Elsevier

Neuropsychologia

Volume 37, Issue 9, August 1999, Pages 989-997
Neuropsychologia

Common effects of emotional valence, arousal and attention on neural activation during visual processing of pictures

https://doi.org/10.1016/S0028-3932(99)00017-2Get rights and content

Abstract

Emotion and attention heighten sensitivity to visual cues. How neural activation patterns associated with emotion change as a function of the availability of attentional resources is unknown. We used positron emission tomography (PET) and 15O-water to measure brain activity in male volunteers while they viewed emotional picture sets that could be classified according to valence or arousal. Subjects simultaneously performed a distraction task that manipulated the availability of attentional resources. Twelve scan conditions were generated in a 3×2×2 factorial design involving three levels of valence (pleasant, unpleasant and neutral), two levels of arousal and two levels of attention (low and high distraction).

Extrastriate visual cortical and anterior temporal areas were independently activated by emotional valence, arousal and attention. Common areas of activation derived from a conjunction analysis of these separate activations revealed extensive areas of activation in extrastriate visual cortex with a focus in right BA18 (12, −88, −2) (Z=5.73, P<0.001 corrected) and right anterior temporal cortex BA38 (42, 14, −30) (Z=4.03, P<0.05 corrected). These findings support an hypothesis that emotion and attention modulate both early and late stages of visual processing.

Introduction

Emotional arousal modifies the allocation of attentional resources and heightens sensitivity to environmental cues related to the motivational state induced by the provoking stimulus [30]. This is particularly true for stimuli with inherent significance for survival, a phenomenon referred to as ‘natural selective attention’ [22]. Conversely, the way in which attention is allocated during emotional arousal can significantly alter an emotional state [31], [36].

Although there is a growing literature on the functional neuroanatomy of visual attention [6], [7], [9], [16], relatively little functional neuroimaging work has addressed how attention and emotion interact during visual processing. We recently demonstrated [21] that a manipulation of attention profoundly influenced neural activation while subjects processed emotional pictures. In that paradigm subjects attended either to the spatial or emotional aspects of each picture.

An alternative approach is to vary, through an independent manipulation, the attentional resources available during picture viewing. Dual task paradigms are a powerful means for varying allocation of attentional resources and have been used in a variety of functional neuroimaging studies [32], [37]. By having subjects view pictures under conditions of high vs. low distraction, we examined how this manipulation of attention influenced neural activation patterns associated with processing emotional pictures.

One theory of emotion is that it is reducible to two fundamental dimensions, valence and arousal [23]. Valence refers to the direction of behavioral activation associated with emotion, either toward (appetitive motivation, pleasant emotion) or away from (aversive motivation, unpleasant emotion) a stimulus. Arousal is proposed to be orthogonal to valence and refers to the intensity of the emotional activation, ranging from excited to calm. To date, the neural correlates of emotional valence have been studied in a variety of functional neuroimaging paradigms [12], [19], [20], [27] but those of emotional arousal have not. Taking both dimensions of emotion into account is arguably necessary to determine whether attention interacts with emotion per se or with high arousal emotion in particular.

The right hemisphere has long been proposed to have a special role in both emotional [35] and attentional [33] processing. It has been suggested that the right hemispheric predominance in attention and emotion may be closely related [14], [15], but the nature of this interaction and the exact location within the right hemisphere where such an interaction occurs has not been determined. By examining the neural correlates of emotional valence and arousal in the context of a dual task paradigm, we were able to examine the nature and location of the interaction between attention and the two proposed dimensions of emotion.

Section snippets

Methods

Subjects were six healthy right-handed males with no history of medical, neurological or psychiatric disorder with a mean age of 33.0 years (SD=7.8). None of the subjects were taking medication nor had a history of substance abuse. All had normal visual and auditory acuity.

Twelve scan conditions were generated from a 3×2×2 factorial design. These factors included: (1) Valence: three levels; pleasant, unpleasant and neutral; (2) Arousal: two levels; high and low arousal; and (3) Attention: two

Behavioral data

Valence ratings for pleasant (mean=7.04; SD=1.27) picture sets were significantly higher (t=8.50; df=5; P<0.001) and valence ratings of unpleasant (mean=2.25; SD=1.11) picture sets were significantly lower (t=6.45; df=5; P<0.001) than valence ratings of neutral picture sets (mean=4.67; SD=1.09). Self-reported arousal was also greater during pleasant (mean=5.54; SD=2.62; t=3.82; df=5; P<0.01) and unpleasant (mean=6.83; SD=1.79; t=11.65; df=5; P<0.001) than neutral picture sets (mean=3.04;

Discussion

The purpose of this study was to evaluate how alterations in attentional resources influenced the activation patterns associated with the processing of emotion-evoking pictures. The finding of a common activation pattern associated with valence, arousal and attention in right extrastriate visual cortex and right anterior temporal cortex indicates common modulations of visual processing both at very early and late stages of cortical analysis.

Activation of extrastriate visual cortex has been

Acknowledgments

This work was supported by the Wellcome Trust amd MH00972 from NIMH to RDL.

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