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Cited by 235Neural and Behavioral Psychology StudiesNeurotransmitter Receptor Influence on BehaviorAnxiety, Depression, Psychometrics, Treatment, Cognitive Processes

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Distinct Contributions of the Dorsolateral Prefrontal and Orbitofrontal Cortex during Emotion Regulation

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Golkar, Armita, Lonsdorf, Tina B., Olsson, Andreas, Lindstrom, Kara M., Berrebi, Jonathan, Fransson, Peter, Schalling, Martin, Ingvar, Martin, Öhman, Arne·2012·PLoS ONE
DOI 10.1371/journal.pone.0048107PMC PMC3492343
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Abstract

The lateral prefrontal and orbitofrontal cortices have both been implicated in emotion regulation, but their distinct roles in regulation of negative emotion remain poorly understood. To address this issue we enrolled 58 participants in an fMRI study in which participants were instructed to reappraise both negative and neutral stimuli. This design allowed us to separately study activations reflecting cognitive processes associated with reappraisal in general and activations specifically related to reappraisal of negative emotion. Our results confirmed that both the dorsolateral prefrontal cortex (DLPFC) and the lateral orbitofrontal cortex (OFC) contribute to emotion regulation through reappraisal. However, activity in the DLPFC was related to reappraisal independently of whether negative or neutral stimuli were reappraised, whereas the lateral OFC was uniquely related to reappraisal of negative stimuli. We suggest that relative to the lateral OFC, the DLPFC serves a more general role in emotion regulation, perhaps by reflecting the cognitive demand that is inherent to the regulation task.

