Mesocorticolimbic Interactions Mediate fMRI-Guided Regulation of Self-Generated Affective States

Abstract

Increasing evidence shows that the generation and regulation of affective responses is associated with activity of large brain networks that also include phylogenetically older regions in the brainstem. Mesencephalic regions not only control autonomic responses but also participate in the modulation of autonomic, emotional, and motivational responses. The specific contribution of the midbrain to emotion regulation in humans remains elusive. Neuroimaging studies grounding on appraisal models of emotion emphasize a major role of prefrontal cortex in modulating emotion-related cortical and subcortical regions but usually neglect the contribution of the midbrain and other brainstem regions. Here, the role of mesolimbic and mesocortical networks in core affect generation and regulation was explored during emotion regulation guided by real-time fMRI feedback of the anterior insula activity. The fMRI and functional connectivity analysis revealed that the upper midbrain significantly contributes to emotion regulation in humans. Moreover, differential functional interactions between the dopaminergic mesocorticolimbic system and frontoparietal networks mediate up and down emotion regulatory processes. Finally, these findings further indicate the potential of real-time fMRI feedback approach in guiding core affect regulation.

Neuroanatomical predictors of real‐time fMRI‐based anterior insula regulation. A supervised machine learning study

“…Overall, our neuroanatomical findings are in accordance with previous functional studies as well as recent theoretical models on the general neural mechanisms underlying brain self-regulation, both indicating the dorsolateral prefrontal cortex and lateral occipital cortex associated with attentional processes related to feedback control (Caria, 2020;Paret et al, 2018;Shibata et al, 2019;Sitaram et al, 2017), and pointing to the basal ganglia as mediators of core learning-related processes such as salience-based strategy selection and reinforcement assessment (Skottnik et al, 2019). In our analysis, the striatum contributed to the first run but not the last, suggesting decreased relevance of strategies' individuation processes when regulation is more easily attainable.…”

“…In particular, it supports adaptive predictive mechanisms during error-based and reinforcement learning (Ito, 2008;Sokolov, Miall, & Ivry, 2017;Swain, Kerr, & Thompson, 2011). An increasing number of studies demonstrated that the cerebellum mediates reward-and error-related signals ( 2020;Wagner, Kim, Savall, Schnitzer, & Luo, 2017). Existing interconnections of the posterior cerebellum with ventral and dorsal striatum (Bostan, Dum, & Strick, 2013) might be then implicated in exchanging of reward-and error-related information during real-time fMRI training.…”

“…In their analysis, Zhao and colleagues included previous real‐time fMRI studies targeting the anterior insula, amygdala and anterior cingulate cortex, all regions relevant to emotional behavior, however, no additional regions implicated in general emotion regulation emerged (Etkin et al, 2015; Grecucci, Giorgetta, Bonini, & Sanfey, 2013; Grecucci, Giorgetta, Van't Wout, et al, 2013; Messina et al, 2021). On the other hand, we previously showed that self‐regulation of AI is functionally mediated by regions in the cortical emotion regulatory network (Etkin et al, 2015), and also relies on core emotional and motivational centers in the upper mesencephalon (Caria, 2020). These results also corroborated indications of possible similarities between cognitive emotion regulation and self‐regulation of emotional brain regions (Caria, 2020; Emmert et al, 2016; Etkin et al, 2015; Gross, 2014; Paret & Hendler, 2020).…”

“…On the other hand, we previously showed that self‐regulation of AI is functionally mediated by regions in the cortical emotion regulatory network (Etkin et al, 2015), and also relies on core emotional and motivational centers in the upper mesencephalon (Caria, 2020). These results also corroborated indications of possible similarities between cognitive emotion regulation and self‐regulation of emotional brain regions (Caria, 2020; Emmert et al, 2016; Etkin et al, 2015; Gross, 2014; Paret & Hendler, 2020).…”

Self-navigating the “Island of Reil”: a systematic review of real-time fMRI neurofeedback training of insula activity

“…Based on these criteria, 1254 articles were excluded, including 333 duplicated articles, 14 non-English articles, 123 non-fMRI articles, 460 non-neurofeedback fMRI articles, 156 rtfMRI articles using other brain regions as neurofeedback sources, and 168 non-original research articles. The remaining 30 articles were entered into the next stage for full text analyses, in which another 8 articles were excluded due to the training not being based on the BOLD signal of the insula (Li et al, 2016b; Ninaus et al, 2013; Weaver et al, 2020; Zhang et al, 2020), no quantitative results being reported (Emmert et al, 2017a), focus on evaluation of task-related BOLD signal artifacts during rtfMRI NF training (Zhang et al, 2011), or conducting additional analyses based on data from pervious rtfMRI studies (Caria, 2020; Lee et al, 2011). These steps resulted in 22 articles for the final quantitative analysis.…”