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Prefrontal-Subcortical Pathways Mediating Successful Emotion Regulation
Open accessAbstract
Although prefrontal cortex has been implicated in the cognitive regulation of emotion, the cortical-subcortical interactions that mediate this ability remain poorly understood. To address this issue, we identified a right ventrolateral prefrontal region (vlPFC) whose activity correlated with reduced negative emotional experience during cognitive reappraisal of aversive images. We then applied a pathway-mapping analysis on subcortical regions to locate mediators of the association between vlPFC activity and reappraisal success (i.e., reductions in reported emotion). Results identified two separable pathways that together explained approximately 50% of the reported variance in self-reported emotion: (1) a path through nucleus accumbens that predicted greater reappraisal success, and (2) a path through ventral amygdala that predicted reduced reappraisal success (i.e., more negative emotion). These results provide direct evidence that vlPFC is involved in both the generation and regulation of emotion through different subcortical pathways, suggesting a general role for this region in appraisal processes.
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“Further, greater dmPFC activation and connectivity with the amygdala corresponded to reappraisal success in both healthy individuals (Banks, Eddy, Angstadt, Nathan, & Phan, 2007; Wager, Davidson, Hughes, Lindquist, & Ochsner, 2008) and patients with social anxiety disorder (Goldin et al., 2009).”
From Changes in functional connectivity with cognitive behavioral therapy for social anxiety disorder predict outcomes at follow-up (2020) · cites this paper as Wager, Davidson, Hughes, Lindquist, & Ochsner, 2008
Experimental — accuracy not yet measuredThe source backs part of the claim, not all of it — or backs it for a different population, condition or comparison.
In the citing paper
“In one of the studies (Wager et al., 2008), when the rated success of emotional regulation was regressed on the cognitive reappraisal of emotion contrast, the dlPFC contribution was smaller and that of the lOFC/vlPFC larger than in the standard subtraction analysis (Figure 5).”
From Top-Down Dysregulation—From ADHD to Emotional Instability (2016) · cites this paper as Wager et al., 2008
Experimental — accuracy not yet measuredThe source backs part of the claim, not all of it — or backs it for a different population, condition or comparison.
In the citing paper
“some studies demonstrated the role of VLPFC on mediating Amygdala activity in respect to negative stimuli41,42”
From Ventrolateral but not Dorsolateral Prefrontal Cortex tDCS effectively impact emotion reappraisal – effects on Emotional Experience and Interbeat Interval (2018) · cites this paper as [41]
Experimental — accuracy not yet measuredThe check wasn’t confident either way, so it gives no verdict — never disputed.
In the citing paper
“The emotional Stroop task regularly shows prefrontal activations both in dlPFC and lateral orbitofrontal cortex (lOFC)/vlPFC (Eippert et al., 2007; Wager et al., 2008; Kanske et al., 2011; Golkar et al., 2012; Buhle et al., 2014)”
From Top-Down Dysregulation—From ADHD to Emotional Instability (2016) · cites this paper as Wager et al., 2008
Experimental — accuracy not yet measuredIn the citing paper
“This dual role of the VLPFC in emotion regulation may be reflected in positive amygdala-VLPFC associations which negatively predict regulation success and positive VS-VLPFC associations which positively predict regulation success (Wager et al., 2008).”
From Neural network of cognitive emotion regulation—an ALE meta-analysis and MACM analysis (2014) · cites this paper as Wager et al., 2008
In the citing paper
“but one can infer from our analyses and the literature, that a highly plausible candidate structure in the direct pathway model would be the VLPFC as it detects salience, is a core structure for appraisal processes (Hampshire et al., 2010; Wager et al., 2008) and would also be in a good position to initiate higher order cognitive processes or complex behaviors through its involvement in the medial”
From Neural network of cognitive emotion regulation—an ALE meta-analysis and MACM analysis (2014) · cites this paper as Wager et al., 2008
In the citing paper
“In this study, vmPFC activity was associated with increased reappraisal success in a manner mediated by changes in the ventral striatum, though other dorsomedial and lateral prefrontal regions are likely to be important as well [54,55].”
