Emotion perception and executive control interact in the salience network during emotionally charged working memory processing

Abstract

Processing of emotional stimuli can either hinder or facilitate ongoing working memory (WM); however, the neural basis of these effects remains largely unknown. Here we examined the neural mechanisms of these paradoxical effects by implementing a novel emotional WM task in an fMRI study. Twenty-five young healthy participants performed an N-back task with fearful and neutral faces as stimuli. Participants made more errors when performing 0-back task with fearful versus neutral faces, whereas they made fewer errors when performing 2-back task with fearful versus neutral faces. These emotional impairment and enhancement on behavioral performance paralleled significant interactions in distributed regions in the salience network including anterior insula (AI) and dorsal cingulate cortex (dACC), as well as in emotion perception network including amygdala and temporal-occipital association cortex (TOC). The dorsal AI (dAI) and dACC were more activated when comparing fearful with neutral faces in 0-back task. Contrarily, dAI showed reduced activation, while TOC and amygdala showed stronger responses to fearful as compared to neutral faces in the 2-back task. These findings provide direct neural evidence to the emerging dual competition model suggesting that the salience network plays a critical role in mediating interaction between emotion perception and executive control when facing ever-changing behavioral demands.

Multimodal Fusion With Reference: Searching for Joint Neuromarkers of Working Memory Deficits in Schizophrenia

“…It integrates external sensory input with the limbic system and is integral to the awareness of the body’s state (interoception) [40]. Recent studies report that the dorsal anterior insular and dACC, core regions of the salience network, play a critical role in mediating the interaction between emotion perception and executive control involving in emotional working memory processing [41]. Although the DLPFC lesion is reported consistently in patients with schizophrenia relative to healthy subjects, abnormal activation patterns are not restricted to this region.…”

Neural architecture underlying classification of face perception paradigms

“…However, our approach was to move beyond this single node to an expanded focus on multiple, distributed functional networks of regions that are differentially engaged by face task requirements (Ishai et al, 2005). Observed convergence in Cluster 1 across dorsal anterior cingulate and orbital frontoinsular cortices suggests a strong role in salience processing (Seeley et al, 2007) to detect and evaluate facial stimuli (Menon and Uddin, 2010; De Martino et al, 2009) in terms of external relevance to one’s self (Ramasubbu et al, 2011) and anticipated outcomes (Nahum et al, 2011), resulting in the mediation of cognitive-affective interactions (Luo et al, 2014). Facial processing of salient features includes not only analysis of a presented face, but also analysis of the emotional expression, gaze, and visuospatial motion, particularly speech-related lip movements (Bruce and Young, 1986).…”

“…Facial processing of salient features includes not only analysis of a presented face, but also analysis of the emotional expression, gaze, and visuospatial motion, particularly speech-related lip movements (Bruce and Young, 1986). In addition to regions associated with the salience network, Cluster 1 included convergence in sensorimotor and premotor areas, driven by tasks associated with facial imitation and movement execution; lateral prefrontal cortex, explained by an association with cognitively demanding tasks (e.g., facial n-back task; Bzdok et al, 2012; Luo et al, 2014); and the superior temporal sulcus, which has been linked to assessment of gaze (Hoffman and Haxby, 2000; Grosbras et al, 2005), perceiving speech and non-speech mouth movements (Calvert et al, 1997; Puce et al, 1998; Rolls, 2007), and voice discrimination (Belin et al, 2000; Shah et al, 2001). Overall, Cluster 1 presented as the most heterogeneous grouping of tasks and appeared to represent a conflation across attention (Fox et al, 2005) and visuomotor responses to faces.…”

Structural connectivity profile supports laterality of the salience network

“…As the main components of the salience network, the dACC and the FIC, undertake to recognize the most salient events among a large number of internal and external stimuli to guide cognitive processing (Gradin et al, 2013;Luo et al, 2014;Manoliu et al, 2013). For example, the right FIC was reported to be dominantly involved in awareness, errors, and emotional feedback (Craig, 2009;Ronchi et al, 2015;Ullsperger, Harsay, Wessel, & Ridderinkhof, 2010).…”