Abstract

The regulation of cognitive and emotional processes is critical for proper executive functions and social behavior, but its specific mechanisms remain unknown. Here, we addressed this issue by studying with functional magnetic resonance imaging the changes in network topology that underlie competitive interactions between emotional and cognitive networks in healthy participants. Our behavioral paradigm contrasted periods with high emotional and cognitive demands by including a sadness provocation task followed by a spatial working memory task. The sharp contrast between successive tasks was designed to enhance the separability of emotional and cognitive networks and reveal areas that regulate the flow of information between them (hubs). By applying graph analysis methods on functional connectivity between 20 regions of interest in 22 participants we identified two main brain network modules, one dorsal and one ventral, and their hub areas: the left dorsolateral prefrontal cortex (dlPFC) and the left medial frontal pole (mFP). These hub areas did not modulate their mutual functional connectivity following sadness but they did so through an interposed area, the subgenual anterior cingulate cortex (sACC). Our results identify dlPFC and mFP as areas regulating interactions between emotional and cognitive networks, and suggest that their modulation by sadness experience is mediated by sACC.

Highlights

  • The regulation of cognitive and emotional processes is critical for proper executive functions and social behavior, but its specific mechanisms remain unknown

  • We found that the dorsolateral prefrontal cortex (dlPFC) acted as connector hub of the dorsal subnetwork, and medial fronto-polar cortex was the connector hub of the ventral subnetwork, but they both interacted via the subgenual anterior cingulate cortex (sACC) in the ventral subnetwork, and these connectivity patterns were associated with the intensity of the sadness experienced by the participants

  • We found that participants in the high-sadness group diminished their working memory (WM) performance following sadness provocation (Fig. 2A, 3-way analyses of variance (ANOVA) with factors high-sadness/low-sadness, WM1/WM2 and subject identity, n = 20, p = 0.04 for the interaction between high-sadness/low-sadness groups and WM1/WM2, paired sample t-test p = 0.033 for WM1-WM2 errors in the high-sadness group, p = 0.37 for WM1-WM2 errors in the low-sadness group)

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Summary

Introduction

The regulation of cognitive and emotional processes is critical for proper executive functions and social behavior, but its specific mechanisms remain unknown. By applying graph analysis methods on functional connectivity between 20 regions of interest in 22 participants we identified two main brain network modules, one dorsal and one ventral, and their hub areas: the left dorsolateral prefrontal cortex (dlPFC) and the left medial frontal pole (mFP). Dorsal areas are typically deactivated (dorsolateral prefrontal cortex (dlPFC), dorsal anterior cingulate cortex (dACC) and parietal cortex) and ventral and subcortical areas are activated (insula, orbitofrontal cortex (OFC), subgenual anterior cingulate cortex (sACC), amygdala, hippocampus), while some other areas may play the role of interconnecting these two networks (basal ganglia, thalamus, rostral ACC)[19,20] At present, it is unclear whether these integration-segregation dynamics occur diffusely between all these participating areas, or whether there are specific areas that channel primarily these interactions. Of particular interest are connector hub nodes, characterized by having high degree and participation coefficient, which are likely to regulate the flow and integration of information between the communities[25]

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