Associations between repetitive negative thinking and resting-state network segregation among healthy middle-aged adults

Solé-Padullés, Cristina; Cattaneo, Gabriele; Marchant, Natalie L.; Cabello-Toscano, María; Mulet-Pons, Lídia; Solana, Javier; Bargalló, Núria; Tormos, Josep M.; Pascual-Leone, Álvaro; Bartrés-Faz, David · 2022 · OpenAlex-citations

DOI: 10.3389/fnagi.2022.1062887

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Summary

This study investigates the neural correlates of Repetitive Negative Thinking (RNT)—a transdiagnostic cognitive style involving worry and rumination—in healthy middle-aged adults. While RNT is a known risk factor for depression, anxiety, and cognitive decline, previous research has largely focused on young clinical populations or isolated brain regions. This research addresses a gap by examining the system segregation (SyS) of large-scale resting-state networks in a non-clinical cohort, aiming to determine how the functional integrity of networks involved in cognitive control and emotion regulation relates to perseverative thinking. The researchers analyzed data from 341 healthy participants aged 40–68 from the Barcelona Brain Health Initiative. Participants completed questionnaires assessing RNT (Perseverative Thinking Questionnaire, Penn State Worry Questionnaire, and Rumination Responses Scale), depression/anxiety/stress, emotional stability, and cognitive complaints. Resting-state functional MRI was acquired using a 3T scanner. The study employed graph theory to calculate system segregation for the Anterior Salience Network (ASN), Default Mode Network (DMN), and Executive Control Network (ECN). Linear regression models were used to identify associations between RNT scores and network segregation, controlling for demographic and clinical variables. Results indicated that RNT was significantly associated with depression, emotional stability, cognitive complaints, age, and the segregation of the left Executive Control Network (LECN) and the ASN. Specifically, higher levels of RNT were linked to increased segregation of the LECN and decreased segregation of the ASN. Post-hoc analyses revealed that increased LECN segregation corresponded to higher within-network connectivity and decreased connectivity with the ventral DMN (vDMN). Conversely, lower ASN segregation was associated with decreased within-network connectivity and increased connectivity with the vDMN. These neural patterns were specifically driven by the Perseverative Thinking Questionnaire scores rather than general depressive symptoms, distinguishing RNT from mood disorders. The findings suggest that RNT is characterized by a distinct pattern of network dysregulation: heightened executive resource allocation (increased LECN segregation) coupled with reduced differentiation of salience-processing regions (decreased ASN segregation). The increased connectivity between the ASN and vDMN may facilitate self-referential processing and autobiographical memory retrieval, while the dissociation from the LECN may impair cognitive control. This study provides the first evidence of resting-state network segregation biomarkers for RNT in middle-aged adults, highlighting that RNT involves specific alterations in the balance between executive control and self-referential networks, independent of clinical depression.

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• anxiety depression driving