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Figure 1 Experimental procedure. Each trial began with an initial 2 sec instruction to either “Attend” or “Reappraise” which was followed by a 5 sec presentation of a negative or a neutral picture. During attend trials, participants were instructed to attend to the picture without trying to alter any ongoing feelings and on reappraise trials they were instructed to neutralize their feelings to the picture. After each picture viewing phase, participants indicated their current level of discomfort on a scale from 1 to 7 (1 = minimal or no discomfort, 7 = maximum discomfort). Each trial ended with a fixation cross jittered between trials with a duration of 3–5 seconds.
Figure 1 Experimental procedure. Each trial began with an initial 2 sec instruction to either “Attend” or “Reappraise” which was followed by a 5 sec presentation of a negative or a neutral picture. During attend trials, participants were instructed to attend to the picture without trying to alter any ongoing feelings and on reappraise trials they were instructed to neutralize their feelings to the picture. After each picture viewing phase, participants indicated their current level of discomfort on a scale from 1 to 7 (1 = minimal or no discomfort, 7 = maximum discomfort). Each trial ended with a fixation cross jittered between trials with a duration of 3–5 seconds.CC BY · PubMed Central
Figure 2 Behavioral results. Discomfort ratings were significantly lower during A. Reappraise negative vs. Attend negative trials and during Reappraise neutral vs. Attend neutral trials. B. Successful emotion regulation as revealed by significantly lower subjective ratings of discomfort during Reappraise negative trials compared to Attend negative trials expressed as difference scores from neutral trials. Errors bars represent SEM. *** = p<.001.
Figure 2 Behavioral results. Discomfort ratings were significantly lower during A. Reappraise negative vs. Attend negative trials and during Reappraise neutral vs. Attend neutral trials. B. Successful emotion regulation as revealed by significantly lower subjective ratings of discomfort during Reappraise negative trials compared to Attend negative trials expressed as difference scores from neutral trials. Errors bars represent SEM. *** = p<.001.CC BY · PubMed Central
Figure 3 Statistical parametric maps showing activations during the main effect of instruction and the Instruction× Valence interaction (A). Activation in the right dorsolateral prefrontal cortex (DLPFC) during the main effect of instruction across stimulus valence in Reappraise (negative + neutral) > Attend (negative + neutral). Significant activations are displayed overlaid on the DLPFC region-of-interest (ROI) image (shown in blue) in sagittal (upper left), coronal (upper right) and axial (lower left) view, respectively and the (B) corresponding contrast estimates for the right and left DLPFC and lateral OFC at peak activation coordinates [right doroslateral PFC: x = 39, y = 24, z = 36; left DLPFC: right OFC; x = 26, y = 46, z = −13; left OFC: x = −36, y = 46, z = −12]. Note that the activations were not significant in the lateral OFC. (C) Activation in the right orbitofrontal cortex (OFC) and the right DLPFC during the Instruction × Valence interaction contrast Reappraise (negative - neutral) > Attend (negative - neutral). Significant activations are displayed overlaid on the DLPFC ROI (shown in blue) and the lateral OFC ROI (shown in green) in sagittal (upper left panel), coronal (upper right panel) and axial (lower left panel) view, and the (D) corresponding contrast estimates during the main effect of instruction and the Instruction × Valence interaction contrasts for the right and left DLPFC and lateral OFC at peak activation coordinates [right DLPFC: x = 46, y = 21, z = 44; left DLPFC; x = −39, y = 24, z = 32; right OFC; x = 42, y = 50, z = −10; left OFC: x = −38, y = 60, z = −4]. All activations were thresholded at p<.05 (FWE) and were based on the DLPFC and lateral OFC ROIs. * = p<.05 (FWE). Error bars represent standard error of the mean.
Figure 3 Statistical parametric maps showing activations during the main effect of instruction and the Instruction× Valence interaction (A). Activation in the right dorsolateral prefrontal cortex (DLPFC) during the main effect of instruction across stimulus valence in Reappraise (negative + neutral) > Attend (negative + neutral). Significant activations are displayed overlaid on the DLPFC region-of-interest (ROI) image (shown in blue) in sagittal (upper left), coronal (upper right) and axial (lower left) view, respectively and the (B) corresponding contrast estimates for the right and left DLPFC and lateral OFC at peak activation coordinates [right doroslateral PFC: x = 39, y = 24, z = 36; left DLPFC: right OFC; x = 26, y = 46, z = −13; left OFC: x = −36, y = 46, z = −12]. Note that the activations were not significant in the lateral OFC. (C) Activation in the right orbitofrontal cortex (OFC) and the right DLPFC during the Instruction × Valence interaction contrast Reappraise (negative - neutral) > Attend (negative - neutral). Significant activations are displayed overlaid on the DLPFC ROI (shown in blue) and the lateral OFC ROI (shown in green) in sagittal (upper left panel), coronal (upper right panel) and axial (lower left panel) view, and the (D) corresponding contrast estimates during the main effect of instruction and the Instruction × Valence interaction contrasts for the right and left DLPFC and lateral OFC at peak activation coordinates [right DLPFC: x = 46, y = 21, z = 44; left DLPFC; x = −39, y = 24, z = 32; right OFC; x = 42, y = 50, z = −10; left OFC: x = −38, y = 60, z = −4]. All activations were thresholded at p<.05 (FWE) and were based on the DLPFC and lateral OFC ROIs. * = p<.05 (FWE). Error bars represent standard error of the mean.CC BY · PubMed Central
Figure 4 Statistical parametric maps showing activations during reappraisal of negative and neutral stimuli. (A) Activation in the right dorsolateral prefrontal cortex (DLPFC) and the lateral orbitofrontal cortex (OFC) in the Reappraise negative > Attend negative and (B) in the right DLPFC during Reappraise neutral > Attend neutral, and (C) overlapping activations in the right DLPFC in the conjunction analysis of the common effect of Reappraise negative > Attend negative and Reappraise neutral > Attend neutral. Significant activations are displayed overlaid on the DLPFC region-of-interest (ROI) image (shown in blue) and the lateral OFC ROI (shown in green) in sagittal view. (D) Contrast estimates extracted for the right DLPFC and the right lateral OFC during the Reappraise negative > Attend negative contrast [DLPFC: x = 42, y = 24, z = 39; lateral OFC: x = 42, y = 45, z = −9] and the Reappraise neutral > Attend neutral contrast [right DLPFC: x = 33, y = 43, z = 30; right lateral OFC x = 25, y = 36, z = −8]. Note that the activations were not significant for the lateral OFC in Reappraise neutral > Attend neutral or in the conjunction analysis. Activations were thresholded at p<.001 (uncorrected) for illustrative purposes and were based on the DLPFC and lateral OFC ROIs. * = p<.05 (FWE). * = p<.05 (FWE). Error bars represent standard error of the mean.
Figure 4 Statistical parametric maps showing activations during reappraisal of negative and neutral stimuli. (A) Activation in the right dorsolateral prefrontal cortex (DLPFC) and the lateral orbitofrontal cortex (OFC) in the Reappraise negative > Attend negative and (B) in the right DLPFC during Reappraise neutral > Attend neutral, and (C) overlapping activations in the right DLPFC in the conjunction analysis of the common effect of Reappraise negative > Attend negative and Reappraise neutral > Attend neutral. Significant activations are displayed overlaid on the DLPFC region-of-interest (ROI) image (shown in blue) and the lateral OFC ROI (shown in green) in sagittal view. (D) Contrast estimates extracted for the right DLPFC and the right lateral OFC during the Reappraise negative > Attend negative contrast [DLPFC: x = 42, y = 24, z = 39; lateral OFC: x = 42, y = 45, z = −9] and the Reappraise neutral > Attend neutral contrast [right DLPFC: x = 33, y = 43, z = 30; right lateral OFC x = 25, y = 36, z = −8]. Note that the activations were not significant for the lateral OFC in Reappraise neutral > Attend neutral or in the conjunction analysis. Activations were thresholded at p<.001 (uncorrected) for illustrative purposes and were based on the DLPFC and lateral OFC ROIs. * = p<.05 (FWE). * = p<.05 (FWE). Error bars represent standard error of the mean.CC BY · PubMed Central

