülich, Jülich, Germany, JARA - Translational Brain Medicine, Department of Child and Adolescent Psychiatry, Psychosomatics, and Psychotherapy, University Hospital Munich, Munich, Germany, Neurobiology and Genetics of Behavior, Department of Psychology and Psychotherapy, Witten/Herdecke University, Germany, Department of Child and Adolescent Psychiatry, Psychosomatics, and Psychotherapy, Philipps University Marburg, Marburg, Germany, Department of Neurology, University Hospital Cologne, Cologne, Germany, and Department of Child and Adolescent Psychiatry, Psychosomatics, and Psychotherapy, University Hospital RWTH Aachen, GermanyChild Neuropsychology Section, Department of Child and Adolescent Psychiatry, Psychosomatics, and Psychotherapy, University Hospital RWTH Aachen, Aachen, Germany, Cognitive Neuroscience, Institute of Neuroscience and Medicine (INM-3), Research Center Jülich, Jülich, Germany, JARA - Translational Brain Medicine, Department of Child and Adolescent Psychiatry, Psychosomatics, and Psychotherapy, University Hospital Munich, Munich, Germany, Neurobiology and Genetics of Behavior, Department of Psychology and Psychotherapy, Witten/Herdecke University, Germany, Department of Child and Adolescent Psychiatry, Psychosomatics, and Psychotherapy, Philipps University Marburg, Marburg, Germany, Department of Neurology, University Hospital Cologne, Cologne, Germany, and Department of Child and Adolescent Psychiatry, Psychosomatics, and Psychotherapy, University Hospital RWTH Aachen, GermanyChild Neuropsychology Section, Department of Child and Adolescent Psychiatry, Psychosomatics, and Psychotherapy, University Hospital RWTH Aachen, Aachen, Germany, Cognitive Neuroscience, Institute of Neuroscience and Medic
² Child Neuropsychology Section, Department of Child and Adolescent Psychiatry, Psychosomatics, and Psychotherapy, University Hospital RWTH Aachen, Aachen, Germany, Cognitive Neuroscience, Institute of Neuroscience and Medicine (INM-3), Research Center Jülich, Jülich, Germany, JARA - Translational Brain Medicine, Department of Child and Adolescent Psychiatry, Psychosomatics, and Psychotherapy, University Hospital Munich, Munich, Germany, Neurobiology and Genetics of Behavior, Department of Psychology and Psychotherapy, Witten/Herdecke University, Germany, Department of Child and Adolescent Psychiatry, Psychosomatics, and Psychotherapy, Philipps University Marburg, Marburg, Germany, Department of Neurology, University Hospital Cologne, Cologne, Germany, and Department of Child and Adolescent Psychiatry, Psychosomatics, and Psychotherapy, University Hospital RWTH Aachen, GermanyChild Neuropsychology Section, Department of Child and Adolescent Psychiatry, Psychosomatics, and Psychotherapy, University Hospital RWTH Aachen, Aachen, Germany, Cognitive Neuroscience, Institute of Neuroscience and Medicine (INM-3), Research Center Jülich, Jülich, Germany, JARA - Translational Brain Medicine, Department of Child and Adolescent Psychiatry, Psychosomatics, and Psychotherapy, University Hospital Munich, Munich, Germany, Neurobiology and Genetics of Behavior, Department of Psychology and Psychotherapy, Witten/Herdecke University, Germany, Department of Child and Adolescent Psychiatry, Psychosomatics, and Psychotherapy, Philipps University Marburg, Marburg, Germany, Department of Neurology, University Hospital Cologne, Cologne, Germany, and Department of Child and Adolescent Psychiatry, Psychosomatics, and Psychotherapy, University Hospital RWTH Aachen, Germany.
³ Child Neuropsychology Section, Department of Child and Adolescent Psychiatry, Psychosomatics, and Psychotherapy, University Hospital RWTH Aachen, Aachen, Germany, Cognitive Neuroscience, Institute of Neuroscience and Medicine (INM-3), Research Center Jülich, Jülich, Germany, JARA - Translational Brain Medicine, Department of Child and Adolescent Psychiatry, Psychosomatics, and Psychotherapy, University Hospital Munich, Munich, Germany, Neurobiology and Genetics of Behavior, Department of Psychology and Psychotherapy, Witten/Herdecke University, Germany, Department of Child and Adolescent Psychiatry, Psychosomatics, and Psychotherapy, Philipps University Marburg, Marburg, Germany, Department of Neurology, University Hospital Cologne, Cologne, Germany, and Department of Child and Adolescent Psychiatry, Psychosomatics, and Psychotherapy, University Hospital RWTH Aachen, Germany.

Abstract

In typical development, empathic abilities continue to refine during adolescence and early adulthood. Children and adolescents with autism spectrum disorders (ASD) show deficits in empathy, whereas adults with ASD may have developed compensatory strategies. We aimed at comparing developmental trajectories in the neural mechanisms underlying empathy in individuals with ASD and typically developing control (TDC) subjects. Using an explicit empathizing paradigm and functional magnetic resonance imaging, 27 participants with ASD and 27 TDC aged 12-31 years were investigated. Participants were asked to empathize with emotional faces and to either infer the face's emotional state (other-task) or to judge their own emotional response (self-task). Differential age-dependent changes were evident during the self-task in the right dorsolateral prefrontal cortex, right medial prefrontal cortex, right inferior parietal cortex, right anterior insula and occipital cortex. Age-dependent decreases in neural activation in TDC were paralleled by either increasing or unchanged age-dependent activation in ASD. These data suggest ASD-associated deviations in the developmental trajectories of self-related processing during empathizing. In TDC, age-dependent modulations of brain areas may reflect the 'fine-tuning' of cortical networks by reduction of task-unspecific brain activity. Increased age-related activation in individuals with ASD may indicate the development of compensatory mechanisms.

Keywords: developmental trajectories; facial emotion; medial prefrontal cortex; social cognition; theory of mind.

MeSH terms

Adolescent
Adult
Brain / growth & development*
Brain / physiopathology*
Child
Child Development
Child Development Disorders, Pervasive / physiopathology*
Empathy / physiology*
Facial Expression
Humans
Judgment / physiology
Magnetic Resonance Imaging
Male
Neuropsychological Tests
Young Adult