Being the target of another’s emotion: a PET study

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Abstract

The eye region and gaze behaviour are known to play a major role in conveying information about direction of attention and emotional dispositions. Positron emission tomography scanning was used to explore the cerebral structures involved while subjects were asked to attribute hostile or friendly intentions to video-taped actors who directed attention towards or away from the subjects. As expected, a number of brain regions known to be involved in emotion processing was found activated when subjects had to attribute an emotion regardless of gaze direction. In addition, results indicate that gaze direction has an impact on the brain regions recruited to interpret emotions. The anterior region of the superior temporal gyrus (STG) was selectively activated during analysis of emotions through eye contact. This result provides neurophysiological evidence for privileged processing when an individual becomes personally involved as the object of another’s emotions.

Introduction

Emotions signalled by the face constitute a critical channel of social information processing. Humans are endowed with a prodigious ability in perceiving the dispositions and intentions of others, an ability often referred to as social cognition [11]. In this respect, gaze behaviour and eye contact are a conspicuous aspect of human interaction and the eye region is often used as a cue to predict emotional/mental states of others [3], [33].

The salience of the eyes as perceptual features within the face has been well demonstrated psychophysically, neuropsychologically and neurophysiologically both in humans and non-human primates [15], [31], [40], [47]. It is essential to keep in mind several distinctions between different aspects of gaze processing. Indeed, detecting where or what another individual is looking at (and thus directing her/his attention, e.g. Is she/he looking at me?) does not always involve the attribution of mental states to the other. On the other hand, interpreting the social significance of eye gaze once it has been detected (e.g. Why is this person looking at me?) does involve the attribution of mental states to the other, an ability referred to as “theory of mind” [41]. Interestingly, individuals affected by autism seem to be specifically impaired in this ability and often exhibit abnormal gaze behaviour [5].

In this respect, the first aim of this study was to determine whether there is a difference between brain regions involved when individuals experience and judge the emotional nature of a gaze compared to when they experience and judge the focus of a neutral gaze. Second, we hypothesised a difference in the brain regions recruited when subjects experienced and judged an emotional direct gaze versus an emotional averted gaze. Indeed, the processing of emotion may be fundamentally different depending on whether we interpret the emotion as directed at ourselves or directed elsewhere. We therefore, manipulated the direction of gaze of faces displaying hostile or friendly expressions as well as the task given to the subjects. The impact of such expressions was expected to depend on the gaze direction. It is only in the case of eye contact that the subject becomes personally involved as the object of the other’s emotion. If this is correct, we might predict such behavioural properties to be underpinned by some specialised neuronal circuitry. Here, we attempt to isolate the brain regions that relate specifically to this personal involvement in emotional perception.

In a previous neuroimaging study, our group has shown that temporal (right superior temporal sulcus, STS) and parietal brain regions are engaged in the perception of eyes, independent of gaze direction [48]. Temporal cortex activation in STS has also been reported during passive viewing of eye and mouth movements [42]. The amygdala, the superior temporal gyrus (STG) and the prefrontal cortex appear involved when subjects attribute mental states (e.g. “unconcerned”, “guilt”) to static pictures of the eye region [6]. The brain circuits underlying the processing of static facial expressions of emotions have been the focus of recent neuropsychological and neuroimaging studies. Their results underline the importance of several interconnected brain regions including the ventromedial and dorsolateral prefrontal cortex, the amygdala, and the right temporal, anterior cingulate and insular cortices [1], [10], [17], [36], [44].

Here we studied the perception of emotions conveyed by the eye region. We used films instead of static display to enhance realism and because additional cues to interpret emotions may be available from movement. To isolate brain structures involved in emotional processing, we compared two cognitive tasks, one involving interpretation of emotion and a second involving interpretation of the focus of attention.

Section snippets

Subjects

Ten healthy right-handed male volunteers with a mean age of 22.5 (range 20–27), screened for neurological and psychiatric antecedents participated in the experiment. Written consent was obtained after the procedure had been fully explained. The study was approved by the local Ethics Committee (Centre Leon Bérard) and was conducted in accordance with the Declaration of Helsinki. Subjects were not specifically informed about the aim of the study. Subjects were paid for their participation.

Experimental design

The

Task performance and eye movements

All subjects in the PET scan performed well in the emotional judgement (mean accuracy±S.D. DGE: 96%±5%; AGE: 94%±6%) and in the fixation distance judgement (DGC: 75%±8%; AGC; 71%±6%) tasks. Eye movements recorded in four subjects showed no differences in the amount of saccades between conditions.

Functional imaging

The first aim of the study was to investigate whether there was a difference in activated brain regions when subjects experienced and judged the emotional nature of a gaze (either direct or averted)

Discussion

The main objective of this study was to identify a brain system associated with perception and attribution of emotion displayed in the eye region in the specific context of direct gaze.

Subjects were involved in a task of detection of an emotional expression displayed in the eye region of an actor and were therefore engaged in a task of explicit emotional judgement. The interpretation of socially relevant signals (including expressions) from the eye region may be compared to a theory of mind

Acknowledgements

We thank Franck Lavenne and Luc Cinotti from the CERMEP for technical and medical assistance and Didier Le Bars for tracer synthesis. This work was supported by the INSERM, the Russell Trust and the Stevenson Foundation.

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