The integration of negative affect, pain and cognitive control in the cingulate cortex

Shackman, Alexander J.; Salomons, Tim V.; Slagter, Heleen A.; Fox, Andrew S.; Winter, Jameel J.; Davidson, Richard J.

doi:10.1038/nrn2994

Cited by 2,082Neural and Behavioral Psychology StudiesNeurotransmitter Receptor Influence on BehaviorMemory and Neural Mechanisms

The integration of negative affect, pain and cognitive control in the cingulate cortex

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Shackman, Alexander J., Salomons, Tim V., Slagter, Heleen A., Fox, Andrew S., Winter, Jameel J., Davidson, Richard J.·2011·Nature Reviews Neuroscience

DOI 10.1038/nrn2994PMC PMC3044650

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Abstract

It has been argued that emotion, pain and cognitive control are functionally segregated in distinct subdivisions of the cingulate cortex. However, recent observations encourage a fundamentally different view. Imaging studies demonstrate that negative affect, pain and cognitive control activate an overlapping region of the dorsal cingulate — the anterior midcingulate cortex (aMCC). Anatomical studies reveal that the aMCC constitutes a hub where information about reinforcers can be linked to motor centres responsible for expressing affect and executing goal-directed behaviour. Computational modelling and other kinds of evidence suggest that this intimacy reflects control processes that are common to all three domains. These observations compel a reconsideration of the dorsal cingulate's contribution to negative affect and pain.

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Brain areas and networks are domain-general, meaning that one brain region or network can be involved in several functions.
“Similarly, brain areas (and sets of brain regions organized into discrete networks) are also domain-general (one to many)-meaning that one brain region/network can be involved in several functions (such as nociception and cognitive control).51,127”
From A new science of emotion: implications for functional neurological disorder (2022) · cites this paper as [127]
The Functional imaging evidence of overlap in aMCC section reports that negative affect, pain, and cognitive control consistently activate the same brain region, supporting the one-region-to-several-functions example. The Limitations of the Available Evidence section says aMCC likely participates in those domains with dissociable networks; it does not establish that the same network serves several functions. Page numbers are unavailable in our copy. (LLM, conf=0.85)
Experimental — accuracy not yet measured
Working memory, emotion, and pain are thought to have somewhat confusable neural correlates, with common activation of regions such as dorsal anterior cingulate cortex (ACC) and anterior insula.
“These domains are excellent candidates for quantitative reverse inference, as they are thought to have somewhat confusable neural correlates, with common activation of regions such as dorsal anterior cingulate cortex (ACC)19 and anterior insula.”
From Large-scale automated synthesis of human functional neuroimaging data. (2011) · cites this paper as [19]
The Functional imaging evidence of overlap in aMCC section reports common anterior midcingulate activation for negative affect, pain, and cognitive control, supporting the cited point about overlapping dorsal cingulate correlates. Its cognitive-control tasks are Stroop, Go/No-Go, and Flanker tasks; it does not establish the same overlap specifically for working memory. The citation is attached to dorsal ACC, not anterior insula. (LLM, conf=0.83)
Experimental — accuracy not yet measured
Working memory, emotion, and pain are excellent candidates for quantitative reverse inference.
“These domains are excellent candidates for quantitative reverse inference, as they are thought to have somewhat confusable neural correlates, with common activation of regions such as dorsal anterior cingulate cortex (ACC)19 and anterior insula.”
From Large-scale automated synthesis of human functional neuroimaging data. (2011) · cites this paper as [19]
The ‘Functional imaging evidence of overlap in aMCC’ section reports overlapping dorsal cingulate activation for negative affect, pain, and cognitive control, supporting the rationale for comparing their neural correlates. Its cognitive-control analysis used tasks such as Stroop and Go/No-Go, not working-memory tasks, so the source does not establish the claimed overlap for working memory specifically. The judgment that these are ‘excellent candidates’ for reverse inference is the citing authors’ framing, not a finding attributed to this source. (LLM, conf=0.84)
Experimental — accuracy not yet measured
The ACC is implicated in a wide variety of cognitive and emotional processes including conflict monitoring, expectancy violation, physical pain and other negative emotions, reactions to being treated unfairly, and social exclusion.
“The ACC is implicated in a wide variety of cognitive and emotional processes including conflict monitoring (Botvinick et al. 2004), expectancy violation (Somerville et al. 2006), physical pain and other negative emotions (Shackman et al. 2011), reactions to being treated unfairly (Sanfey et al. 2003) and social exclusion (Eisenberger et al. 2003).”
From Chronic Childhood Peer Rejection is Associated with Heightened Neural Responses to Social Exclusion During Adolescence (2016) · cites this paper as Shackman et al. 2011
Some processes such as pain and emotion, or motor control and aspects of attention, likely overlap.
“It is, of course, most likely that some processes, such as pain and emotion (Shackman et al., 2011), or motor control and aspects of attention (Paus, 2001) will overlap given their close relationships with one another.”
From The cingulum bundle: Anatomy, function, and dysfunction (2018) · cites this paper as Shackman et al., 2011

