Elsevier

Cognitive Brain Research

Volume 12, Issue 2, October 2001, Pages 225-231
Cognitive Brain Research

Research report
Attention to emotion modulates fMRI activity in human right superior temporal sulcus

https://doi.org/10.1016/S0926-6410(01)00053-2Get rights and content

Abstract

A parallel neural network has been proposed for processing various types of information conveyed by faces including emotion. Using functional magnetic resonance imaging (fMRI), we tested the effect of the explicit attention to the emotional expression of the faces on the neuronal activity of the face-responsive regions. Delayed match to sample procedure was adopted. Subjects were required to match the visually presented pictures with regard to the contour of the face pictures, facial identity, and emotional expressions by valence (happy and fearful expressions) and arousal (fearful and sad expressions). Contour matching of the non-face scrambled pictures was used as a control condition. The face-responsive regions that responded more to faces than to non-face stimuli were the bilateral lateral fusiform gyrus (LFG), the right superior temporal sulcus (STS), and the bilateral intraparietal sulcus (IPS). In these regions, general attention to the face enhanced the activities of the bilateral LFG, the right STS, and the left IPS compared with attention to the contour of the facial image. Selective attention to facial emotion specifically enhanced the activity of the right STS compared with attention to the face per se. The results suggest that the right STS region plays a special role in facial emotion recognition within distributed face-processing systems. This finding may support the notion that the STS is involved in social perception.

Introduction

The face conveys various types of information, such as identity, emotion, intention (of another person), and gender. Bruce and Young [8] proposed that the different attributes of the face are processed by a parallel information processing system. Further, several lines of evidence suggest that there are distinct neural substrates for processing different aspects of the face [19]. In particular, the cerebral cortex in and near the superior temporal sulcus (STS) has been well studied as an important structure for the processing of information relevant to interpersonal communication, such as eye gaze direction, expression, and mouth movement [2]. A body of evidence suggests that the STS region is involved in the perception of eye gaze direction [31], [34], [35], [45]. Recently, a neuroimaging study [21] showed that the STS region has distinct neural representation of eye gaze direction within the distributed face-responsive areas.

Similarly, several lines of evidence have suggested that expression, which is another important social signal, is also processed in the STS. Single-cell recordings in monkeys [18] and humans [30] showed that there are independent cell populations in the STS that respond specifically to expression. Moreover, an electrical stimulation study in humans [15] showed that stimulation of the right STS disturbed labeling of facial emotions. A recent magnetoencephalography study [40] also showed an expression-specific response in the STS. Although these previous studies suggested that there might be a distinct neural representation for emotional expression in the temporal neocortex, neuroimaging studies mainly focused on the subcortical structures [7], [27], [28], [33], [44]. Furthermore, the reported activation of the STS during facial emotion recognition [3], [11], [17], [32], [39] was anterior extension of diffusely activated visual association cortices including fusiform face areas. These findings indicate that the STS is a part of the face-responsive areas, but it is still inconclusive whether the STS region plays a special role in processing the emotional expression.

In the present study, we sought to determine whether selective attention to facial emotion specifically enhanced activity in the STS. We hypothesized that selective attention to facial emotion, compared with attention to other aspects of the face, should elicit a stronger response of the STS than of other face-responsive areas. To test this, we adopted a delayed match to sample procedure with face or non-face samples. First face-responsive areas were functionally defined by comparing face tasks with a non-face one. Within these areas, tested was the effect of explicit attention to the characteristics of the face such as identity and emotional expressions. Considering the result of multi-dimensional scaling of emotional facial expressions [38], happy and fearful expressions were used in a valence discrimination task, and sad and fearful expressions were used in an arousal discrimination task.

Section snippets

Subjects

Twelve right-handed healthy volunteers (nine men and three women), aged 19–35 years, with no history of neurological or psychiatric illness, participated in the study. The study was conducted at the Biomedical Imaging Research Center, Fukui Medical University, where the protocol was approved by the ethics committee. All subjects gave their written informed consent for the study. One man’s data were excluded from the analysis owing to task performance error.

Stimuli

We used 18 facial expressions from

Behavioral data

The mean (±S.D.) percentage of correct responses was 96±2.6% for the CO task, 97±3.1% for the FA task, 92±6.2% for the HF task, and 84±9.4% for the SF task. Repeated-measures ANOVA showed that the accuracies were significantly greater in the CO task than in the other face tasks (F(1,10)=11.2, P<0.007), in the FA task than in the emotion tasks (F(1,10)=19.8, P<0.001), and in the HF task than the SF task (F(1,10)=5.2, P<0.046). Subjects performed at ceiling level during the non-face task (>99%

Discussion

We found that attention to face characteristics diffusely activate the face-responsive areas whereas the right STS was the only area which was activated by the attention to the facial emotion. The results indicate that the STS plays a unique role in processing facial emotion within the distributed human neural system for face perception. This finding also supports the notion that the STS is involved in social perception from visual cues [2]. In addition, our results show that explicit

Acknowledgements

The authors wish to thank B.J. Hessie, E.L.S., for skillful editing. This study was supported by a research grant (JSPS-RFTF97L00203) for the ‘Research for the Future’ Program from the Japan Society for the Promotion of Science.

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