Unattended emotional faces elicit early lateralized amygdala–frontal and fusiform activations

doi:10.1016/j.neuroimage.2009.12.093

NeuroImage

Volume 50, Issue 2, 1 April 2010, Pages 727-733

https://doi.org/10.1016/j.neuroimage.2009.12.093 Get rights and content

Abstract

Human adaptive behaviour to potential threats involves specialized brain responses allowing rapid and reflexive processing of the sensory input and a more directed processing for later evaluation of the nature of the threat. The amygdalae are known to play a key role in emotion processing. It is suggested that the amygdalae process threat-related information through a fast subcortical route and slower cortical feedback. Evidence from human data supporting this hypothesis is lacking. The present study investigated event-related neural responses during processing of facial emotions in the unattended hemifield using magnetoencephalography (MEG) and found activations of the amygdala and anterior cingulate cortex to fear as early as 100 ms. The right amygdala exhibited temporally dissociated activations to input from different visual fields, suggesting early subcortical versus later cortical processing of fear. We also observed asymmetrical fusiform activity related to lateralized feed-forward processing of the faces in the visual–ventral stream. Results demonstrate fast, automatic, and parallel processing of unattended emotional faces, providing important insights into the specific and dissociated neural pathways in emotion and face perception.

Section snippets

Subjects

Fourteen healthy, right-handed subjects (mean age, 27 years; seven females) participated in the study. None had a history of neurological or psychiatric disorders and all had normal vision. All subjects provided informed written consent; the study was approved by the Hospital for Sick Children Research Ethics Board.

Task

We studied the effect of task-irrelevant emotional expressions and their location in the visual field (left or right hemifield). Stimuli were projected on a black-background screen

Reaction times

The reaction times (RTs) showed a significant interaction between emotion and the location of the face in the visual field (P < 0.001, two-way ANOVA): RTs to the target (the scrambled pattern) were the longest when the target was paired with a LVF fearful face (mean value = 324 ms). These RTs were significantly longer than those when the target was presented with either a neutral (309 ms, P < 0.005) or a happy (317 ms, P < 0.05) LVF face.

ACC and amygdala activations

Contrasts between the fearful and neutral faces calculated from

Discussion

The present study demonstrates that the ACC–amygdala regions are involved in the rapid processing of unattended fearful facial expressions. We found significant activations within the ACC and right amygdala at 100 ms that were stronger in response to the task-irrelevant fearful, relative to the neutral, faces. The dorsal ACC showed increased activity in response to the fearful relative to the neutral faces, while the ventral ACC showed decreased activity in this comparison. Research has

Conclusions

The present study provides novel timing information on early brain activations in the amygdala, ACC, and fusiform regions, adding to our knowledge of implicit processing of human facial emotions. The sensitivity to task-irrelevant fearful emotions suggests that the unattended information operates at a level where potential threat is automatically processed. The early timing of amygdala–ACC activations (at 100 ms) suggests a specialized frontal–limbic network that could facilitate fast reaction

Acknowledgments

This work is supported by the Canadian Institutes of Health Research grants to M.J.T. (MOP-81161) and Y.H. (CDG-87793) and the Ontario Student Opportunity Trust Fund—Hospital for Sick Children Foundation Student Scholarship Program to Y.H.

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Unattended emotional faces elicit early lateralized amygdala–frontal and fusiform activations

Abstract

Section snippets

Subjects

Task

Reaction times

ACC and amygdala activations

Discussion

Conclusions

Acknowledgments

Cogn. Brain Res.

Cortex

Neuron

Trends Cogn. Sci.

NeuroImage

Clin. Neurophysiol.

Brain Res.

Neuropsychologia

NeuroImage

Cogn. Brain Res.

Trends Neurosci.

NeuroImage

NeuroImage

NeuroImage

Curr. Biol.

Curr. Opin. Neurobiol.

Med. Image Anal.

NeuroImage

Neuropsychologia

Amygdala–frontal connectivity during emotion regulation

Soc. Cogn. Affect. Neurosci.

Spatio temporal dynamics of face recognition

Cereb. Cortex

Is the face-sensitive N170 the only ERP not affected by selective attention?

NeuroReport

Spatiotemporal mapping of cortical activity accompanying voluntary movements using an event-related beamforming approach

Hum. Brain Mapp.

Afferent connections of the medial frontal cortex of the rat. II: cortical and subcortical afferents

J. Comp. Neurol.

Reciprocal suppression of regional cerebral blood flow during emotional versus higher cognitive processes: implications for interactions between emotion and cognition

Cognition Emotion

An ERP study on the time course of emotional face processing

NeuroReport

Changes in anterior cingulate and amygdala after cognitive behavior therapy of posttraumatic stress disorder

Psychological Science