Dissociable Modulation of Overt Visual Attention in Valence and Arousal Revealed by Topology of Scan Path

Jianguang Ni,Nanhui Chen,Jianhong Wang,Xintian Hu,Zhengbo Wang,Yuanye Ma,Huihui Jiang,Yuejia Luo,Yixiang Jin,Jan Lauwereyns

doi:10.1371/journal.pone.0018262

Abstract

Emotional stimuli have evolutionary significance for the survival of organisms; therefore, they are attention-grabbing and are processed preferentially. The neural underpinnings of two principle emotional dimensions in affective space, valence (degree of pleasantness) and arousal (intensity of evoked emotion), have been shown to be dissociable in the olfactory, gustatory and memory systems. However, the separable roles of valence and arousal in scene perception are poorly understood. In this study, we asked how these two emotional dimensions modulate overt visual attention. Twenty-two healthy volunteers freely viewed images from the International Affective Picture System (IAPS) that were graded for affective levels of valence and arousal (high, medium, and low). Subjects' heads were immobilized and eye movements were recorded by camera to track overt shifts of visual attention. Algebraic graph-based approaches were introduced to model scan paths as weighted undirected path graphs, generating global topology metrics that characterize the algebraic connectivity of scan paths. Our data suggest that human subjects show different scanning patterns to stimuli with different affective ratings. Valence salient stimuli (with neutral arousal) elicited faster and larger shifts of attention, while arousal salient stimuli (with neutral valence) elicited local scanning, dense attention allocation and deep processing. Furthermore, our model revealed that the modulatory effect of valence was linearly related to the valence level, whereas the relation between the modulatory effect and the level of arousal was nonlinear. Hence, visual attention seems to be modulated by mechanisms that are separate for valence and arousal.

Highlights

The emotional system is intrinsically significant to the survival of the organism
Picture familiarity ratings were not significantly different between valence and arousal blocks, despite there being a marked difference within both the Valence Block (VB) and Arousal Block (AB), due to the enhanced memory effect [8,37]
Within the three graded arousal levels, j2 had no significant quadratic trend (F(1, 216) = 2.56, p = 0.11); j3 exhibited a marginally significant quadratic trend (F(1, 216) = 3.69, p = 0.056). These results suggest that embedded scan paths in the valence block were more stable than in the arousal block and indicated a possible nonlinear arousal effect

Summary

Introduction

The emotional system is intrinsically significant to the survival of the organism. From an evolutionary perspective, emotional experience enables organisms to automatically evade threats in the environment, such as predators [1]. We hypothesized that valence and arousal play different roles in guiding visual attention as human subjects freely view affective images. To test this hypothesis, we needed to overcome two technical difficulties. We used complex color pictures selected from the International Affective Picture System (IAPS) as visual stimuli [14] These pictures were categorized into two stimuli blocks, the Valence Block (VB) and the Arousal Block (AB), and a single emotional dimension dominated pictures in each block. We integrated the global topology information provided by the SPPG model with local pattern information from discrete local metrics to explore the separable roles of valence and arousal in modulating overt visual attention

Results

Discussion

Methods