Neural substrates for voluntary suppression of negative affect: A functional magnetic resonance imaging study

Successful control of affect partly depends on the capacity to modulate negative emotional responses through the use of cognitive strategies. Although the capacity to regulate emotions is critical to mental well-being, its neural substrates remain unclear. We used functional magnetic resonance imagi...

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Published inBiological psychiatry (1969) Vol. 57; no. 3; pp. 210 - 219
Main Authors Phan, K. Luan, Fitzgerald, Daniel A., Nathan, Pradeep J., Moore, Gregory J., Uhde, Thomas W., Tancer, Manuel E.
Format Journal Article
LanguageEnglish
Published New York, NY Elsevier Inc 01.02.2005
Elsevier Science
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Abstract Successful control of affect partly depends on the capacity to modulate negative emotional responses through the use of cognitive strategies. Although the capacity to regulate emotions is critical to mental well-being, its neural substrates remain unclear. We used functional magnetic resonance imaging to ascertain brain regions involved in the voluntary regulation of emotion and whether dynamic changes in negative emotional experience can modulate their activation. Fourteen healthy subjects were scanned while they either maintained the negative affect evoked by highly arousing and aversive pictures (e.g., experience naturally) or suppressed their affect using cognitive reappraisal. In addition to a condition-based analysis, online subjective ratings of intensity of negative affect were used as covariates of brain activity. Inhibition of negative affect was associated with activation of dorsal anterior cingulate, dorsal medial prefrontal, and lateral prefrontal cortices, and attenuation of brain activity within limbic regions (e.g., nucleus accumbens/extended amygdala). Furthermore, activity within dorsal anterior cingulate was inversely related to intensity of negative affect, whereas activation of the amygdala was positively covaried with increasing negative affect. These findings highlight a functional dissociation of corticolimbic brain responses, involving enhanced activation of prefrontal cortex and attenuation of limbic areas, during volitional suppression of negative emotion.
AbstractList Successful control of affect partly depends on the capacity to modulate negative emotional responses through the use of cognitive strategies. Although the capacity to regulate emotions is critical to mental well-being, its neural substrates remain unclear. We used functional magnetic resonance imaging to ascertain brain regions involved in the voluntary regulation of emotion and whether dynamic changes in negative emotional experience can modulate their activation. Fourteen healthy subjects were scanned while they either maintained the negative affect evoked by highly arousing and aversive pictures (e.g., experience naturally) or suppressed their affect using cognitive reappraisal. In addition to a condition-based analysis, online subjective ratings of intensity of negative affect were used as covariates of brain activity. Inhibition of negative affect was associated with activation of dorsal anterior cingulate, dorsal medial prefrontal, and lateral prefrontal cortices, and attenuation of brain activity within limbic regions (e.g., nucleus accumbens/extended amygdala). Furthermore, activity within dorsal anterior cingulate was inversely related to intensity of negative affect, whereas activation of the amygdala was positively covaried with increasing negative affect. These findings highlight a functional dissociation of corticolimbic brain responses, involving enhanced activation of prefrontal cortex and attenuation of limbic areas, during volitional suppression of negative emotion.
