Integration of gaze direction and facial expression in patients with unilateral amygdala damage

Abstract

Affective and social processes play a major role in everyday life, but appropriate methods to assess disturbances in these processes after brain lesions are still lacking. Past studies have shown that amygdala damage can impair recognition of facial expressions, particularly fear, as well as processing of gaze direction; but the mechanisms responsible for these deficits remain debated. Recent accounts of human amygdala function suggest that it is a critical structure involved in self-relevance appraisal. According to such accounts, responses to a given facial expression may vary depending on concomitant gaze direction and perceived social meaning. Here we investigated facial emotion recognition and its interaction with gaze in patients with unilateral amygdala damage (n = 19), compared to healthy controls (n = 10), using computer-generated dynamic face stimuli expressing variable intensities of fear, anger or joy, with different gaze directions (direct versus averted). If emotion perception is influenced by the self-relevance of expression based on gaze direction, a fearful face with averted gaze should be more relevant than the same expression with direct gaze because it signals danger near the observer; whereas anger with direct gaze should be more relevant than with averted gaze because it directly threatens the observer. Our results confirm a critical role for the amygdala in self-relevance appraisal, showing an interaction between gaze and emotion in healthy controls, a trend for such interaction in left-damaged patients but not in right-damaged patients. Impaired expression recognition was generally more severe for fear, but with a greater deficit for right versus left damage. These findings do not only provide new insights on human amygdala function, but may also help design novel neuropsychological tests sensitive to amygdala dysfunction in various patient populations.

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

“…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.…”

“Avoiding or approaching eyes”? Introversion/extraversion affects the gaze-cueing effect

“…Such findings would suggest that specific neural structures are strongly activated when the combination of eye gaze direction and facial expressions give rise to unambiguous, self-relevant threats (e.g., Cristinzio et al 2010). In apparent contrast with these data, showed that angry faces coupled with averted gaze and fearful faces coupled with direct gaze (ambiguous threat) elicited stronger amygdala activations than angry faces coupled with direct gaze and fearful faces coupled with averted gaze (unambiguous threat).…”

The functional profile of the human amygdala in affective processing: Insights from intracranial recordings

“…That is, eye-gaze direction of fearful faces may play a key role in arousal and threat processing, as is suggested by neuroimaging evidence in healthy (Wicker et al, 2003) and lesioned (Cristinzio et al, 2010) participants. While Sato et al (2011a) showed that both direct and averted gaze elicited differential amygdala neuronal activity, they did not control for emotion.…”