Dynamic Changes in Amygdala Psychophysiological Connectivity Reveal Distinct Neural Networks for Facial Expressions of Basic Emotions

Abstract

The quest to characterize the neural signature distinctive of different basic emotions has recently come under renewed scrutiny. Here we investigated whether facial expressions of different basic emotions modulate the functional connectivity of the amygdala with the rest of the brain. To this end, we presented seventeen healthy participants (8 females) with facial expressions of anger, disgust, fear, happiness, sadness and emotional neutrality and analyzed amygdala’s psychophysiological interaction (PPI). In fact, PPI can reveal how inter-regional amygdala communications change dynamically depending on perception of various emotional expressions to recruit different brain networks, compared to the functional interactions it entertains during perception of neutral expressions. We found that for each emotion the amygdala recruited a distinctive and spatially distributed set of structures to interact with. These changes in amygdala connectional patters characterize the dynamic signature prototypical of individual emotion processing, and seemingly represent a neural mechanism that serves to implement the distinctive influence that each emotion exerts on perceptual, cognitive, and motor responses. Besides these differences, all emotions enhanced amygdala functional integration with premotor cortices compared to neutral faces. The present findings thus concur to reconceptualise the structure-function relation between brain-emotion from the traditional one-to-one mapping toward a network-based and dynamic perspective.

Distraction and Expressive Suppression Strategies in Regulation of High- and Low-Intensity Negative Emotions

“…We agree with another study 38 , which found that changes in amygdala connections are usually compared across broad domains, such as emotion processing and attention. These results suggest that structure−function relationships between brain and emotion should be reconceptualized from a dynamic perspective.…”

Emotional valence modulates the topology of the parent-infant inter-brain network

“…For example, deep brain stimulation of the basal ganglia causes impairment of emotion perception from facial and vocal expressions (Péron et al, 2010). More recent approaches have used connectivity-based measures to examine how these networks of brain regions coordinate their activity dynamically during emotion processing (Diano et al, 2017;Sato et al, 2017) . Extensive previous research has also examined how these intra-individual neural networks become disrupted during atypical development (Goulden et al, 2012;Lu et al, 2012;Nicholson et al, 2017).…”

The premotor syndrome of cervical dystonia: Disordered processing of salient environmental stimuli

“…Fast emotional face processing with responses in the amygdala at 74 ms has been demonstrated in epilepsy patients being evaluated for temporal lobectomy; in nonhuman primates, pulvinar recordings show 50‐ms latency responses to face‐like stimuli, including cartoon faces . The traditional conception of the function of the amygdala as a “fear hub” (responsive to visual images of fear alone) has been challenged by recent fMRI studies, which have shown that the amygdala was comparably active in response to facial emotional expressions indicating anger, disgust, fear, happiness, and sadness …”