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      A face versus non-face context influences amygdala responses to masked fearful eye whites

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          Abstract

          The structure of the mask stimulus is crucial in backward masking studies and we recently demonstrated such an effect when masking faces. Specifically, we showed that activity of the amygdala is increased to fearful facial expressions masked with neutral faces and decreased to fearful expressions masked with a pattern mask—but critically both masked conditions discriminated fearful expressions from happy expressions. Given this finding, we sought to test whether masked fearful eye whites would produce a similar profile of amygdala response in a face vs non-face context. During functional magnetic resonance imaging scanning sessions, 30 participants viewed fearful or happy eye whites masked with either neutral faces or pattern images. Results indicated amygdala activity was increased to fearful vs happy eye whites in the face mask condition, but decreased to fearful vs happy eye whites in the pattern mask condition—effectively replicating and expanding our previous report. Our data support the idea that the amygdala is responsive to fearful eye whites, but that the nature of this activity observed in a backward masking design depends on the mask stimulus.

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          Most cited references18

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          Conscious and unconscious emotional learning in the human amygdala.

          If subjects are shown an angry face as a target visual stimulus for less than forty milliseconds and are then immediately shown an expressionless mask, these subjects report seeing the mask but not the target. However, an aversively conditioned masked target can elicit an emotional response from subjects without being consciously perceived. Here we study the mechanism of this unconsciously mediated emotional learning. We measured neural activity in volunteer subjects who were presented with two angry faces, one of which, through previous classical conditioning, was associated with a burst of white noise. In half of the trials, the subjects' awareness of the angry faces was prevented by backward masking with a neutral face. A significant neural response was elicited in the right, but not left, amygdala to masked presentations of the conditioned angry face. Unmasked presentations of the same face produced enhanced neural activity in the left, but not right, amygdala. Our results indicate that, first, the human amygdala can discriminate between stimuli solely on the basis of their acquired behavioural significance, and second, this response is lateralized according to the subjects' level of awareness of the stimuli.
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            Emotion drives attention: detecting the snake in the grass.

            Participants searched for discrepant fear-relevant pictures (snakes or spiders) in grid-pattern arrays of fear-irrelevant pictures belonging to the same category (flowers or mushrooms) and vice versa. Fear-relevant pictures were found more quickly than fear-irrelevant ones. Fear-relevant, but not fear-irrelevant, search was unaffected by the location of the target in the display and by the number of distractors, which suggests parallel search for fear-relevant targets and serial search for fear-irrelevant targets. Participants specifically fearful of snakes but not spiders (or vice versa) showed facilitated search for the feared objects but did not differ from controls in search for nonfeared fear-relevant or fear-irrelevant, targets. Thus, evolutionary relevant threatening stimuli were effective in capturing attention, and this effect was further facilitated if the stimulus was emotionally provocative.
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              Masked presentations of emotional facial expressions modulate amygdala activity without explicit knowledge.

              Functional magnetic resonance imaging (fMRI) of the human brain was used to study whether the amygdala is activated in response to emotional stimuli, even in the absence of explicit knowledge that such stimuli were presented. Pictures of human faces bearing fearful or happy expressions were presented to 10 normal, healthy subjects by using a backward masking procedure that resulted in 8 of 10 subjects reporting that they had not seen these facial expressions. The backward masking procedure consisted of 33 msec presentations of fearful or happy facial expressions, their offset coincident with the onset of 167 msec presentations of neutral facial expressions. Although subjects reported seeing only neutral faces, blood oxygen level-dependent (BOLD) fMRI signal in the amygdala was significantly higher during viewing of masked fearful faces than during the viewing of masked happy faces. This difference was composed of significant signal increases in the amygdala to masked fearful faces as well as significant signal decreases to masked happy faces, consistent with the notion that the level of amygdala activation is affected differentially by the emotional valence of external stimuli. In addition, these facial expressions activated the sublenticular substantia innominata (SI), where signal increases were observed to both fearful and happy faces--suggesting a spatial dissociation of territories that respond to emotional valence versus salience or arousal value. This study, using fMRI in conjunction with masked stimulus presentations, represents an initial step toward determining the role of the amygdala in nonconscious processing.
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                Author and article information

                Journal
                Soc Cogn Affect Neurosci
                Soc Cogn Affect Neurosci
                scan
                scan
                Social Cognitive and Affective Neuroscience
                Oxford University Press
                1749-5016
                1749-5024
                December 2016
                12 August 2016
                12 August 2016
                : 11
                : 12
                : 1933-1941
                Affiliations
                [1 ]Department of Psychological and Brain Sciences, Dartmouth College, Hanover, NH 03755, USA
                [2 ]Department of Psychology, Princeton University, Princeton, NJ 08544, USA
                [3 ]Department of Psychology, University of Nebraska-Lincoln, Lincoln, NE 68588, USA
                [4 ]Cognitive Science, US Army Natick Soldier Research Development and Engineering Center (NSRDEC), Natick, MA 01760, USA
                [5 ]Department of Psychiatry, University of Wisconsin-Madison School of Medicine and Public Health, Madison, WI 53719, USA,
                [6 ]Behavior Therapy and Psychotherapy Center, University of Vermont, Burlington, VT 05405, USA
                Author notes
                Correspondence should be addressed to Paul J. Whalen, Department of Psychological and Brain Sciences, Dartmouth College, 6207 Moore Hall, Hanover, NH 03755, USA. E-mail: paul.j.whalen@ 123456dartmouth.edu
                Article
                nsw110
                10.1093/scan/nsw110
                5141961
                27521301
                90e88942-9a97-4726-b19b-521bd681e990
                © The Author (2016). Published by Oxford University Press.

                This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License ( http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com

                History
                : 12 March 2016
                : 09 June 2016
                : 03 August 2016
                Page count
                Pages: 9
                Categories
                Original Articles

                Neurosciences
                amygdala,backward masking,eyes,fmri,fear
                Neurosciences
                amygdala, backward masking, eyes, fmri, fear

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