Brain system segregation and pain catastrophizing in chronic pain progression

Front Neurosci. 2023 Mar 16:17:1148176. doi: 10.3389/fnins.2023.1148176. eCollection 2023.

Abstract

Pain processing involves emotional and cognitive factors that can modify pain perception. Increasing evidence suggests that pain catastrophizing (PC) is implicated, through pain-related self-thoughts, in the maladaptive plastic changes related to the maintenance of chronic pain (CP). Functional magnetic resonance imaging (fMRI) studies have shown an association between CP and two main networks: default mode (DMN) and dorsoattentional (DAN). Brain system segregation degree (SyS), an fMRI framework used to quantify the extent to which functional networks are segregated from each other, is associated with cognitive abilities in both healthy individuals and neurological patients. We hypothesized that individuals suffering from CP would show worst health-related status compared to healthy individuals and that, within CP individuals, longitudinal changes in pain experience (pain intensity and affective interference), could be predicted by SyS and PC subdomains (rumination, magnification, and helplessness). To assess the longitudinal progression of CP, two pain surveys were taken before and after an in-person assessment (physical evaluation and fMRI). We first compared the sociodemographic, health-related, and SyS data in the whole sample (no pain and pain groups). Secondly, we ran linear regression and a moderation model only in the pain group, to see the predictive and moderator values of PC and SyS in pain progression. From our sample of 347 individuals (mean age = 53.84, 55.2% women), 133 responded to having CP, and 214 denied having CP. When comparing groups, results showed significant differences in health-related questionnaires, but no differences in SyS. Within the pain group, helplessness (β = 0.325; p = 0.003), higher DMN (β = 0.193; p = 0.037), and lower DAN segregation (β = 0.215; p = 0.014) were strongly associated with a worsening in pain experience over time. Moreover, helplessness moderated the association between DMN segregation and pain experience progression (p = 0.003). Our findings indicate that the efficient functioning of these networks and catastrophizing could be used as predictors of pain progression, bringing new light to the influence of the interplay between psychological aspects and brain networks. Consequently, approaches focusing on these factors could minimize the impact on daily life activities.

Keywords: chronic pain; functional magnetic resonance imaging; pain catastrophizing; psychological distress; resilience; system segregation.

Grants and funding

This research has received funding from La Caixa Foundation (grant number LCF/PR/PR16/11110004), Institut Guttmann, and Fundació Abertis. AP-L was partially supported by Fundació La Marató De TV3 (202129-30-31). DB-F was supported in part by the Spanish Ministry of Science, Innovation and Universities (MICIU/FEDER; grant number RTI2018-095181-B-C21) and the Catalan Institute for Advanced Research and Studies Academia 2019 grant award and Fundació La Marató De TV3 (202129-30-31). JMT was partly supported by the Fundació Joan Ribas Araquistain_Fjra (PREHABILITA-IUN91752), Agency for Management of University and Research Grants, Agència de Gestió d’Ajuts Universitaris i de Recerca (2018 PROD 00172), and the European Commission (call H2020-SC1-2016-2017_RIA_777107). GC was partly supported by the Fundació La Marató De TV3 (202211-30-31). KA-P was financially supported by a Juan de la Cierva-Formación research grant (FJC2021-047380-I) of the Spanish Ministry of Science and Innovation.