Elsevier

NeuroImage

Volume 21, Issue 4, April 2004, Pages 1215-1223
NeuroImage

Activation of the amygdala and anterior cingulate during nonconscious processing of sad versus happy faces

https://doi.org/10.1016/j.neuroimage.2003.12.033Get rights and content

Abstract

Previous functional neuroimaging studies have demonstrated that the amygdala activates in response to fearful faces presented below the threshold of conscious visual perception. Using a backward masking procedure similar to that of previous studies, we used functional magnetic resonance imaging (fMRI) to study the amygdala and anterior cingulate gyrus during preattentive presentations of sad and happy facial affect. Twelve healthy adult females underwent blood oxygen level dependent (BOLD) fMRI while viewing sad and happy faces, each presented for 20 ms and “masked” immediately by a neutral face for 100 ms. Masked happy faces were associated with significant bilateral activation within the anterior cingulate gyrus and amygdala, whereas masked sadness yielded only limited activation within the left anterior cingulate gyrus. In a direct comparison, masked happy faces yielded significantly greater activation in the anterior cingulate and amygdala relative to identically masked sad faces. Conjunction analysis showed that masked affect perception, regardless of emotional valence, was associated with greater activation within the left amygdala and left anterior cingulate. Findings suggest that the amygdala and anterior cingulate are important components of a network involved in detecting and discriminating affective information presented below the normal threshold of conscious visual perception.

Section snippets

Subjects

Twelve healthy right-handed female adults, ranging in age from 21 to 28 years (M = 23.7, SD = 2.1), underwent functional magnetic resonance imaging (fMRI) using blood oxygenation level dependent (BOLD) contrast. Participants, recruited from the local community and the staff of McLean Hospital, were without history of psychiatric or neurological illness according to a structured clinical interview, and all had normal or corrected–normal vision. Subjects were naı̈ve to the face stimuli and

Masked happiness

Presentation of happy faces masked by neutral faces yielded significant activation within the left (P < 0.005) and right (P < 0.05) amygdala (see Fig. 3 and Table 1). Several clusters of suprathreshold activation were also observed within the left (P < 0.01) and right (P < 0.01) anterior cingulate gyrus.

Masked sadness

Presentations of masked sad faces were not associated with any suprathreshold clusters of activation within either the left or right amygdala relative to the fixation baseline (see Fig. 3 and

Discussion

Subjects were presented with photographs of happy and sad faces in a manner that minimized or eliminated conscious visual perception of the presented affect. Despite being presented below the threshold of conscious awareness, these “unseen” emotional stimuli yielded specific patterns of activation within the amygdala and anterior cingulate gyrus that differed as a function of the emotional valence of the masked facial expression. Masked happiness was associated with significant bilateral

Conclusion

This is the first fMRI study to use backward masking of facial stimuli to demonstrate differential regional activation associated with nonconscious processing of happy versus sad facial affect. While the cingulate gyrus demonstrated relative consistency across affect conditions, the amygdala showed clearly distinct patterns of activation depending on whether the nonconscious stimuli depicted happy or sad expressions. These findings suggest a role for the amygdala in processing nonconscious

Acknowledgements

This material has been reviewed by the Walter Reed Army Institute of Research. There is no objection to its presentation and/or publication. The opinions or assertions contained herein are the private views of the authors, and are not to be construed as official, or as reflecting true views of the Department of the Army or the Department of Defense. This work was supported by a grant from the National Institute of Child Health and Human Development (NICHD) to William D. Killgore, PhD, NIH grant

References (44)

  • M.L. Phillips et al.

    Investigation of facial recognition memory and happy and sad facial expression perception: an fMRI study

    Psychiatry Res.

    (1998)
  • J.J. Soares et al.

    Preattentive processing, preparedness and phobias: effects of instruction on conditioned electrodermal responses to masked and non-masked fear-relevant stimuli

    Behav. Res. Ther.

    (1993)
  • N. Tzourio-Mazoyer et al.

    Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain

    NeuroImage

    (2002)
  • C. Barr-Zisowitz

    “Sadness”—is there such a thing?

  • R.J. Blair et al.

    Dissociable neural responses to facial expressions of sadness and anger

    Brain

    (1999)
  • J.C. Borod et al.

    Neuropsychological aspects of facial asymmetry during emotional expression: a review of the normal adult literature

    Neuropsychol. Rev.

    (1997)
  • C.S. Carter et al.

    Anterior cingulate cortex activity and impaired self-monitoring of performance in patients with schizophrenia: an event-related fMRI study

    Am. J. Psychiatry

    (2001)
  • B. de Gelder et al.

    Non-conscious recognition of affect in the absence of striate cortex

    NeuroReport

    (1999)
  • O. Devinsky et al.

    Contributions of anterior cingulate cortex to behaviour

    Brain

    (1995)
  • U. Dimberg et al.

    Unconscious facial reactions to emotional facial expressions

    Psychol. Sci.

    (2000)
  • N. Eisenberg et al.

    Relation of sympathy and personal distress to prosocial behavior: a multimethod study

    J. Pers. Soc. Psychol.

    (1989)
  • N. Eisenberg et al.

    Sympathy and personal distress: development, gender differences, and interrelations of indexes

    New Dir. Child Dev.

    (1989)
  • Cited by (0)

    View full text