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Masked Presentations of Emotional Facial Expressions Modulate Amygdala Activity without Explicit Knowledge
Open accessAbstract
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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“In particular, a range of studies have demonstrated that the amygdala rapidly habituates to repeated presentations of emotional faces (Breiter et al., 1996 ;Whalen et al., 1998 ;Wright et al., 2001) and pictures (Fischer et al., 2000 ;Irwin et al., 1996).”
From Short-term serotonergic but not noradrenergic antidepressant administration reduces attentional vigilance to threat in healthy volunteers (2009) · cites this paper as Whalen et al., 1998
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“Consistent with this, it is well established that the habituation of neural responses to repeated exposure to stimuli is particularly pronounced in response to stimuli with an emotional valence.”
From Short-term serotonergic but not noradrenergic antidepressant administration reduces attentional vigilance to threat in healthy volunteers (2009) · cites this paper as Whalen et al., 1998
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“Anger as well as fear are accepted to be amygdala-mediated emotions and behaviors that concur with sympathetic arousal in the need of prefrontal control when inhibition is desired (e.g., Morris et al., 1998; Whalen et al., 1998; Izdebski, 2008; see Kreibig, 2010 for a review on autonomic responses to emotions).”
From Voice Stress Analysis: A New Framework for Voice and Effort in Human Performance (2018) · cites this paper as Whalen et al., 1998
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“Numerous studies have demonstrated that this is also reflected in attentional control and suggested that neuronal activity associated with threat- or fear-related stimuli is obligatory (Pessoa, McKenna, Gutierrez, & Ungerleider, 2002; Vuilleumier, Armony, Driver, & Dolan, 2001; Whalen et al., 1998).”
From Selection history: How reward modulates selectivity of visual attention. (2018) · cites this paper as Whalen et al., 1998
In the citing paper
“In normal individuals, exposure to threat-related social signals such as fearful and angry facial expressions increases amygdala activity (Whalen et al. 1998; Zald, 2003); this effect is heightened in individuals with social anxiety (Phan et al. 2006).”
From Effects of MDMA on sociability and neural response to social threat and social reward (2009) · cites this paper as Whalen et al. 1998
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“show the amygdala to be particularly important in socioemotional processing, especially processing of threat-related social information (Whalen et al. 1998; Zald 2003).”
From Effects of MDMA on sociability and neural response to social threat and social reward (2009) · cites this paper as Whalen et al. 1998
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“amygdala activation to fearful faces can occur in the absence of attention, potentially when the fearful faces are masked and not consciously detected94”
From Neural Substrates of Childhood Anxiety Disorders (2012) · cites this paper as [94]
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Metadata
- Authors
- Whalen, P. J., Rauch, S. L., Etcoff, N. L., McInerney, S. C., Lee, M. B., & Jenike, M. A.
- Affiliations
- Harvard University (US)
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 1998-01-01
- Volume
- 18
- Issue
- 1
- Pages
- 411-418
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC6793390
- OpenAlex
- W2164058388
- Cited by
- 2,205
- References
- 72
- Citations by year
- 2026: 7 · 2025: 30 · 2024: 24 · 2023: 31 · 2022: 28 · 2021: 45 · 2020: 35 · 2019: 52 · 2018: 66 · 2017: 72 · 2016: 78 · 2015: 81 · 2014: 99 · 2013: 126 · 2012: 121
- FWCI
- 34.14
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Alliance for Research on Schizophrenia and Depression
- National Institutes of Health (5k20mh001215-05)
- National Institute of Mental Health (MH 16259, MH01215, T32MH016259)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Face Recognition and Perception
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Keywords
- amygdala, emotional facial expressions, masked stimuli, backward masking, fear, happiness, emotional valence, unconscious processes, substantia innominata, emotional salience, face perception
- MeSH terms
- Adult, Amygdala, Awareness, Facial Expression, Fear, Happiness, Heart Rate, Humans, Functional Laterality, Magnetic Resonance Imaging, Male, Substantia Innominata
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