Amygdala integrates emotional expression and gaze direction in response to dynamic facial expressions

Sato, Wataru; Kochiyama, Takanori; Uono, Shota; Yoshikawa, Sakiko

doi:10.1016/j.neuroimage.2010.01.049

Cited by 55 publications

(76 citation statements)

References 54 publications

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“…We confirm that activity within motorrelated cortical areas arises 150 -200 ms after the onset of a perceived action (Nishitani and Hari, 2002;Caetano et al, 2007;Tkach et al, 2007;Catmur et al, 2010) and that the interaction between gaze direction and emotion takes place at ϳ200 -300 ms (Klucharev and Sams, 2004;Rigato et al, 2010). However, in contrast to recent accounts of human amygdala function in social cue integration (Sander et al, 2007;NЈDiaye et al, 2009;Cristinzio et al, 2010;Sato et al, 2010), we found that emotional content is processed earlier within the amygdala and independently of other cues.…”

Section: Discussionsupporting

confidence: 78%

“…Amygdala damage diminishes the brain's response to threatening faces at both the ϳ100 -150 and ϳ500 -600 ms time ranges (Rotshtein et al, 2010), and, in both infants and adults, the interaction between gaze direction and emotion takes place at ϳ200 -300 ms (Klucharev and Sams, 2004;Rigato et al, 2010). Furthermore, previous fMRI studies manipulating self-involvement during face perception revealed that facial expression and gaze direction are integrated in the medial temporal poles (Schilbach et al, 2006;Conty and Grèzes, 2012) or in amygdala (Adams and Kleck, 2003;Hadjikhani et al, 2008;NЈDiaye et al, 2009;Sato et al, 2010). Here, we show that the binding of emotion with gaze direction and pointing gesture arises at ϳ200 ms in the PM.…”

Section: Discussionmentioning

confidence: 96%

“…To assess whether the emotional system also participates in early binding of gaze, emotion, and gesture, we tested whether ERP components modulated by the emotional content of stimuli (P100, N170, and P200) (Batty and Taylor, 2003;Blau et al, 2007;van Heijnsbergen et al, 2007) were associated with activity in the amygdala, known to be highly involved in threat (Adolphs, 1999) and self-relevance processing (Sander et al, 2007;NЈDiaye et al, 2009;Sato et al, 2010). To do so, we used that structure bilaterally as a region of interest.…”

Section: Brain Network Involved In the Integration Of Self-relevant Vmentioning

confidence: 99%

“…However, these social signals can take on new significance once merged. In particular, processing of these social signals will vary according to their self-relevance, e.g., when coupled with direct gaze, angry faces are perceived to be more threatening (Sander et al, 2007;Hadjikhani et al, 2008;NЈDiaye et al, 2009;Sato et al, 2010). So far, it remains unclear how these social signals are integrated in the brain.…”

Section: Introductionmentioning

confidence: 99%

“…At the neural level, there is some evidence that emotion and gaze direction interact in the amygdala (Adams and Kleck, 2003;Hadjikhani et al, 2008;NЈDiaye et al, 2009;Sato et al, 2010), a key structure for the processing of emotionally salient stimuli (Adolphs, 2002). The amygdala may thus sustain early binding of visually presented social signals.…”

Section: Introductionmentioning

confidence: 99%

See 4 more Smart Citations

Early Binding of Gaze, Gesture, and Emotion: Neural Time Course and Correlates

Conty

Dezecache²,

Hugueville³

et al. 2012

J. Neurosci.

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Communicative intentions are transmitted by many perceptual cues, including gaze direction, body gesture, and facial expressions. However, little is known about how these visual social cues are integrated over time in the brain and, notably, whether this binding occurs in the emotional or the motor system. By coupling magnetic resonance and electroencephalography imaging in humans, we were able to show that, 200 ms after stimulus onset, the premotor cortex integrated gaze, gesture, and emotion displayed by a congener. At earlier stages, emotional content was processed independently in the amygdala (170 ms), whereas directional cues (gaze direction with pointing gesture) were combined at ϳ190 ms in the parietal and supplementary motor cortices. These results demonstrate that the early binding of visual social signals displayed by an agent engaged the dorsal pathway and the premotor cortex, possibly to facilitate the preparation of an adaptive response to another person's immediate intention.

