Cited by 957Neural and Behavioral Psychology StudiesNeurotransmitter Receptor Influence on BehaviorAnxiety, Depression, Psychometrics, Treatment, Cognitive Processes

The DOI matches its Crossref record; 107 of the 107 references it cites were found in a registry or an index; 1 of the 47 sources its claims cite were checked for support.

Neural network of cognitive emotion regulation—an ALE meta-analysis and MACM analysis

Open access

Abstract

Cognitive regulation of emotions is a fundamental prerequisite for intact social functioning which impacts on both well being and psychopathology. The neural underpinnings of this process have been studied intensively in recent years, without, however, a general consensus. We here quantitatively summarize the published literature on cognitive emotion regulation using activation likelihood estimation in fMRI and PET (23 studies/479 subjects). In addition, we assessed the particular functional contribution of identified regions and their interactions using quantitative functional inference and meta-analytic connectivity modeling, respectively. In doing so, we developed a model for the core brain network involved in emotion regulation of emotional reactivity. According to this, the superior temporal gyrus, angular gyrus and (pre) supplementary motor area should be involved in execution of regulation initiated by frontal areas. The dorsolateral prefrontal cortex may be related to regulation of cognitive processes such as attention, while the ventrolateral prefrontal cortex may not necessarily reflect the regulatory process per se, but signals salience and therefore the need to regulate. We also identified a cluster in the anterior middle cingulate cortex as a region, which is anatomically and functionally in an ideal position to influence behavior and subcortical structures related to affect generation. Hence this area may play a central, integrative role in emotion regulation. By focusing on regions commonly active across multiple studies, this proposed model should provide important a priori information for the assessment of dysregulated emotion regulation in psychiatric disorders.

Overview

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TL;DR

This paper quantitatively integrates fMRI/PET studies of conscious cognitive emotion regulation using activation likelihood estimation, meta-analytic connectivity modeling, and BrainMap functional decoding. It proposes a three-stage network model in which VLPFC supports appraisal/salience detection, DLPFC initiates regulation, and STG, angular gyrus, and pre-SMA execute regulation, with aMCC as a central integrator.

Key findings

  • Across 23 studies, 47 experiments, 479 subjects, and 505 foci, the ALE meta-analysis found eight significant clusters: bilateral inferior frontal gyrus/VLPFC extending into anterior insula, a large SMA/pre-SMA cluster extending into aMCC, bilateral precentral/DLPFC clusters, left middle temporal cortex, and bilateral angular gyri.
  • MACM showed distinct co-activation patterns for these regions: the IFG/VLPFC seed co-activated with insula, middle frontal, precentral, aMCC/SMA, parietal, thalamus, temporal, striatal, and amygdala regions; DLPFC co-activated with aMCC, angular gyri, insula, and left middle frontal gyrus; aMCC and SMA seeds showed broad sensorimotor, insular, parietal, thalamic, and striatal co-activation; angular gyrus co-activated with parietal, cingulate, left IFG, and left SMA; STG co-activated with left IFG/precentral, temporal, SMA, parietal, insular, striatal, and thalamic regions.
  • Functional decoding linked DLPFC to working memory, reasoning, social cognition, and action inhibition rather than emotion processing; VLPFC to language, social cognition, emotion, and action inhibition; aMCC to language, working/explicit memory, and action inhibition; SMA to language and memory; STG to language, social cognition, and audition; and angular gyrus to social cognition, imagery, and deception tasks.
  • The authors propose a three-stage model: VLPFC as a hub for affective evaluation and salience detection, DLPFC for initiating regulation via “cold” cognitive control, STG/angular gyrus/pre-SMA for executing regulation, and aMCC as a mediator integrating these steps.

Methods

  • ALE meta-analysis of fMRI and PET studies selected from BrainMap and manual PubMed/Google Scholar searches; inclusion required whole-brain coverage, standard-space group analysis, no pharmacological treatment or mental/neurological disorder, and antecedent-focused, conscious, cognitive regulation strategies. The final sample comprised 23 studies, 47 experiments, 479 subjects, and 505 foci; Talairach coordinates were converted to MNI.
  • ALE modeled activation foci as Gaussian probability distributions weighted by sample size, with a family-wise error-corrected threshold of p = 0.05.
  • MACM was performed on six volumes of interest from the ALE clusters using BrainMap co-activation searches; functional decoding used BrainMap Behavioral Domain and Paradigm Class metadata with forward and reverse inference, binomial and chi-square tests, and Bonferroni correction at p < .05.

