Rapid Extraction of Emotion Regularities from Complex Scenes in the Human Brain

Antonio Schettino,Christopher Gundlach,Matthias M Müller,Sebastiaan Mathot,Rolf Zwaan

doi:10.1525/collabra.226

Abstract

Adaptive behavior requires the rapid extraction of behaviorally relevant information in the environment, with particular emphasis on emotional cues. However, the speed of emotional feature extraction from complex visual environments is largely undetermined. Here we use objective electrophysiological recordings in combination with frequency tagging to demonstrate that the extraction of emotional information from neutral, pleasant, or unpleasant naturalistic scenes can be completed at a presentation speed of 167 ms (i.e., 6 Hz) under high perceptual load. Emotional compared to neutral pictures evoked enhanced electrophysiological responses with distinct topographical activation patterns originating from different neural sources. Cortical facilitation in early visual cortex was also more pronounced for scenes with pleasant compared to unpleasant or neutral content, suggesting a positivity offset mechanism dominating under conditions of rapid scene processing. These results significantly advance our knowledge of complex scene processing in demonstrating rapid integrative content identification, particularly for emotional cues relevant for adaptive behavior in complex environments.

Highlights

The prioritization of emotional stimuli is pivotal for fast behavioral reactions, for example in the case of threat or danger when the decision for fight-or-flight needs to be made almost instantaneously in order to survive
While electrophysiological enhancement is typically interpreted as a consequence of the high relevance of valence and arousal features for adaptive behavior and survival (Frijda, 2016; Lang & Bradley, 2010), the speed at which these emotional cues are extracted from complex visual scenes is still unresolved
2003, 2009, 2008) used this technique by presenting identical images ten times per second (i.e., 10 Hz) and found larger SSVEP amplitudes for emotional compared to neutral scenes, suggesting once again attention-dependent sensory enhancement for emotional material

Summary

Introduction

The prioritization of emotional stimuli is pivotal for fast behavioral reactions, for example in the case of threat or danger when the decision for fight-or-flight needs to be made almost instantaneously in order to survive. One obvious solution is to shorten the presentation time of each individual stimulus, creating a train of identical images in rapid succession (rapid serial visual presentation; RSVP). Such a presentation typically elicits steady-state visually evoked potentials (SSVEPs), oscillatory posterior brain responses considered a continuous marker of stimulus processing in early visual cortex (Norcia, Appelbaum, Ales, Cottereau, & Rossion, 2015; Regan, 1977; Vialatte, Maurice, Dauwels, & Cichocki, 2010; Wieser, Miskovic, & Keil, 2016). 2003, 2009, 2008) used this technique by presenting identical images ten times per second (i.e., 10 Hz) and found larger SSVEP amplitudes for emotional compared to neutral scenes, suggesting once again attention-dependent sensory enhancement for emotional material

Methods

Results

Discussion

Conclusion