Atypical dorsolateral prefrontal activity in females with conduct disorder during effortful emotion regulation

Nora Maria Raschle, Lynn Valérie Fehlbaum, Willeke Martine Menks, Anne Martinelli, Martin Prätzlich, Anka Bernhard, Katharina Ackermann, Christine M. Freitag, Stephane A. De Brito, Graeme Fairchild, Christina Stadler

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Abstract

Background: Conduct disorder (CD), which is characterized by severe aggressive and antisocial behavior, is linked to emotion processing and regulation deficits. However, the neural correlates of emotion regulation are yet to be investigated in adolescents with CD. Furthermore, it remains unclear whether CD is associated with deficits in emotional reactivity, emotion regulation, or both. Methods: We used whole-brain fMRI to study effortful emotion regulation by cognitive reappraisal in 59 female adolescents aged 15-18 years (30 with a CD diagnosis and 29 typically-developing (TD) controls) during an emotion regulation task (p<0.05, FWE-corrected).
Results: Behaviorally, in-scanner self-report ratings confirmed successful emotion regulation within each group individually, but significant group differences in emotional reactivity and reappraisal success when comparing the groups (CD<TD). fMRI results revealed significantly lower activation in left dorsolateral prefrontal cortex and angular gyrus in CD compared to TD adolescents during emotion regulation, but no group differences for emotional reactivity. Furthermore, connectivity between left dorsolateral prefrontal cortex and the bilateral putamen, right prefrontal cortex and amygdala was reduced in CD compared to TD adolescents during reappraisal. Callous-unemotional traits were unrelated to the neural activation observed, but correlated negatively with behavioral reports of emotional reactivity.
Conclusions: Our results demonstrate abnormally reduced prefrontal brain activity and functional connectivity during effortful emotion regulation in females with CD. This sheds light on the neural basis of the behavioral deficits that have been reported previously. Future studies should investigate whether cognitive interventions are effective in enhancing emotion regulation abilities and/or normalizing prefrontal and temporoparietal activity in females with CD.
Original languageEnglish
Number of pages11
JournalBiological Psychiatry: Cognitive Neuroscience and Neuroimaging
Early online date22 May 2019
DOIs
Publication statusE-pub ahead of print - 22 May 2019

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Atypical dorsolateral prefrontal activity in females with conduct disorder during effortful emotion regulation. / Raschle, Nora Maria; Fehlbaum, Lynn Valérie; Menks, Willeke Martine; Martinelli, Anne; Prätzlich, Martin; Bernhard, Anka; Ackermann, Katharina ; Freitag, Christine M.; De Brito, Stephane A.; Fairchild, Graeme; Stadler, Christina.

In: Biological Psychiatry: Cognitive Neuroscience and Neuroimaging, 22.05.2019.

Research output: Contribution to journalArticle

Raschle, Nora Maria ; Fehlbaum, Lynn Valérie ; Menks, Willeke Martine ; Martinelli, Anne ; Prätzlich, Martin ; Bernhard, Anka ; Ackermann, Katharina ; Freitag, Christine M. ; De Brito, Stephane A. ; Fairchild, Graeme ; Stadler, Christina. / Atypical dorsolateral prefrontal activity in females with conduct disorder during effortful emotion regulation. In: Biological Psychiatry: Cognitive Neuroscience and Neuroimaging. 2019.
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title = "Atypical dorsolateral prefrontal activity in females with conduct disorder during effortful emotion regulation",
abstract = "Background: Conduct disorder (CD), which is characterized by severe aggressive and antisocial behavior, is linked to emotion processing and regulation deficits. However, the neural correlates of emotion regulation are yet to be investigated in adolescents with CD. Furthermore, it remains unclear whether CD is associated with deficits in emotional reactivity, emotion regulation, or both. Methods: We used whole-brain fMRI to study effortful emotion regulation by cognitive reappraisal in 59 female adolescents aged 15-18 years (30 with a CD diagnosis and 29 typically-developing (TD) controls) during an emotion regulation task (p<0.05, FWE-corrected). Results: Behaviorally, in-scanner self-report ratings confirmed successful emotion regulation within each group individually, but significant group differences in emotional reactivity and reappraisal success when comparing the groups (CD<TD). fMRI results revealed significantly lower activation in left dorsolateral prefrontal cortex and angular gyrus in CD compared to TD adolescents during emotion regulation, but no group differences for emotional reactivity. Furthermore, connectivity between left dorsolateral prefrontal cortex and the bilateral putamen, right prefrontal cortex and amygdala was reduced in CD compared to TD adolescents during reappraisal. Callous-unemotional traits were unrelated to the neural activation observed, but correlated negatively with behavioral reports of emotional reactivity. Conclusions: Our results demonstrate abnormally reduced prefrontal brain activity and functional connectivity during effortful emotion regulation in females with CD. This sheds light on the neural basis of the behavioral deficits that have been reported previously. Future studies should investigate whether cognitive interventions are effective in enhancing emotion regulation abilities and/or normalizing prefrontal and temporoparietal activity in females with CD.",
author = "Raschle, {Nora Maria} and Fehlbaum, {Lynn Val{\'e}rie} and Menks, {Willeke Martine} and Anne Martinelli and Martin Pr{\"a}tzlich and Anka Bernhard and Katharina Ackermann and Freitag, {Christine M.} and {De Brito}, {Stephane A.} and Graeme Fairchild and Christina Stadler",
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AU - Fehlbaum, Lynn Valérie