Limitations

  • Stated by the authors: five included studies did not report participants’ mental health status or assessment methods, describing them only as “normal”; a sensitivity analysis excluding these studies did not change the general activation pattern.
  • Stated by the authors: the data cannot establish causal relationships within the network, and the study was not designed to test mediation versus direct-pathway hypotheses.
  • Evident from the text: the meta-analysis aggregates published coordinates and cannot resolve causality; inclusion was restricted to conscious, antecedent-focused, functional regulation strategies in fMRI/PET with whole-brain group analyses, so findings may not generalize to automatic, response-focused, dysfunctional, or clinical populations; functional decoding depends on BrainMap metadata and reverse inference.

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Integrity signals

Registry

Crossref · 10.1016/j.neuroimage.2013.11.001

Cites

107 of 107 references verified0 citation errors · 0 not checkable

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Claims the paper makes

31 Own interpretation · 29 Not checked yet · 23 Own result · 5 Own method · 1 Partly supported · 1 No basis given · accuracy not yet measured

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  • The quote only partly states this claim. 2
  • It may state two separate claims as one. 30
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39 of 39
  • The authors state this as an assumption.

    Subcortical brain areas are involved in signaling affective arousal or excitation.

    “It can therefore be assumed that these brain areas will be involved in signaling affective arousal or excitation (Wager et al., 2008).”
  • The authors state this as an assumption.

    Subcortical areas project affective arousal to the VLPFC via the anterior insula and the aMCC.

    “We assume that subcortical areas project affective arousal to the VLPFC (via the anterior insula and the aMCC).”
  • The authors state this as an assumption.

    Regulation of emotional reactivity is mediated by an influence of cortical networks on subcortical affect generation structures.

    “Our line of argument implicitly assumes regulation of emotional reactivity to be mediated by an influence of (cortical) networks on subcortical affect generation structures.”
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Citations

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Research works printed but not linked: 1

  1. Haber, 2009, Chapter 1 — anatomy and connectivity of the reward circuit, 1

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Metadata

Authors
Kohn, N., Eickhoff, S. B., Scheller, M., Laird, A. R., Fox, P. T., & Habel, U.
Affiliations
  • Jülich Aachen Research Alliance (DE)
  • Forschungszentrum Jülich (DE)
  • Florida International University (US)
  • The University of Texas at San Antonio Health Science Center (US)
Corresponding author
Kohn, N.
Venue
NeuroImage
Publisher
Elsevier BV
Published
2014-02
Volume
87
Pages
345-355
ISSN
1053-8119 (ISSN-L)
OpenAlex
W2088242772
Cited by
956
References
106
Citations by year
2026: 65 · 2025: 83 · 2024: 99 · 2023: 90 · 2022: 102 · 2021: 106 · 2020: 80 · 2019: 76 · 2018: 78 · 2017: 50 · 2016: 52 · 2015: 51 · 2014: 21
FWCI
3.57
Type
journal article
Language
en
Update notices
erratum (2015-05-01)
Open access
Locations
  • NeuroImage (publishedVersion)
  • PubMed (publishedVersion)
  • Europe PMC (PubMed Central) (acceptedVersion)
  • PubMed Central (acceptedVersion)
  • RWTH Publications (RWTH Aachen) (submittedVersion)
Funders
  • Faculty of Medicine, RWTH Aachen University (138/09)
  • German Research Foundation
  • IZKF Aachen
  • National Institute of Mental Health (R01-MH074457)
  • Helmholtz Alliance on Systems Biology
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
cognitive emotion regulation, neural network model, emotional reactivity, dorsolateral prefrontal cortex, ventrolateral prefrontal cortex, supplementary motor area, angular gyrus, superior temporal gyrus, meta-analytic connectivity modeling, activation likelihood estimation, mental illness
MeSH terms
Brain, Cognition, Emotions, Female, Humans, Male, Nerve Net, Likelihood Functions

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