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Metadata

Authors
Golkar, A., Lonsdorf, T. B., Olsson, A., Lindstrom, K. M., Berrebi, J., Fransson, P., Schalling, M., Ingvar, M., & Öhman, A.
Affiliations
Karolinska Institutet (SE)
Corresponding author
Golkar, Armita
ORCID
Venue
PLoS ONE
Publisher
Public Library of Science (PLoS)
Published
2012-11-07
Volume
7
Issue
11
Pages
e48107
ISSN
1932-6203 (ISSN-L)
DOI
10.1371/journal.pone.0048107
PMC
PMC3492343
OpenAlex
W2076380444
Cited by
235
References
47
Citations by year
2026: 17 · 2025: 23 · 2024: 19 · 2023: 18 · 2022: 20 · 2021: 26 · 2020: 14 · 2019: 20 · 2018: 16 · 2017: 15 · 2016: 7 · 2015: 16 · 2014: 14 · 2013: 9
FWCI
6.39
Type
journal article
Language
en
Open access
Licence
Locations
  • PLoS ONE (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • RePEc: Research Papers in Economics (submittedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • Figshare (submittedVersion, cc-by)
  • PUB – Publications at Bielefeld University (Bielefeld University) (submittedVersion)
Funders
  • Stiftelsen för Strategisk Forskning
  • VINNOVA
  • Vetenskapsrådet
  • National Institute of Mental Health
Topics
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
  • Social Sciences › Psychology › Experimental and Cognitive Psychology › Anxiety, Depression, Psychometrics, Treatment, Cognitive Processes
Keywords
emotion regulation, cognitive reappraisal, dorsolateral prefrontal cortex, orbitofrontal cortex, negative emotions, cognitive demand
MeSH terms
Adult, Amygdala, Brain Mapping, Emotions, Female, Humans, Magnetic Resonance Imaging, Male, Photic Stimulation, Prefrontal Cortex, Young Adult

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