Neural response to social rejection in children with early separation experiences

Vanessa B. Puetz, Nils Kohn, Brigitte Dahmen, Mikhail Zvyagintsev, André Schüppen, Robert T. Schultz, Christine Marcelle Heim, Gereon R. Fink, Beate Herpertz-Dahlmann, Kerstin Konrad

Research output: Contribution to journalArticle

25 Citations (Scopus)

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.

Original languageEnglish (US)
Pages (from-to)1328-1337.e8
JournalJournal of the American Academy of Child and Adolescent Psychiatry
Volume53
Issue number12
DOIs
StatePublished - Jan 1 2014

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Social Distance
Psychological Stress
Gyrus Cinguli
Prefrontal Cortex
Emotions
Ventral Tegmental Area
Frustration
Temporal Lobe
Arousal
Thalamus
Mood Disorders
Magnetic Resonance Imaging
Brain

All Science Journal Classification (ASJC) codes

  • Developmental and Educational Psychology
  • Psychiatry and Mental health

Cite this

Puetz, V. B., Kohn, N., Dahmen, B., Zvyagintsev, M., Schüppen, A., Schultz, R. T., ... Konrad, K. (2014). Neural response to social rejection in children with early separation experiences. Journal of the American Academy of Child and Adolescent Psychiatry, 53(12), 1328-1337.e8. https://doi.org/10.1016/j.jaac.2014.09.004
Puetz, Vanessa B. ; Kohn, Nils ; Dahmen, Brigitte ; Zvyagintsev, Mikhail ; Schüppen, André ; Schultz, Robert T. ; Heim, Christine Marcelle ; Fink, Gereon R. ; Herpertz-Dahlmann, Beate ; Konrad, Kerstin. / Neural response to social rejection in children with early separation experiences. In: Journal of the American Academy of Child and Adolescent Psychiatry. 2014 ; Vol. 53, No. 12. pp. 1328-1337.e8.
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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.",
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Puetz, VB, Kohn, N, Dahmen, B, Zvyagintsev, M, Schüppen, A, Schultz, RT, Heim, CM, Fink, GR, Herpertz-Dahlmann, B & Konrad, K 2014, 'Neural response to social rejection in children with early separation experiences', Journal of the American Academy of Child and Adolescent Psychiatry, vol. 53, no. 12, pp. 1328-1337.e8. https://doi.org/10.1016/j.jaac.2014.09.004

Neural response to social rejection in children with early separation experiences. / Puetz, Vanessa B.; Kohn, Nils; Dahmen, Brigitte; Zvyagintsev, Mikhail; Schüppen, André; Schultz, Robert T.; Heim, Christine Marcelle; Fink, Gereon R.; Herpertz-Dahlmann, Beate; Konrad, Kerstin.

In: Journal of the American Academy of Child and Adolescent Psychiatry, Vol. 53, No. 12, 01.01.2014, p. 1328-1337.e8.

Research output: Contribution to journalArticle

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T1 - Neural response to social rejection in children with early separation experiences

AU - Puetz, Vanessa B.

AU - Kohn, Nils

AU - Dahmen, Brigitte

AU - Zvyagintsev, Mikhail

AU - Schüppen, André

AU - Schultz, Robert T.

AU - Heim, Christine Marcelle

AU - Fink, Gereon R.

AU - Herpertz-Dahlmann, Beate

AU - Konrad, Kerstin

PY - 2014/1/1

Y1 - 2014/1/1

N2 - 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.

AB - 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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