Some structures may perform information processing that pertains both to emotional and non-emotional processes.
“Finally, some structures may perform information processing that pertains both to emotional and non-emotional processes (Shackman et al., 2011).”
From Top-Down Dysregulation—From ADHD to Emotional Instability (2016) · cites this paper as Shackman et al., 2011
One view holds that rdACC translates between meaning and action systems, including selecting meaning-guided actions under uncertainty and monitoring action consequences, whereas ventral vmPFC updates representations of the organism's internal state.
“One view is that rdACC is involved in translating between ‘meaning’ and action systems—including selecting meaning-guided actions under conditions of uncertainty [23,24] and monitoring the consequences of actions [25]—whereas ventral vmPFC are primarily involved in updating representations of the internal state of the organism.”
From Ventromedial prefrontal–subcortical systems and the generation of affective meaning (2012) · cites this paper as [23]
The association between positive outcomes and high baseline connectivity between dmPFC and sgACC and low baseline connectivity with striatum may suggest that positive outcomes are associated with the capacity for executive control over core emotional functions.
“Given the role of this particular region of dmPFC in facilitating goal-directed behavior by integrating cognitive information with associated rewards and punishments (Shackman et al, 2011), the association between positive outcomes and high baseline connectivity between this region and the sgACC and low baseline connectivity with striatum may suggest that positive outcomes are associated with the”
From Resting-state cortico-thalamic-striatal connectivity predicts response to dorsomedial prefrontal rTMS in major depressive disorder (2014) · cites this paper as Shackman et al, 2011
Stress, negative affect, and pain provide interoceptive input that elicits drug use schemas and further dysregulates prefrontal control over automaticity, amplifying addictive behavior.
“Stress, negative affect, and pain provide additional interoceptive input to elicit drug use schemas and further dysregulate prefrontal control over automaticity,20–23 amplifying addictive behavior.24”
From Restructuring reward processing with Mindfulness‐Oriented Recovery Enhancement: novel therapeutic mechanisms to remediate hedonic dysregulation in addiction, stress, and pain (2016) · cites this paper as [22]
The periaqueductal gray sends monosynaptic reciprocal projections to ventromedial prefrontal cortex and to anterior mid-cingulate cortex, orbitofrontal cortex, and other areas involved in action value and defensive behavior.
“It also sends monosynaptic, reciprocal projections to the vmPFC—which is essential for value updating in the RL framework and likely for behavioral choice as well31—and to aMCC32, OFC and other areas involved in determining action value and coordinating defensive behavior18,33.”
From Representation of aversive prediction errors in the human periaqueductal gray (2014) · cites this paper as [33]
A recent meta-analysis of 939 studies found that aMCC is crucial for processing negative affect, pain and cognitive control.
“A recent meta-analysis of 939 studies (Shackman et al., 2011) found that aMCC is crucial for processing negative affect, pain and cognitive control.”
From Differential pattern of functional brain plasticity after compassion and empathy training (2014) · cites this paper as Shackman et al., 2011

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[121]Rolls ET Emotion explained 2007 Oxford University Press NY
[214]Nichols T Brett M Andersson J Wager T Poline JB Valid conjunction inference with the minimum statistic Neuroimage 2005 25 653 660 15808966

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Authors: Shackman, A. J., Salomons, T. V., Slagter, H. A., Fox, A. S., Winter, J. J., & Davidson, R. J.
Affiliations: University of Wisconsin–Madison (US)
University of Amsterdam (NL)
University of Minnesota (US)
Corresponding author: Shackman, Alexander J.
Salomons, Tim V.
Davidson, Richard J.
ORCID: Shackman, Alexander J.
Salomons, Tim V.
Slagter, Heleen A.
Fox, Andrew S.
Winter, Jameel J.
Davidson, Richard J.
Venue: Nature Reviews Neuroscience
Publisher: Springer Science and Business Media LLC
Published: 2011-02-18
Volume: 12
Issue: 3
Pages: 154-167
ISSN: 1471-003X (ISSN-L)
1471-0048
DOI: 10.1038/nrn2994
PMC: PMC3044650
OpenAlex: W2112135274
Semantic Scholar: 71fcfd6beb3837dbe9c28226b56cb08c7a2ff2fe
Cited by: 2,082
References: 478
Citations by year: 2026: 118 · 2025: 125 · 2024: 103 · 2023: 111 · 2022: 140 · 2021: 142 · 2020: 133 · 2019: 158 · 2018: 170 · 2017: 168 · 2016: 147 · 2015: 153 · 2014: 134 · 2013: 142 · 2012: 95
FWCI: 11.10
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.springer.com/tdm (tdm)
Locations: Nature reviews. Neuroscience (publishedVersion)
PubMed (publishedVersion)
UvA-DARE (University of Amsterdam) (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
UvA-DARE (University of Amsterdam) (submittedVersion)
Data Archiving and Networked Services (DANS) (submittedVersion)
Funders: National Institute of Mental Health (R01MH064498, P50MH069315, R01MH43454, P50MH084051, R01MH043454, T32MH018931)
Eunice Kennedy Shriver National Institute of Child Health and Human Development (P30HD003352)
Topics: Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
Keywords: anterior midcingulate cortex, negative affect, pain, cognitive control, emotion-cognition integration, punishment, goal-directed behavior, functional segregation, reward processing, computational modelling
MeSH terms: Animals, Cognition, Emotions, Gyrus Cinguli, Humans, Pain, Reinforcement, Psychology

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The integration of negative affect, pain and cognitive control in the cingulate cortex

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