From Ventromedial prefrontal–subcortical systems and the generation of affective meaning (2012) · cites this paper as [54]
In the citing paper
“In one recent study, positive reappraisal reduced amygdala responses to aversive visual images and increases activity in the ventral striatum, which in turn predict reappraisal effects on emotional experience [54] (figure 1h).”
From Ventromedial prefrontal–subcortical systems and the generation of affective meaning (2012) · cites this paper as [54]
In the citing paper
“A second prediction is that reappraisal-related fMRI activity will emerge when controlling for activity in lateral cortical ‘attention systems’ (partially done in [54]; see Supplementary Online Materials for additional discussion).”
From Ventromedial prefrontal–subcortical systems and the generation of affective meaning (2012) · cites this paper as [54]
In the citing paper
“the NAc-vmPFC pathway previously shown to be important for emotion/pain regulation, and valuation in a range of contexts [6],[53],[74]–[77]”
From Distinct Brain Systems Mediate the Effects of Nociceptive Input and Self-Regulation on Pain (2015) · cites this paper as [6]
In the citing paper
“Ex-partner versus Friend was predicted by increased activity in dorsomedial prefrontal cortex (dmPFC), right temporal parietal junction (TPJ) and precuneus, which are reliably associated with mentalizing about others38,39, and several other regions associated with negative emotion and its regulation20,40,41, including thalamus, supplementary motor area and inferior frontal gyrus.”
From Separate neural representations for physical pain and social rejection (2014) · cites this paper as [40]
In the citing paper
“and VS activity mediated the relationship between ventrolateral PFC activation and reappraisal success (i.e. less negative emotional experience).”
From Neural correlates of social exclusion across ages: A coordinate-based meta-analysis of functional MRI studies (2017) · cites this paper as Wager et al., 2008
In the citing paper
“Wager and colleagues (2008) found that ventrolateral PFC activation was positively correlated with that of the VS when engaging in cognitive reappraisal of aversive images”
From Neural correlates of social exclusion across ages: A coordinate-based meta-analysis of functional MRI studies (2017) · cites this paper as Wager et al., 2008
In the citing paper
“Similarly, ventral lPFC has also been identified in studies of negative affect following social exclusion (Sebastian et al., 2009), emotion regulation in labeling negative affect (Lieberman et al., 2007), and negative emotion reappraisal (Wager et al., 2008).”
From Risk-taking and social exclusion in adolescence: neural mechanisms underlying peer influences on decision-making (2013) · cites this paper as Wager et al., 2008
In the citing paper
“Given its role in reward processing, the ventral striatum may serve to aid in the reappraisal of negative experiences into positive interpretations (Masten et al., 2009, Wager et al., 2009).”
From Dopaminergic reward sensitivity can promote adolescent health: a new perspective on the mechanism of ventral striatum activation (2016) · cites this paper as Wager et al., 2009
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“Further, greater dmPFC activation and connectivity with the amygdala corresponded to reappraisal success in both healthy individuals (Banks, Eddy, Angstadt, Nathan, & Phan, 2007; Wager, Davidson, Hughes, Lindquist, & Ochsner, 2008) and patients with social anxiety disorder (Goldin et al., 2009).”
BackgroundResultBrain mediators of biased social learning of self-perception in social anxiety disorder
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Neuro-genetics of persistent pain
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Felder, J. N., Smoski, M. J., Kozink, R. V., Froeliger, B., McClernon, F. J., Bizzell, J., Petty, C., & Dichter, G. S. (2012) · BMC Psychiatry · doi:10.1186/1471-244x-12-152 · Cited by 18
Cingulate-centered large-scale networks: Normal functions, aging, and neurodegenerative disease
Touroutoglou, A., & Dickerson, B. C. (2019) · Handbook of clinical neurology · doi:10.1016/b978-0-444-64196-0.00008-x · Cited by 23
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Bogaerts, K., Houte, M. V. D., Jongen, D., Ly, H. G., Coppens, E., Schruers, K. R. J., Diest, I. V., Jan, T., Wambeke, P. V., Petre, B., et al. (2023) · Translational Psychiatry · doi:10.1038/s41398-023-02567-3 · Cited by 23
“Two complementary mediation analyses were performed using the CANlab mediation toolbox (https://github.com/canlab/MediationToolbox) [36].”
