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

Matteo Diano,Arianna Bagnis,Alessia Celeghin,Giuliano Geminiani,Franco Cauda,Marco Tamietto,Lawrence Weiskrantz,Sergio Duca,Tommaso Costa,Mona-Karina Tatu

doi:10.1038/srep45260

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.

Highlights

These functional magnetic resonance imaging investigations are improving our understanding of which individual brain regions respond to specific emotions
Amygdala voxels were found to contribute to the classification of happiness and disgust, in addition to fear, when multivariate pattern analysis (MVPA) techniques were applied to decode brain activity patterns induced by exposure to short movies or mental imagery[6]
The functional magnetic resonance imaging (fMRI) data were entered in a repeated-measures Analysis of Variance (ANOVA) with the six-levels within-subjects factor ‘Facial Expressions’

Summary

Introduction

These functional magnetic resonance imaging (fMRI) investigations are improving our understanding of which individual brain regions respond to specific emotions. Lesion studies in patients with selective bilateral amygdala damage reported that some of these patients may still be able to recognize fear from different stimuli, showing that fear perception does not invariably depend on the necessary contribution of the amygdala[34,35,36,37] This heterogeneity of functions in the amygdala has been initially taken as suggesting that emotions do not have a characteristic or unique neural signature[2], these findings can more parsimoniously indicate that a one-to-one mapping between single instances of emotions and brain regions is too simplistic[11]. Understanding these context- and emotion-dependent changes of amygdala inter-regional connectional patterns is of crucial importance given its implication in virtually all psychiatric or neurological states characterized by social deficits, including addiction, autism or anxiety disorders[38,39]

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Results

Conclusion