Vulnerability and resilience to prenatal stress exposure: behavioral and molecular characterization in adolescent rats

Abstract Exposure to stress can lead to long lasting behavioral and neurobiological consequences, which may enhance the susceptibility for the onset of mental disorders. However, there are significant individual differences in the outcome of stress exposure since only a percentage of exposed individ...

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Main Authors: Kerstin Camile Creutzberg, Veronica Begni, Rodrigo Orso, Francisco Sindermann Lumertz, Luis Eduardo Wearick-Silva, Saulo Gantes Tractenberg, Moira Marizzoni, Annamaria Cattaneo, Rodrigo Grassi-Oliveira, Marco Andrea Riva
Format: Article
Language:English
Published: Nature Publishing Group 2023-11-01
Series:Translational Psychiatry
Online Access:https://doi.org/10.1038/s41398-023-02653-6
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author Kerstin Camile Creutzberg
Veronica Begni
Rodrigo Orso
Francisco Sindermann Lumertz
Luis Eduardo Wearick-Silva
Saulo Gantes Tractenberg
Moira Marizzoni
Annamaria Cattaneo
Rodrigo Grassi-Oliveira
Marco Andrea Riva
author_facet Kerstin Camile Creutzberg
Veronica Begni
Rodrigo Orso
Francisco Sindermann Lumertz
Luis Eduardo Wearick-Silva
Saulo Gantes Tractenberg
Moira Marizzoni
Annamaria Cattaneo
Rodrigo Grassi-Oliveira
Marco Andrea Riva
author_sort Kerstin Camile Creutzberg
collection DOAJ
description Abstract Exposure to stress can lead to long lasting behavioral and neurobiological consequences, which may enhance the susceptibility for the onset of mental disorders. However, there are significant individual differences in the outcome of stress exposure since only a percentage of exposed individuals may show pathological consequences, whereas others appear to be resilient. In this study, we aimed to characterize the effects of prenatal stress (PNS) exposure in rats at adolescence and to identify subgroup of animals with a differential response to the gestational manipulation. PNS adolescent offspring (regardless of sex) showed impaired emotionality in different pathological domains, such as anhedonia, anxiety, and sociability. However, using cluster analysis of the behavioral data we could identify 70% of PNS-exposed animals as vulnerable (PNS-vul), whereas the remaining 30% were considered resilient (PNS-res). At the molecular level, we found that PNS-res males show a reduced basal activation of the ventral hippocampus whereas other regions, such as amygdala and dorsal hippocampus, show significant PNS-induced changes regardless from vulnerability or resilience. Taken together, our results provide evidence of the variability in the behavioral and neurobiological effects of PNS-exposed offspring at adolescence. While these data may advance our understanding of the association between exposure to stress during gestation and the risk for psychopathology, the investigation of the mechanisms associated to stress vulnerability or resilience may be instrumental to develop novel strategies for therapeutic intervention.
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spelling doaj.art-14c27868a3654187a3fe69dc261784732023-11-26T14:19:18ZengNature Publishing GroupTranslational Psychiatry2158-31882023-11-0113111110.1038/s41398-023-02653-6Vulnerability and resilience to prenatal stress exposure: behavioral and molecular characterization in adolescent ratsKerstin Camile Creutzberg0Veronica Begni1Rodrigo Orso2Francisco Sindermann Lumertz3Luis Eduardo Wearick-Silva4Saulo Gantes Tractenberg5Moira Marizzoni6Annamaria Cattaneo7Rodrigo Grassi-Oliveira8Marco Andrea Riva9Department of Pharmacological and Biomolecular Sciences, University of MilanDepartment of Pharmacological and Biomolecular Sciences, University of MilanDepartment of Pharmacological and Biomolecular Sciences, University of MilanSchool of Medicine, Pontifical Catholic University of Rio Grande do SulSchool of Medicine, Pontifical Catholic University of Rio Grande do SulSchool of Medicine, Pontifical Catholic University of Rio Grande do SulBiological Psychiatry Unit, IRCCS Istituto Centro San Giovanni di Dio FatebenefratelliDepartment of Pharmacological and Biomolecular Sciences, University of MilanSchool of Medicine, Pontifical Catholic University of Rio Grande do SulDepartment of Pharmacological and Biomolecular Sciences, University of MilanAbstract Exposure to stress can lead to long lasting behavioral and neurobiological consequences, which may enhance the susceptibility for the onset of mental disorders. However, there are significant individual differences in the outcome of stress exposure since only a percentage of exposed individuals may show pathological consequences, whereas others appear to be resilient. In this study, we aimed to characterize the effects of prenatal stress (PNS) exposure in rats at adolescence and to identify subgroup of animals with a differential response to the gestational manipulation. PNS adolescent offspring (regardless of sex) showed impaired emotionality in different pathological domains, such as anhedonia, anxiety, and sociability. However, using cluster analysis of the behavioral data we could identify 70% of PNS-exposed animals as vulnerable (PNS-vul), whereas the remaining 30% were considered resilient (PNS-res). At the molecular level, we found that PNS-res males show a reduced basal activation of the ventral hippocampus whereas other regions, such as amygdala and dorsal hippocampus, show significant PNS-induced changes regardless from vulnerability or resilience. Taken together, our results provide evidence of the variability in the behavioral and neurobiological effects of PNS-exposed offspring at adolescence. While these data may advance our understanding of the association between exposure to stress during gestation and the risk for psychopathology, the investigation of the mechanisms associated to stress vulnerability or resilience may be instrumental to develop novel strategies for therapeutic intervention.https://doi.org/10.1038/s41398-023-02653-6
spellingShingle Kerstin Camile Creutzberg
Veronica Begni
Rodrigo Orso
Francisco Sindermann Lumertz
Luis Eduardo Wearick-Silva
Saulo Gantes Tractenberg
Moira Marizzoni
Annamaria Cattaneo
Rodrigo Grassi-Oliveira
Marco Andrea Riva
Vulnerability and resilience to prenatal stress exposure: behavioral and molecular characterization in adolescent rats
Translational Psychiatry
title Vulnerability and resilience to prenatal stress exposure: behavioral and molecular characterization in adolescent rats
title_full Vulnerability and resilience to prenatal stress exposure: behavioral and molecular characterization in adolescent rats
title_fullStr Vulnerability and resilience to prenatal stress exposure: behavioral and molecular characterization in adolescent rats
title_full_unstemmed Vulnerability and resilience to prenatal stress exposure: behavioral and molecular characterization in adolescent rats
title_short Vulnerability and resilience to prenatal stress exposure: behavioral and molecular characterization in adolescent rats
title_sort vulnerability and resilience to prenatal stress exposure behavioral and molecular characterization in adolescent rats
url https://doi.org/10.1038/s41398-023-02653-6
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