Novelty seeking and reward dependence‐related large‐scale brain networks functional connectivity variation during salience expectancy

Abstract

A salience network (SN) anchored in the anterior insula (AI) and dorsal anterior cingulate cortex (dACC) plays a key role in switching between brain networks during salience detection and attention regulation. Previous fMRI studies have associated expectancy behaviors and SN activation with novelty seeking (NS) and reward dependence (RD) personality traits. To address the question of how functional connectivity (FC) in the SN is modulated by internal (expectancy-related) salience assignment and different personality traits, 68 healthy participants performed a salience expectancy task using functional magnetic resonance imaging, and psychophysiological interaction analysis (PPI) was conducted to determine salience-related connectivity changes during these anticipation periods. Correlation was then evaluated between PPI and personality traits, assessed using the temperament and character inventory of 32 male participants. During high salience expectancy, SN-seed regions showed reduced FC to visual areas and parts of the default mode network, but increased FC to the central executive network. With increasing NS, participants showed significantly increasing disconnection between right AI and middle cingulate cortex when expecting high-salience pictures as compared to low-salience pictures, while increased RD also predicted decreased right dACC and caudate FC for high salience expectancy. Our findings suggest a direct link between personality traits and internal salience processing mediated by differential network integration of the SN. SN activity and coordination may therefore be moderated by novelty seeking and reward dependency personality traits, which are associated with risk of addiction. Hum Brain Mapp 38:4064-4077, 2017. © 2017 Wiley Periodicals, Inc.

Motivation but not valence modulates neuroticism‐dependent cingulate cortex and insula activity

“…The activation of ACC and insula have been previously related to neuroticism (Haas et al, ; Stein et al, ; Tolkunov et al, ), and the two regions play an important role in SN and respond to behaviorally salient events (Li et al, ; Menon and Uddin, ; Seeley et al, ). However previous studies focused on the processing of negative emotional stimuli, regardless of their motivational status.…”

The anterior insula channels prefrontal expectancy signals during affective processing

“…In the replication study, we used a similar paradigm described in detail elsewhere (Li et al, 2017). Briefly, the design was modified to show expected or unexpected emotional pictures of low or high salience.…”

Commentary: Novelty seeking and reward dependence-related large-scale brain networks functional connectivity variation during salience expectancy

“…The study by Li et al ( 2017 ) thus shed further light on the relation between personality and neuropsychological function and has important clinical implications. Considering past evidence showing associations between temperament and risk of addiction (see Crescentini et al, 2015 for a brief review), the authors argued that addiction behavior may result in part from structural or functional impairments of the SN and associated affective/reward systems (e.g., MCC, caudate), which may lead to dysfunctions during salience expectancy (e.g., perceiving low-salience stimuli with higher significance) depending on individuals' personality predispositions.…”

“…In a recent study, Li et al ( 2017 ) have provided crucial neuroimaging (fMRI) evidence about how functional connectivity (FC) and activation within and beyond the SN can be modulated by internal salience expectancy and temperament. Li et al explored salience-related connectivity changes (using psychophysiological interaction analysis, PPI) during the anticipation periods involved in a salience expectancy task, in which a group of healthy adults ( n = 68) had to rely on visual cues (arrows pointing up or down) in order to actively expect the high or low salience of the following pictures (positive and neutral pictures).…”

“…Critically, concerning FC, Li et al found that both the right dACC and the right AI (the two areas used as PPI seed regions) showed positive FC with parts of the CEN and negative FC with posterior visual areas and parts of the default mode network (DMN) as a function of high versus low salience expectancy. Moreover, with regard to FC and personality correlation, Li et al ( 2017 ) found reduced FC between right AI and right middle cingulate cortex (MCC) with increasing NS, and reduced FC between right dACC and caudate, with increasing RD. These correlations occurred when participants were expecting high-salience pictures as compared to low-salience pictures, suggesting that whether participants had high or low NS and high or low RD led them to use different salience expectancy processing neurocognitive mechanisms.…”