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Cited by 2,205Face Recognition and PerceptionNeural and Behavioral Psychology StudiesMemory and Neural Mechanisms

Masked Presentations of Emotional Facial Expressions Modulate Amygdala Activity without Explicit Knowledge

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Whalen, Paul J., Rauch, Scott L., Etcoff, Nancy L., McInerney, Sean C., Lee, Michael B., Jenike, Michael A.·1998·The Journal of Neuroscience
DOI 10.1523/jneurosci.18-01-00411.1998PMC PMC6793390
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Abstract

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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Crossref · 10.1523/jneurosci.18-01-00411.1998

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  • A range of studies have demonstrated that the amygdala rapidly habituates to repeated presentations of emotional faces and pictures.

    “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

    The fMRI data report that amygdala signal increases to masked fearful faces were attenuated to baseline with subsequent presentation epochs, supporting habituation to repeated emotional faces. The ‘Direction of signal changes in the amygdala’ section says the response to happy faces persisted across all epochs, so the finding does not apply to emotional faces generally. The study’s 28-second epochs also do not establish precisely how rapidly habituation occurred. (LLM, conf=0.88)

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  • 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.

    “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

    The fMRI data section reports that amygdala responses to repeated masked fearful faces attenuated to baseline. But responses to happy faces persisted, and the paper does not establish that habituation is particularly pronounced for emotional stimuli compared with other stimuli. The claim generalizes beyond the finding reported here. (LLM, conf=0.88)

    Experimental — accuracy not yet measured

  • Anger and fear are amygdala-mediated emotions and behaviors that concur with sympathetic arousal in the need of prefrontal control when inhibition is desired.

    “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

    The 'Direction of signal changes in the amygdala' section reports increased amygdala activity in response to masked fearful faces and discusses angry faces as threat cues. The 'Significance of SI activation' section links arousal-related responses chiefly to the sublenticular substantia innominata, not specifically to sympathetic arousal. Neither passage establishes that anger and fear require prefrontal control when inhibition is desired; page numbers are unavailable in our copy. (LLM, conf=0.87)

    Experimental — accuracy not yet measured

  • Neuronal activity associated with threat- or fear-related stimuli is obligatory.

    “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 healthy people, threat-related social signals such as fearful and angry faces increase amygdala activity.

    “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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Research works printed but not linked: 1

  1. Halgren E (1992) Emotional neurophysiology of the human amygdala within the context of human cognition. In: The amygdala: neurobiolog- ical aspects of emotion, memory, and mental dysf unction (Aggleton JP, ed), pp 191-228. New York: Wiley.

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Authors
Whalen, P. J., Rauch, S. L., Etcoff, N. L., McInerney, S. C., Lee, M. B., & Jenike, M. A.
Affiliations
Harvard University (US)
ORCID
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
DOI
10.1523/jneurosci.18-01-00411.1998
PMC
PMC6793390
OpenAlex
W2164058388
Cited by
2,205
References
73
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
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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