MethodSelf-citationXu, B., Wei, S., Yin, X., Jin, X., Yan, S., & Jia, L. (2023) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2023.927389 · Cited by 15
“Abnormal prefrontal cortex functional activities have been reported in a large number of studies to closely correlate with difficulties in emotion regulation and emotional disorders (Wager et al., 2008; Kanske et al., 2011; Rabinak et al., 2014; Koch et al., 2016; Yang et al., 2020).”
BackgroundCaballero, C., Nook, E. C., & Gee, D. G. (2022) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2022.105002 · Cited by 23
“reappraisal was associated with reappraisal effectiveness in adults (Morawetz et al., 2017; Wager et al., 2008).”
BackgroundCao, D., Li, Y., & Tang, Y.-Y. (2021) · Cognitive, Affective, & Behavioral Neuroscience · doi:10.3758/s13415-021-00881-1 · Cited by 19
Sulpizio, S., Grecucci, A., & Job, R. (2020) · European Journal of Neuroscience · doi:10.1111/ejn.15013 · Cited by 19
“Previous fMRI studies clearly showed a reduction in amygdala activity when the prefrontal cortex was operating under regulatory instructions (Lee et al., 2012; Wager et al., 2008).”
BackgroundChen, Y., Chen, T., & Cai, X. (2020) · Behavioural Brain Research · doi:10.1016/j.bbr.2020.112862 · Cited by 20
Zhang, T., Bai, T., Xie, W., Wei, Q., Lv, H., Wang, A., Guan, J., Tian, Y., & Wang, K. (2020) · Brain Imaging and Behavior · doi:10.1007/s11682-020-00371-x · Cited by 21
Your presence soothes me: a neural process model of aversive emotion regulation via social buffering
Bratec, S. M., Bertram, T., Starke, G., Brandl, F., Xie, X., & Sorg, C. (2020) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nsaa068 · Cited by 29
“Recently developed mediation analysis, in contrast, allows one to assess how changes in brain activity induced by an experimental manipulation lead to specific behavioural outcomes (Wager et al., 2008).”
BackgroundDörfel, D., Gärtner, A., & Scheffel, C. (2020) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2020.00128 · Cited by 23
The impact of focused attention on subsequent emotional recollection: A functional MRI investigation
Dolcos, F., Katsumi, Y., Bogdan, P. C., Shen, C., Jun, S., Buetti, S., Lleras, A., Bost, K. K., Weymar, M., & Dolcos, S. M. (2020) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2020.107338 · Cited by 20
Neural correlates of up-regulating positive emotions in fMRI and their link to affect in daily life
Rueschkamp, J. M. G., Brose, A., Villringer, A., & Gaebler, M. (2019) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nsz079 · Cited by 20
“Such regulatory effects are usually ascribed to cognitive control processes in prefrontal and parietal regions (such as lateral and medial prefrontal as well as lateral parietal cortices), which in turn modulate activity in subcortical affect processing regions, such as the VS and the amygdala (Wager et al., 2008; Och…”
BackgroundGoodin, P., Lamp, G., Hughes, M. E., Rossell, S. L., & Ciorciari, J. (2019) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2019.00060 · Cited by 25
Emotion Reactivity and Regulation in Adolescent Girls Following an Interpersonal Rejection
Miller, A. B., Prinstein, M. J., Munier, E., Machlin, L., & Sheridan, M. A. (2018) · Journal of Cognitive Neuroscience · doi:10.1162/jocn_a_01351 · Cited by 24
Jacob, Y., Shany, O., Goldin, P. R., Gross, J. J., & Hendler, T. (2018) · Cerebral Cortex · doi:10.1093/cercor/bhy181 · Cited by 20
Functional Mediation Analysis with an Application to Functional Magnetic Resonance Imaging DataPreprint
Zhao, Y., Luo, X., Lindquist, M. A., & Caffo, B. S. (2018) · arXiv (Cornell University) · doi:10.48550/arxiv.1805.06923 · Cited by 7
“In the neuroimaging context, causal mediation analysis is becoming an increasingly important method for assessing the intermediate effects of brain function on cognitive behavior (Wager et al., 2008, 2009b,a; Atlas et al., 2010, 2014; Woo et al., 2015).”
