Abstract
The occurrence of suicidal behaviors increases during adolescence. Hypersensitivity to negative social signals and deficits in cognitive control are putative mechanisms of suicidal behaviors, which necessitate confirmation in youths. Multidomain functional neuroimaging could enhance the identification of patients at suicidal risk beyond standard clinical measures. Three groups of adolescents (N = 96; 78% females, age = 11.6–18.1) were included: patients with depressive disorders and previous suicide attempts (SA, n = 29); patient controls with depressive disorders but without any suicide attempt history (PC, n = 35); and healthy controls (HC, n = 32). We scanned participants with 3T-MRI during social inclusion/exclusion (Cyberball Game) and response inhibition (Go-NoGo) tasks. Neural activation was indexed by the blood-oxygenation-level dependent (BOLD) of the hemodynamic response during three conditions in the Cyberball Game (“Control condition”, “Social Inclusion”, and “Social Exclusion”), and two conditions in Go-NoGo task (“Go” and “NoGo” blocks). ANCOVA-style analysis identified group effects across three whole-brain contrasts: 1) NoGo vs. Go, 2) Social inclusion vs. control condition, 3) Social exclusion vs. control condition. We found that SA had lower activation in the left insula during social inclusion vs. control condition compared to PC and HC. Moreover, SA compared to PC had higher activity in the right middle prefrontal gyrus during social exclusion vs. control condition, and in bilateral precentral gyri during NoGo vs. Go conditions. Task-related behavioral and self-report measures (Self-reported emotional reactivity in the Cyberball Game, response times and number of errors in the Go-NoGo Task) did not discriminate groups. In conclusion, adolescent suicidal behaviors are likely associated with neural alterations related to the processing of social perception and response inhibition. Further research, involving prospective designs and diverse cohorts of patients, is necessary to explore the potential of neuroimaging as a tool in understanding the emergence and progression of suicidal behaviors.
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Code availability
The primary code used for neuroimaging analysis can be openly accessed on the Open Science Framework (OSF) repository at the following link: https://osf.io/by7sm/.
Data availability
MRI data and analyses can be obtained upon request with detailed motives and objectives to Dr Johanne Renaud, Anthony Gifuni and Fabrice Jollant.
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Acknowledgements
This research was financed by Manulife Research Fund in Teen Depression, which supports the Manulife Centre for Breakthroughs in Teen Depression and Suicide Prevention in Montréal, Canada. AJG was supported the Fonds de Recherche du Québec – Santé (FRQS/MSSS Resident Physician Health Research Career Training Program). MMC was supported by a Junior 2 Research Scholar Salary from the FQRS. ML was supported by a Research Chair from FRQS and from a James McGill Professorship. MCG holds a Canada Research Chair Tier-2 and both JR and MCG are supported by the Fonds de recherche du Québec – Société et Culture research team on youth suicide prevention. The content is solely the responsibility of the authors. We thank Daysi Zentner, Geneviève Laurent, and Léa Perret for their assistance with data collection and organization. Finally, we thank the participants and their families participating in this study as well as the clinicians involved with adolescents and their families (Theodora Mikedis, Jean-Chrysostome Zanga, Didier Blondin-Lavoie).
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M.C. Geoffroy, E. Lacourse, J. Renaud, and F. Jollant designed the study. A. Gifuni and J. Renaud acquired the data, which A. Gifuni, F. Pereira, M. Chakravarty, M. Lepage, E. Lacourse, J. Renaud, and F. Jollant analyzed. A. Gifuni and F. Jollant wrote the first version of the article, which all authors reviewed. All authors approved the final version to be published and can certify that no other individuals not listed as authors have made substantial contributions to the paper.
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Gifuni, A.J., Pereira, F., Chakravarty, M.M. et al. Perception of social inclusion/exclusion and response inhibition in adolescents with past suicide attempt: a multidomain task-based fMRI study. Mol Psychiatry (2024). https://doi.org/10.1038/s41380-024-02485-w
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DOI: https://doi.org/10.1038/s41380-024-02485-w