Valence-Dependent Coupling of Prefrontal-Amygdala Effective Connectivity during Facial Affect Processing

Abstract

Despite the importance of the prefrontal-amygdala (AMY) network for emotion processing, valence-dependent coupling within this network remains elusive. In this study, we assessed the effect of emotional valence on brain activity and effective connectivity. We tested which functional pathways within the prefrontal-AMY network are specifically engaged during the processing of emotional valence. Thirty-three healthy adults were examined with functional magnetic resonance imaging while performing a dynamic faces and dynamic shapes matching task. The valence of the facial expressions varied systematically between positive, negative, and neutral across the task. Functional contrasts determined core areas of the emotion processing circuitry, comprising the medial prefrontal cortex (MPFC), the right lateral prefrontal cortex (LPFC), the AMY, and the right fusiform face area (FFA). Dynamic causal modelling demonstrated that the bidirectional coupling within the prefrontal-AMY circuitry is modulated by emotional valence. Additionally, Bayesian model averaging showed significant bottom-up connectivity from the AMY to the MPFC during negative and neutral, but not positive, valence. Thus, our study provides strong evidence for alterations of bottom-up coupling within the prefrontal-AMY network as a function of emotional valence. Thereby our results not only advance the understanding of the human prefrontal-AMY circuitry in varying valence context, but, moreover, provide a model to examine mechanisms of valence-sensitive emotional dysregulation in neuropsychiatric disorders.

Differential Modulation of Effective Connectivity in the Brain’s Extended Face Processing System by Fearful and Sad Facial Expressions

“…Additionally, we found a significant difference between the fearful and sad associated connectivity from the amygdala to dlPFC. Overall, the pattern of connectivity observed here is generally consistent with previous investigations of implicit processing of negative expressions, particularly those findings concerning the connectivity from the amygdala to dlPFC and vmPFC to amygdala (Vai et al, 2015;Willinger et al, 2019). While we did not observe the significant modulation from the dlPFC to amygdala reported in the study by Vai et al (2015), this was likely because of their indirect interaction via the vmPFC in our model.…”

“…Given their roles, the interaction between the dlPFC and amygdala, depending on the directionality, may be important in directing conscious awareness toward and regulating emotional responses to salient emotional stimuli ( Dolcos et al, 2006 ; Banks et al, 2007 ; Costafreda et al, 2008 ; Etkin et al, 2015 ). Despite this, previous research examining the directionality of these interactions has not examined whether facial expressions with differing arousal ratings, such as fearful and sad expressions, differently modulate this relationship ( Sladky et al, 2015 ; Vai et al, 2015 ; Willinger et al, 2019 ). The sparse anatomic connectivity between these regions additionally suggests that the regulatory role of the dlPFC on the amygdala is likely dependent on interactions with mediatory regions including the vmPFC ( Phillips et al, 2003 ; Ray and Zald, 2012 ).…”

Social Behavior Is Modulated by Valence-Encoding mPFC-Amygdala Sub-circuitry

“…It is likely that these two circuits regulate general emotional states rather than specifically affecting social behaviors. Interestingly, human neuroimaging studies showed that connectivity from mPFC to amygdala is modulated by both positive and negative valence, whereas the inverse connection (BLA-mPFC) is affected only by positive valence ( Willinger et al, 2019 ). In the case of the PL-BLA circuit, our data suggest that its activation creates a negative emotional state that is sufficient to promote avoidance and leads to a lack of social preference.…”

The Effect of Emotional Valence and Arousal on Visuo-Spatial Working Memory: Incidental Emotional Learning and Memory for Object-Location

“…A possible explanation of our results is that competition for accessing the working memory system could depend upon a dichotomic evaluation between what is endowed with an emotional valence and what is not (emotional vs. non-emotional), independently from the “ valence direction ” (negative or positive). Recently, Willinger et al (2019) performed an fMRI analysis during an emotional face-matching task and found that the processing of valence directly induces changes in the strength of the bidirectional coupling within a prefrontal-amygdala circuitry (Willinger et al, 2019). Moreover, Kensinger and Schacter (2006) found that independent brain networks specifically processed either positive or negative stimuli.…”