Vanessa B Puetz1, Nils Kohn2, Brigitte Dahmen3, Mikhail Zvyagintsev4, André Schüppen5, Robert T Schultz6, Christine M Heim7, Gereon R Fink8, Beate Herpertz-Dahlmann9, Kerstin Konrad10. 1. Division of Psychology and Language Sciences, University College London (UCL), UK, and Child Neuropsychology Section, University Hospital Rheinisch-Westfälische Technische Hochschule (RWTH), Aachen, Germany. 2. University Hospital RWTH Aachen and JARA Translational Brain Medicine, Aachen and Jülich, Germany. 3. University Hospital RWTH Aachen. 4. University Hospital RWTH Aachen and the Brain Imaging Facility of the Interdisciplinary Centre for Clinical Research at the RWTH Aachen University. 5. Brain Imaging Facility of the Interdisciplinary Centre for Clinical Research. 6. Center for Autism Research, Children's Hospital of Philadelphia, USA. 7. Institute of Medical Psychology, Charité University Medicine Berlin, Germany. 8. Institute of Neuroscience and Medicine (INM-3), Research Centre Jülich, and University Hospital Cologne, Cologne, Germany. 9. University Hospital RWTH Aachen and JARA Translational Brain Medicine. 10. Child Neuropsychology Section, University Hospital RWTH Aachen, and JARA Translational Brain Medicine and the Institute of Neuroscience and Medicine (INM-3) Research Centre Jülich. Electronic address: kkonrad@ukaachen.de.
Abstract
OBJECTIVE: Nonhuman and human studies have documented the adverse effects of early life stress (ELS) on emotion regulation and underlying neural circuitry. Less is known about how these experiences shape social processes and neural circuitry. In this study, we thus investigated how ELS affects children's perception of, and neural response to, negative social experiences in a social exclusion paradigm (Cyberball). METHOD: Twenty-five foster or adopted children with ELS (age 10.6 ± 1.8 years, 13 male and 12 female) and 26 matched nonseparated controls (age 10.38 ± 1.7 years, 12 male and 14 female) took part in a Cyberball paradigm during functional magnetic resonance imaging (fMRI). RESULTS: During peer rejection, children with ELS reported significantly more feelings of exclusion and frustration than nonseparated controls. On the neural level, children with ELS showed reduced activation in the dorsal anterior cingulate cortex (dACC) and dorsolateral prefrontal cortex (dlPFC), and reduced connectivity between dlPFC-dACC, areas previously implicated in affect regulation. Conversely, children with ELS showed increased neural activation in brain regions involved in memory, arousal, and threat-related processing (middle temporal gyrus, thalamus, ventral tegmental area) relative to controls during social exclusion. The number of separation experiences before entering the permanent family predicted reductions in fronto-cingulate recruitment. The relationship between early separations and self-reported exclusion was mediated by dlPFC activity. CONCLUSION: The findings suggest that ELS leads to alterations in neural circuitry implicated in the regulation of socioemotional processes. This neural signature may underlie foster children's differential reactivity to rejection in everyday life and could increase risk for developing affective disorders.
OBJECTIVE: Nonhuman and human studies have documented the adverse effects of early life stress (ELS) on emotion regulation and underlying neural circuitry. Less is known about how these experiences shape social processes and neural circuitry. In this study, we thus investigated how ELS affects children's perception of, and neural response to, negative social experiences in a social exclusion paradigm (Cyberball). METHOD: Twenty-five foster or adopted children with ELS (age 10.6 ± 1.8 years, 13 male and 12 female) and 26 matched nonseparated controls (age 10.38 ± 1.7 years, 12 male and 14 female) took part in a Cyberball paradigm during functional magnetic resonance imaging (fMRI). RESULTS: During peer rejection, children with ELS reported significantly more feelings of exclusion and frustration than nonseparated controls. On the neural level, children with ELS showed reduced activation in the dorsal anterior cingulate cortex (dACC) and dorsolateral prefrontal cortex (dlPFC), and reduced connectivity between dlPFC-dACC, areas previously implicated in affect regulation. Conversely, children with ELS showed increased neural activation in brain regions involved in memory, arousal, and threat-related processing (middle temporal gyrus, thalamus, ventral tegmental area) relative to controls during social exclusion. The number of separation experiences before entering the permanent family predicted reductions in fronto-cingulate recruitment. The relationship between early separations and self-reported exclusion was mediated by dlPFC activity. CONCLUSION: The findings suggest that ELS leads to alterations in neural circuitry implicated in the regulation of socioemotional processes. This neural signature may underlie foster children's differential reactivity to rejection in everyday life and could increase risk for developing affective disorders.
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