Enhanced neural activity in response to dynamic facial expressions of emotion: an fMRI study

Abstract

Dynamic facial expressions of emotion constitute natural and powerful media of communication between individuals. However, little is known about the neural substrate underlying the processing of dynamic facial expressions of emotion. We depicted the brain areas by using fMRI with 22 right-handed healthy subjects. The facial expressions are dynamically morphed from neutral to fearful or happy expressions. Two types of control stimuli were presented: (i) static facial expressions, which provided sustained fearful or happy expressions, and (ii) dynamic mosaic images, which provided dynamic information with no facial features. Subjects passively viewed these stimuli. The left amygdala was highly activated in response to dynamic facial expressions relative to both control stimuli in the case of fearful expressions, but not in the case of happy expressions. The broad region of the occipital and temporal cortices, especially in the right hemisphere, which included the activation foci of the inferior occipital gyri, middle temporal gyri, and fusiform gyri, showed higher activation during viewing of the dynamic facial expressions than it did during the viewing of either control stimulus, common to both expressions. In the same manner, the right ventral premotor cortex was also activated. These results identify the neural substrate for enhanced emotional, perceptual/cognitive, and motor processing of dynamic facial expressions of emotion.

Introduction

Dynamic facial expressions of emotion are natural and powerful media of emotional communication between individuals. However, little is known about the neural substrate underlying the processing of dynamic facial expressions. Previous neuroimaging studies have used static facial images; however, these images do not necessarily reflect the liveliness and true form of dynamic facial expressions as they occur in daily life [20].

Existing psychological evidence indicates that emotional processing is facilitated when expressions are dynamic rather than static. Several studies have shown that the dynamic presentation of facial expressions improves recognition of the emotional content of the expressions [15], [20], [32]. In neuropsychological studies, dynamic presentation improved emotion recognition relative to static presentation in a brain damaged patients [10]. Another line of evidence indicates that the dynamic presentation of facial expressions affects not only emotional processing but also various types of perceptual and/or cognitive processing for faces. Several studies have reported that the differences between spontaneous and deliberate expressions were more evident in the case of dynamic expressions, as compared to static expressions [9], [23], [24]. Other studies have reported that the dynamic presentation of facial expressions facilitated age [5] and familiarity [33] recognition, as compared with static image presentations.

Previous neuroimaging studies have demonstrated that static facial expressions of emotion activate the emotion-related brain regions, such as the amygdala, especially in the case of negative emotions such as fear [6], [18], [19], [37], [38], [43], [44], [51], [52]. Some areas in the visual cortices have also been shown to specifically relate to the analysis of observed facial images; these areas include the inferior occipital gyrus [28], the fusiform gyrus [30], [45], and the middle temporal gyrus and superior temporal sulcus (STS) [30], [45]. Based on the aforementioned psychological findings, we expected that these brain regions might be more activated by dynamic facial expressions than by the corresponding static expressions. This concept was also supported by recent functional imaging studies, which reported that the observation of another's eye and mouth movements, both of which are important social signals, induced higher activation of the STS [41], [46], [53] and fusiform gyrus [41].

One might also expect that additional brain structures may be involved in the processing of dynamic facial expressions. A recent fMRI study that examined the neural correlates of the perception of movement of others' facial parts reported the activation of the ventral premotor cortex [8] and intraparietal sulcus [41], [46]. Though it remains uncertain whether these areas are also active when subjects observe facial movements that provide emotional information, previous psychological evidence indicating spontaneous facial mimicry while viewing others' facial expressions [25] suggests the involvement of these motor-related areas.

In the present study, we measured brain activity by fMRI when subjects were passively observing dynamic emotional facial expressions. We used a computer morphing technique to present the dynamic expressions. This method allowed us to strictly compare the dynamic and static presentation of facial expressions relative to other methods, such as comparison between videotaped films and frames cut from the films. In addition, because this method enabled us to implement motion on static images chosen from a stimulus set frequently used in previous studies [14], the results can be properly compared with previous findings. In particular, we were interested in the facial expressions of fear and happiness, as previous studies using static expressions have yielded a lot of information with respect to these expressions of emotion (e.g., Ref. [6]). For comparison with the dynamic expressions, two types of control condition were prepared. In the primary condition, subjects viewed fearful or happy expressions that were static; these expressions provided images of sustained emotional expression. In an additional condition, subjects observed dynamic mosaic images; these images provided dynamic information with no facial or emotional properties. This condition allowed us to test whether higher brain activity for dynamic facial expressions, as compared to static expressions, was due, simply, to the processing of dynamic visual information. Based on the aforementioned psychological and neuroscientific evidence, we predicted that, the observation of dynamic facial expressions would induce higher activation in the amygdala compared with both control conditions, specifically in the case of fearful expressions. In addition, we predicted that dynamic facial expressions of both emotions would elicit the higher activity in the face-related visual areas including the inferior occipital gyrus, middle temporal gyrus/STS, and fusiform gyrus, than both control stimuli would do. We also expected the activity of the premotor and parietal cortex in the same manner.