AU - Menks, Willeke Martine

AU - Martinelli, Anne

AU - Prätzlich, Martin

AU - Bernhard, Anka

AU - Ackermann, Katharina

AU - Freitag, Christine M.

AU - De Brito, Stephane A.

AU - Fairchild, Graeme

AU - Stadler, Christina

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N2 - Background: Conduct disorder (CD), which is characterized by severe aggressive and antisocial behavior, is linked to emotion processing and regulation deficits. However, the neural correlates of emotion regulation are yet to be investigated in adolescents with CD. Furthermore, it remains unclear whether CD is associated with deficits in emotional reactivity, emotion regulation, or both. Methods: We used whole-brain fMRI to study effortful emotion regulation by cognitive reappraisal in 59 female adolescents aged 15-18 years (30 with a CD diagnosis and 29 typically-developing (TD) controls) during an emotion regulation task (p<0.05, FWE-corrected). Results: Behaviorally, in-scanner self-report ratings confirmed successful emotion regulation within each group individually, but significant group differences in emotional reactivity and reappraisal success when comparing the groups (CD<TD). fMRI results revealed significantly lower activation in left dorsolateral prefrontal cortex and angular gyrus in CD compared to TD adolescents during emotion regulation, but no group differences for emotional reactivity. Furthermore, connectivity between left dorsolateral prefrontal cortex and the bilateral putamen, right prefrontal cortex and amygdala was reduced in CD compared to TD adolescents during reappraisal. Callous-unemotional traits were unrelated to the neural activation observed, but correlated negatively with behavioral reports of emotional reactivity. Conclusions: Our results demonstrate abnormally reduced prefrontal brain activity and functional connectivity during effortful emotion regulation in females with CD. This sheds light on the neural basis of the behavioral deficits that have been reported previously. Future studies should investigate whether cognitive interventions are effective in enhancing emotion regulation abilities and/or normalizing prefrontal and temporoparietal activity in females with CD.

AB - Background: Conduct disorder (CD), which is characterized by severe aggressive and antisocial behavior, is linked to emotion processing and regulation deficits. However, the neural correlates of emotion regulation are yet to be investigated in adolescents with CD. Furthermore, it remains unclear whether CD is associated with deficits in emotional reactivity, emotion regulation, or both. Methods: We used whole-brain fMRI to study effortful emotion regulation by cognitive reappraisal in 59 female adolescents aged 15-18 years (30 with a CD diagnosis and 29 typically-developing (TD) controls) during an emotion regulation task (p<0.05, FWE-corrected). Results: Behaviorally, in-scanner self-report ratings confirmed successful emotion regulation within each group individually, but significant group differences in emotional reactivity and reappraisal success when comparing the groups (CD<TD). fMRI results revealed significantly lower activation in left dorsolateral prefrontal cortex and angular gyrus in CD compared to TD adolescents during emotion regulation, but no group differences for emotional reactivity. Furthermore, connectivity between left dorsolateral prefrontal cortex and the bilateral putamen, right prefrontal cortex and amygdala was reduced in CD compared to TD adolescents during reappraisal. Callous-unemotional traits were unrelated to the neural activation observed, but correlated negatively with behavioral reports of emotional reactivity. Conclusions: Our results demonstrate abnormally reduced prefrontal brain activity and functional connectivity during effortful emotion regulation in females with CD. This sheds light on the neural basis of the behavioral deficits that have been reported previously. Future studies should investigate whether cognitive interventions are effective in enhancing emotion regulation abilities and/or normalizing prefrontal and temporoparietal activity in females with CD.

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