Lifespan adversities affect neural correlates of behavioral inhibition in adults
IntroductionGrowing evidence suggests that adverse experiences have long-term effects on executive functioning and underlying neural circuits. Previous work has identified functional abnormalities during inhibitory control in frontal brain regions in individuals exposed to adversities. However, thes...
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| Format: | Article |
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Frontiers Media S.A.
2024-01-01
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| Series: | Frontiers in Psychiatry |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fpsyt.2024.1298695/full |
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| author | Seda Sacu Pascal-M. Aggensteiner Maximilian Monninger Anna Kaiser Daniel Brandeis Daniel Brandeis Daniel Brandeis Tobias Banaschewski Nathalie E. Holz Nathalie E. Holz Nathalie E. Holz |
| author_facet | Seda Sacu Pascal-M. Aggensteiner Maximilian Monninger Anna Kaiser Daniel Brandeis Daniel Brandeis Daniel Brandeis Tobias Banaschewski Nathalie E. Holz Nathalie E. Holz Nathalie E. Holz |
| author_sort | Seda Sacu |
| collection | DOAJ |
| description | IntroductionGrowing evidence suggests that adverse experiences have long-term effects on executive functioning and underlying neural circuits. Previous work has identified functional abnormalities during inhibitory control in frontal brain regions in individuals exposed to adversities. However, these findings were mostly limited to specific adversity types such as maltreatment and prenatal substance abuse.MethodsWe used data from a longitudinal birth cohort study (n = 121, 70 females) to investigate the association between adversities and brain responses during inhibitory control. At the age of 33 years, all participants completed a stop-signal task during fMRI and an Adult Self-Report scale. We collected seven prenatal and postnatal adversity measures across development and performed a principal component analysis to capture common variations across those adversities, which resulted in a three-factor solution. Multiple regression analysis was performed to identify links between adversities and brain responses during inhibitory control using the identified adversity factors to show the common effect and single adversity measures to show the specific contribution of each adversity. To find neural correlates of current psychopathology during inhibitory control, we performed additional regression analyses using Adult Self-Report subscales.ResultsThe first adversity factor reflecting prenatal maternal smoking and postnatal psychosocial adversities was related to higher activation during inhibitory control in bilateral inferior frontal gyri, insula, anterior cingulate cortex, and middle temporal gyri. Similar results were found for the specific contribution of the adversities linked to the first adversity factor. In contrast, we did not identify any significant association between brain responses during inhibitory control and the second adversity factor reflecting prenatal maternal stress and obstetric risk or the third adversity factor reflecting lower maternal sensitivity. Higher current depressive symptoms were associated with higher activation in the bilateral insula and anterior cingulate cortex during inhibitory control.ConclusionOur findings extended previous work and showed that early adverse experiences have a long-term effect on the neural circuitry of inhibitory control in adulthood. Furthermore, the overlap between neural correlates of adversity and depressive symptomatology suggests that adverse experiences might increase vulnerability via neural alterations, which needs to be investigated by future longitudinal research. |
| first_indexed | 2024-03-08T12:24:29Z |
| format | Article |
| id | doaj.art-b761d4981cf6455db8a771f6b33529d4 |
| institution | Directory Open Access Journal |
| issn | 1664-0640 |
| language | English |
| last_indexed | 2024-03-08T12:24:29Z |
| publishDate | 2024-01-01 |
| publisher | Frontiers Media S.A. |
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| series | Frontiers in Psychiatry |
| spelling | doaj.art-b761d4981cf6455db8a771f6b33529d42024-01-22T12:56:10ZengFrontiers Media S.A.Frontiers in Psychiatry1664-06402024-01-011510.3389/fpsyt.2024.12986951298695Lifespan adversities affect neural correlates of behavioral inhibition in adultsSeda Sacu0Pascal-M. Aggensteiner1Maximilian Monninger2Anna Kaiser3Daniel Brandeis4Daniel Brandeis5Daniel Brandeis6Tobias Banaschewski7Nathalie E. Holz8Nathalie E. Holz9Nathalie E. Holz10Department of Child and Adolescent Psychiatry and Psychotherapy, Central Institute of Mental Health, Medical Faculty Mannheim, University of Heidelberg, Mannheim, GermanyDepartment of Child and Adolescent Psychiatry and Psychotherapy, Central Institute of Mental Health, Medical Faculty Mannheim, University of Heidelberg, Mannheim, GermanyDepartment of Child and Adolescent Psychiatry and Psychotherapy, Central Institute of Mental Health, Medical