MethodSelf-citationFirk, C., Dahmen, B., Lehmann, C., Herpertz‐Dahlmann, B., & Konrad, K. (2017) · Emotion · doi:10.1037/emo0000373 · Cited by 23
The association between resting functional connectivity and dispositional optimism
Ran, Q., Yang, J., Yang, W., Wei, D., Qiu, J., & Zhang, D. (2017) · PLoS ONE · doi:10.1371/journal.pone.0180334 · Cited by 21
Light, S. N., Bieliauskas, L. A., & Zubieta, J. (2017) · Journal of Neuropsychiatry · doi:10.1176/appi.neuropsych.16090171 · Cited by 24
Localized or diffuse: the link between prefrontal cortex volume and cognitive reappraisal.
Moore, M., Iordan, A., Hu, Y., Kragel, J., Dolcos, S., & Dolcos, F. (2016) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nsw043 · Cited by 19
Computational dissection of human episodic memory reveals mental process-specific genetic profiles
Lukšys, G., Fastenrath, M., Coynel, D., Freytag, V., Gschwind, L., Heck, A., Jessen, F., Maier, W., Milnik, A., Riedel-Heller, S. G., et al. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1500860112 · Cited by 20
Gu, X., Kirk, U., Lohrenz, T. M., & Montague, P. R. (2013) · Human Brain Mapping · doi:10.1002/hbm.22433 · Cited by 15
“This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.”
BackgroundMethodGendron, M., Mesquita, B., & Barrett, L. F. (2020) · Culture, Mind, and Brain · doi:10.1017/9781108695374.010 · Cited by 20
Li, J., Kuang, S., Liu, Y., Wu, Y., & Li, H. (2024) · Human Brain Mapping · doi:10.1002/hbm.26702 · Cited by 21
“Insula is also a part of the affective network and has functional interconnections to regions associated with the experience of emotion (Wager et al., 2008).”
BackgroundElton, A., Faulkner, M. L., Robinson, D. L., & Boettiger, C. A. (2021) · Neuropsychopharmacology · doi:10.1038/s41386-021-00993-9 · Cited by 20
Wang, Y., Liao, C., Shangguan, C., Wenjing, S., & Zhang, W. (2020) · Psychophysiology · doi:10.1111/psyp.13690 · Cited by 23
Maltreatment and Emotional Development
Harms, M. B., Leitzke, B. T., & Pollak, S. D. (2019) · Springer eBooks · doi:10.1007/978-3-030-17332-6_28 · Cited by 18
Neural Subtypes of Euthymic Bipolar I Disorder Characterized by Emotion Regulation Circuitry
Njau, S. N., Townsend, J. D., Wade, B., Hellemann, G., Bookheimer, S. Y., Narr, K. L., & Brooks, J. O. (2020) · Biological Psychiatry Cognitive Neuroscience and Neuroimaging · doi:10.1016/j.bpsc.2020.02.011 · Cited by 19
Cui, G., Wang, Y., Wang, X., Zheng, L., Li, L., Li, P., Zhang, L., Guo, Y. Q., Chen, Y., Sun, Z., et al. (2019) · Behavioural Brain Research · doi:10.1016/j.bbr.2019.112335 · Cited by 20
Right ventrolateral prefrontal cortex involvement in proactive and reactive aggression
Chen, C.-Y. (2018) · Neuroreport · doi:10.1097/wnr.0000000000001144 · Cited by 19
An endocannabinoid receptor polymorphism modulates affective processing under stress
Wirz, L., Reuter, M., Felten, A., & Schwabe, L. (2018) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nsy083 · Cited by 23
“, 2002), as well as PFC areas [medial PFC (mPFC), ventromedial PFC (vmPFC), ventrolateral PFC (vlPFC)] that play a pivotal role in emotion regulation (Wager et al., 2008; Motzkin et al., 2015).”