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Section: Discussionsupporting

confidence: 78%

Section: Discussionmentioning

confidence: 96%

Section: Brain Network Involved In the Integration Of Self-relevant Vmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 3 more Smart Citations

Early Binding of Gaze, Gesture, and Emotion: Neural Time Course and Correlates

Conty

Dezecache²,

Hugueville³

et al. 2012

J. Neurosci.

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Memory for facial expressions on the autism spectrum: The influence of gaze direction and type of expression

Macinska

Jellema

2022

Autism Research

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Face memory research in autism has largely neglected memory for facial expressions, in favor of memory for identity. This study in three experiments examined the role of gaze direction and type of expression on memory for facial expressions in relation to the autism spectrum. In the learning phase, four combinations of facial expressions (joy/anger) and gaze direction (toward/away), displayed by 16 different identities, were presented. In a subsequent surprise test the same identities were presented displaying neutral expressions, and the expression of each identity had to be recalled. In Experiment 1, typically‐developed (TD) individuals with low and high Autism Quotient (AQ) scores were tested with three repetitions of each emotion/gaze combination, which did not produce any modulations. In Experiment 2, another group of TD individuals with low and high AQ scores were tested with eight repetitions, resulting in a “happy advantage” and a “direct gaze advantage”, but no interactions. In Experiment 3, individuals with high‐functioning autism (HFA) and a matched TD group were tested using eight repetitions. The HFA group revealed no emotion or gaze effects, while the matched TD group showed both a happy and a direct gaze advantage, and again no interaction. The results suggest that in autistic individuals the memory for facial expressions is intact, but is not modulated by the person's expression type and gaze direction. We discuss whether anomalous implicit learning of facial cues could have contributed to these findings, its relevance for social intuition, and its possible contribution to social deficits in autism. Lay summary It has often been found that memory for someone's face (facial identity) is less good in autism. However, it is not yet known whether memory for someone's facial expression is also less good in autism. In this study, the memory for expressions of joy and anger was investigated in typically‐developed (TD) individuals who possessed either few or many autistic‐like traits (Experiments 1 and 2), and in individuals with high‐functioning autism (Experiment 3). The gaze direction was also varied (directed either toward, or away from, the observer). We found that TD individuals best remembered expressions of joy, and remembered expressions of both joy and anger better when the gaze was directed at them. These effects did not depend on the extent to which they possessed autistic‐like traits. Autistic participants remembered the facial expression of a previously encountered person as good as TD participants did. However, in contrast to the TD participants, the memory of autistic participants was not influenced by the expression type and gaze direction of the previously encountered persons. We discuss whether this may lead to difficulties in the development of social intuition, which in turn could give rise to difficulties in social interaction that are characteristic for autism.

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Look at me, I'll remember you

Conty¹,

Grèzes²

2011

Human Brain Mapping

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Being looked at by a person enhances the subsequent memorability of her/his identity. Here, we tested the specificity of this effect and its underlying brain processes. We manipulated three social cues displayed by an agent: Gaze Direction (Direct/Averted), Emotional Expression (Anger/Neutral), and Pointing gesture (Presence/Absence). Our behavioral experiment showed that direct as compared with averted gaze perception enhanced subsequent retrieval of face identity. Similar effect of enhanced retrieval was found when pointing finger was absent as compared with present but not for anger as compared with neutral expression. The fMRI results revealed amygdala activity for both Anger and Direct gaze conditions, suggesting emotional arousal. Yet, the right hippocampus, known to play a role in self-relevant memory processes, was only revealed during direct gaze perception. Further investigations suggest that right hippocampal activity was maximal for the most self-relevant social event (i.e. actor expressing anger and pointing toward the participant with direct gaze). Altogether, our results suggest that the perception of self-relevant social cues such as direct gaze automatically prompts "self-relevant memory" processes.

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Amygdala integrates emotional expression and gaze direction in response to dynamic facial expressions

Cited by 55 publications

References 54 publications

Early Binding of Gaze, Gesture, and Emotion: Neural Time Course and Correlates

Early Binding of Gaze, Gesture, and Emotion: Neural Time Course and Correlates

Memory for facial expressions on the autism spectrum: The influence of gaze direction and type of expression

Look at me, I'll remember you

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