Faculty Mannheim, University of Heidelberg, Mannheim, GermanyDepartment of Child and Adolescent Psychiatry and Psychotherapy, Central Institute of Mental Health, Medical Faculty Mannheim, University of Heidelberg, Mannheim, GermanyDepartment of Child and Adolescent Psychiatry and Psychotherapy, Central Institute of Mental Health, Medical Faculty Mannheim, University of Heidelberg, Mannheim, GermanyDepartment of Child and Adolescent Psychiatry and Psychotherapy, University Hospital of Psychiatry Zurich, University of Zurich, Zurich, SwitzerlandNeuroscience Center Zurich, University of Zurich and ETH Zurich, Zurich, SwitzerlandDepartment of Child and Adolescent Psychiatry and Psychotherapy, Central Institute of Mental Health, Medical Faculty Mannheim, University of Heidelberg, Mannheim, GermanyDepartment of Child and Adolescent Psychiatry and Psychotherapy, Central Institute of Mental Health, Medical Faculty Mannheim, University of Heidelberg, Mannheim, GermanyDonders Center for Brain, Cognition and Behavior, Radboud University Nijmegen, Nijmegen, NetherlandsDepartment for Cognitive Neuroscience, Radboud University Medical Center Nijmegen, Nijmegen, NetherlandsIntroductionGrowing evidence suggests that adverse experiences have long-term effects on executive functioning and underlying neural circuits. Previous work has identified functional abnormalities during inhibitory control in frontal brain regions in individuals exposed to adversities. However, these findings were mostly limited to specific adversity types such as maltreatment and prenatal substance abuse.MethodsWe used data from a longitudinal birth cohort study (n = 121, 70 females) to investigate the association between adversities and brain responses during inhibitory control. At the age of 33 years, all participants completed a stop-signal task during fMRI and an Adult Self-Report scale. We collected seven prenatal and postnatal adversity measures across development and performed a principal component analysis to capture common variations across those adversities, which resulted in a three-factor solution. Multiple regression analysis was performed to identify links between adversities and brain responses during inhibitory control using the identified adversity factors to show the common effect and single adversity measures to show the specific contribution of each adversity. To find neural correlates of current psychopathology during inhibitory control, we performed additional regression analyses using Adult Self-Report subscales.ResultsThe first adversity factor reflecting prenatal maternal smoking and postnatal psychosocial adversities was related to higher activation during inhibitory control in bilateral inferior frontal gyri, insula, anterior cingulate cortex, and middle temporal gyri. Similar results were found for the specific contribution of the adversities linked to the first adversity factor. In contrast, we did not identify any significant association between brain responses during inhibitory control and the second adversity factor reflecting prenatal maternal stress and obstetric risk or the third adversity factor reflecting lower maternal sensitivity. Higher current depressive symptoms were associated with higher activation in the bilateral insula and anterior cingulate cortex during inhibitory control.ConclusionOur findings extended previous work and showed that early adverse experiences have a long-term effect on the neural circuitry of inhibitory control in adulthood. Furthermore, the overlap between neural correlates of adversity and depressive symptomatology suggests that adverse experiences might increase vulnerability via neural alterations, which needs to be investigated by future longitudinal research.https://www.frontiersin.org/articles/10.3389/fpsyt.2024.1298695/fulladverse experiencesearly life stressstop-signal taskfMRIinhibitory control |
| spellingShingle | Seda Sacu Pascal-M. Aggensteiner Maximilian Monninger Anna Kaiser Daniel Brandeis Daniel Brandeis Daniel Brandeis Tobias Banaschewski Nathalie E. Holz Nathalie E. Holz Nathalie E. Holz Lifespan adversities affect neural correlates of behavioral inhibition in adults Frontiers in Psychiatry adverse experiences early life stress stop-signal task fMRI inhibitory control |
| title | Lifespan adversities affect neural correlates of behavioral inhibition in adults |
| title_full | Lifespan adversities affect neural correlates of behavioral inhibition in adults |
| title_fullStr | Lifespan adversities affect neural correlates of behavioral inhibition in adults |
| title_full_unstemmed | Lifespan adversities affect neural correlates of behavioral inhibition in adults |
| title_short | Lifespan adversities affect neural correlates of behavioral inhibition in adults |
| title_sort | lifespan adversities affect neural correlates of behavioral inhibition in adults |
| topic | adverse experiences early life stress stop-signal task fMRI inhibitory control |
| url | https://www.frontiersin.org/articles/10.3389/fpsyt.2024.1298695/full |
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