Successful control of affect partly depends on the capacity to modulate negative emotional responses through the use of cognitive strategies. Although the capacity to regulate emotions is critical to mental well-being, its neural substrates remain unclear.BACKGROUNDSuccessful control of affect partly depends on the capacity to modulate negative emotional responses through the use of cognitive strategies. Although the capacity to regulate emotions is critical to mental well-being, its neural substrates remain unclear.We used functional magnetic resonance imaging to ascertain brain regions involved in the voluntary regulation of emotion and whether dynamic changes in negative emotional experience can modulate their activation. Fourteen healthy subjects were scanned while they either maintained the negative affect evoked by highly arousing and aversive pictures (e.g., experience naturally) or suppressed their affect using cognitive reappraisal. In addition to a condition-based analysis, online subjective ratings of intensity of negative affect were used as covariates of brain activity.METHODSWe used functional magnetic resonance imaging to ascertain brain regions involved in the voluntary regulation of emotion and whether dynamic changes in negative emotional experience can modulate their activation. Fourteen healthy subjects were scanned while they either maintained the negative affect evoked by highly arousing and aversive pictures (e.g., experience naturally) or suppressed their affect using cognitive reappraisal. In addition to a condition-based analysis, online subjective ratings of intensity of negative affect were used as covariates of brain activity.Inhibition of negative affect was associated with activation of dorsal anterior cingulate, dorsal medial prefrontal, and lateral prefrontal cortices, and attenuation of brain activity within limbic regions (e.g., nucleus accumbens/extended amygdala). Furthermore, activity within dorsal anterior cingulate was inversely related to intensity of negative affect, whereas activation of the amygdala was positively covaried with increasing negative affect.RESULTSInhibition of negative affect was associated with activation of dorsal anterior cingulate, dorsal medial prefrontal, and lateral prefrontal cortices, and attenuation of brain activity within limbic regions (e.g., nucleus accumbens/extended amygdala). Furthermore, activity within dorsal anterior cingulate was inversely related to intensity of negative affect, whereas activation of the amygdala was positively covaried with increasing negative affect.These findings highlight a functional dissociation of corticolimbic brain responses, involving enhanced activation of prefrontal cortex and attenuation of limbic areas, during volitional suppression of negative emotion.CONCLUSIONSThese findings highlight a functional dissociation of corticolimbic brain responses, involving enhanced activation of prefrontal cortex and attenuation of limbic areas, during volitional suppression of negative emotion.
Author Fitzgerald, Daniel A.
Tancer, Manuel E.
Moore, Gregory J.
Nathan, Pradeep J.
Phan, K. Luan
Uhde, Thomas W.
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  givenname: K. Luan
  surname: Phan
  fullname: Phan, K. Luan
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– sequence: 2
  givenname: Daniel A.
  surname: Fitzgerald
  fullname: Fitzgerald, Daniel A.
  organization: Department of Psychiatry, University of Chicago, Chicago, Illinois
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  fullname: Nathan, Pradeep J.
  organization: Brain Sciences Institute, Swinburne University, Hawthorn, Australia
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  organization: Department of Psychiatry, Penn State University College of Medicine, Hershey, Pennsylvania
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  givenname: Thomas W.
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  fullname: Uhde, Thomas W.
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  fullname: Tancer, Manuel E.
  organization: Department of Psychiatry and Behavioral Neurosciences, Wayne State University School of Medicine, Detroit, Michigan
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https://www.ncbi.nlm.nih.gov/pubmed/15691521$$D View this record in MEDLINE/PubMed
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Issue 3
Keywords emotion regulation
fMRI
emotion
Amygdala
cognition
prefrontal cortex
Human
Affect affectivity
Healthy subject
Voluntary control
Central nervous system
Basal ganglion
Functional analysis
Emotion emotionality
Prefrontal cortex
Experimental study
Nuclear magnetic resonance imaging
Encephalon
Acquisition process
Acquired experience
Language English
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Snippet Successful control of affect partly depends on the capacity to modulate negative emotional responses through the use of cognitive strategies. Although the...
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SubjectTerms Adult
Affectivity. Emotion
Amygdala
Biological and medical sciences
Brain - blood supply
Brain - physiology
Brain Mapping
cognition
emotion
emotion regulation
Emotions - physiology
Female
fMRI
Fundamental and applied biological sciences. Psychology
Humans
Image Processing, Computer-Assisted - methods
Magnetic Resonance Imaging
Male
Neural Inhibition - physiology
Oxygen - blood
Personality. Affectivity
Photic Stimulation - methods
prefrontal cortex
Psychology. Psychoanalysis. Psychiatry
Psychology. Psychophysiology
Title Neural substrates for voluntary suppression of negative affect: A functional magnetic resonance imaging study
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https://dx.doi.org/10.1016/j.biopsych.2004.10.030
https://www.ncbi.nlm.nih.gov/pubmed/15691521
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