Amygdala Activation Predicts Gaze toward Fearful Eyes

Abstract

The human amygdala can be robustly activated by presenting fearful faces, and it has been speculated that this activation has functional relevance for redirecting the gaze toward the eye region. To clarify this relationship between amygdala activation and gaze-orienting behavior, functional magnetic resonance imaging data and eye movements were simultaneously acquired in the current study during the evaluation of facial expressions. Fearful, angry, happy, and neutral faces were briefly presented to healthy volunteers in an event-related manner. We controlled for the initial fixation by unpredictably shifting the faces downward or upward on each trial, such that the eyes or the mouth were presentedatfixation.Acrossemotionalexpressions,participantsshowedabiastoshifttheirgazetowardtheeyes,butthemagnitudeofthiseffect followed the distribution of diagnostically relevant regions in the face. Amygdala activity was specifically enhanced for fearful faces with the mouth aligned to fixation, and this differential activation predicted gazing behavior preferentially targeting the eye region. These results reveal a direct role of the amygdala in reflexive gaze initiation toward fearfully widened eyes. They mirror deficits observed in patients with amygdala lesions and open a window for future studies on patients with autism spectrum disorder, in which deficits in emotion recognition, probably related to atypical gaze patterns and abnormal amygdala activation, have been observed.

Neurons in the human amygdala selective for perceived emotion

“…Compared with our previous neuronal classification images which were based on pixelwise analyses of face regions that drive neuronal response (17), we here used a fully independent permutation test to further illustrate that when eyes are more visible, the population of neurons can discriminate the emotions better (also see Table S2). Together with a substantial prior literature, this finding supports the idea that amygdala neurons synthesize their responses based substantially on information from the eye region of faces (18,21,34).…”

“…This was complemented by a neuroimaging study showing that amygdala activity was specifically enhanced for fear faces when saccading from the mouth to the eye region (21). Patients with schizophrenia (22), social phobia (23), and autism (24) also show abnormal facial scanning patterns, which have been hypothesized to result from amygdala dysfunction (25).…”

Linking social behaviour and anxiety to attention to emotional faces in Williams syndrome

“…In addition, emotional expressions of faces have been shown to influence attention allocation, with positive (happy) emotions yielding greater visual attention than negative emotions (fearful, angry) in faces (Dodd & Porter, 2010;Plesa-Skwerer, Faja, Schofield, Verbalis, & Tager-Flusberg, 2006;Santos, Silva, Rosset, & Deruelle, 2010). The findings of atypical attention to positive emotional faces, specifically the eye region of faces in WS, are consistent with previous evidence of the role of the amygdala in directing visual attention (Gamer & Buechel, 2009;Gamer, Zurowski, & Buechel, 2010).…”

“…Future studies will need to incorporate more direct physiological measures of arousal as well as functional imaging techniques to investigate how differential amygdala reactivity is related to variability in anxiety and social reciprocity behaviours in WS. Furthermore, on the basis of the regulatory effect of the neuropeptide oxytocin on social behaviour, amygdalar responses and eye gaze (Gamer et al, 2009;Gamer et al, 2010), it will be important for future studies to explore the relationship between endogenous levels of oxytocin, amygdala reactivity and individual differences in anxiety and gaze behaviour toward emotional faces in WS. Together these future studies would provide a more detailed understanding of the role of the amygdala in attention allocation to emotional facial expressions and clarify the previously reported variations in social behaviour in WS (Dai et al, 2012;Haas et al, 2010).…”

Neurobiological Mechanisms Underlying the Blocking Effect in Aversive Learning

“…Although participants fixated significantly longer on the predictive parts of the compound, they still showed fixations to the nonpredictive parts, demonstrating that blocking is not due to a failure of stimulus detection (Kamin, 1968;Waelti et al, 2001). The observed attentional bias toward the predictive part of each compound was paralleled by enhanced amygdala responses, which is not only interesting with respect to the amygdala's role in attentional processes (Holland and Gallagher, 1999;Holland et al, 2000), but even more so with regard to its involvement in directing gaze to relevant features of the visual field, as demonstrated by both lesion (Adolphs et al, 2005) and imaging studies (Gamer and Büchel, 2009). These latter studies focused on facial features, but, considering the amygdala's more general role in detecting and responding to relevant events (Anderson and Phelps, 2001;Sander et al, 2003;Klinge et al, 2010), it is likely that such a process also occurs for more abstract stimuli that have been endowed with relevance via associative learning processes.…”