BackgroundResultKummar, A. S. (2017) · Psychological Reports · doi:10.1177/0033294117740137 · Cited by 17
Harenski, C. L., Harenski, K. A., Calhoun, V. D., & Kiehl, K. A. (2018) · Brain Imaging and Behavior · doi:10.1007/s11682-018-9957-2 · Cited by 26
Ellard, K., Gosai, A., Bernstein, E. E., Kaur, N., Sylvia, L., Camprodon, J., Dougherty, D., Nierenberg, A., & Deckersbach, T. (2018) · Journal of Affective Disorders · doi:10.1016/j.jad.2018.06.002 · Cited by 18
“The IPL represents a key node in the frontoparietal control network, and has been identified as an important region in an integrative multi-network system implicated in emotion-cognition integration (Cromheeke and Mueller, 2014; Wager et al., 2008; Wang et al., 2017).”
BackgroundWiemer, J., & Pauli, P. (2016) · Biological Psychology · doi:10.1016/j.biopsycho.2016.01.007 · Cited by 20
Yin, H., Tully, L. M., Lincoln, S. H., & Hooker, C. I. (2015) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2015.00469 · Cited by 19
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“…lateral PFC, both ventral and dorsolateral aspects (or inferior, middle and superior frontal gyrus, respectively), as integral for emotion regulation, including findings indicating a central role for VLPFC in both the generation and regulation of emotional processes (Wager et al ., 2008).”
BackgroundExecutive-affective connectivity in smokers viewing anti-smoking images: An fMRI study
Dinh-Williams, L., Mendrek, A., Dumais, A., Bourque, J., & Potvin, S. (2014) · Psychiatry Research Neuroimaging · doi:10.1016/j.pscychresns.2014.10.018 · Cited by 17
“The IFG and LOFC possess a rich set of connections to cortical and subcortical regions that are key to emotional processing, and this connectivity is believed to underlie emotionregulation processes (Eippert et al., 2007; Wager et al., 2008).”
BackgroundMorawetz, C., Berboth, S., & Bode, S. (2024) · Human Brain Mapping · doi:10.1002/hbm.26667 · Cited by 19
“The results are compatible with top-down models, which assume that frontal and parietal cognitive control regions inhibit the activity in emotion-generation regions such as the amygdala (Berboth & Morawetz, 2021; Buhle et al., 2014; Ochsner et al., 2012; Wager et al., 2008).”
BackgroundResultUpton, S., Brown, A. A., Ithman, M., Newman‐Norlund, R., Sahlem, G. L., Prisciandaro, J. J., McClure, E. A., & Froeliger, B. (2023) · Biological Psychiatry Cognitive Neuroscience and Neuroimaging · doi:10.1016/j.bpsc.2023.07.014 · Cited by 16
Sankar, A., Shen, X., Čolić, L., Goldman, D. A., Villa, L. M., Kim, J. A., Pittman, B. P., Scheinost, D., Constable, R. T., & Blumberg, H. P. (2023) · Psychological Medicine · doi:10.1017/s003329172300003x · Cited by 22
“…(inferior temporal gyrus), and cerebellar regions that are implicated in various emotion regulation processes (Braunstein, Gross, & Ochsner, 2017; Ohira et al., 2006; Phillips, Ladouceur, & Drevets, 2008a; Schutter & van Honk, 2009; Wager, Davidson, Hughes, Lindquist, & Ochsner, 2008) (Table 1).”
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Association between parental age, brain structure, and behavioral and cognitive problems in children
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The dynamics of pain reappraisal: the joint contribution of cognitive change and mental load
Adamczyk, A. K., Ligeza, T. S., & Wyczesany, M. (2020) · Cognitive Affective & Behavioral Neuroscience · doi:10.3758/s13415-020-00768-7 · Cited by 29
Painold, A., Faber, P. L., Reininghaus, E. Z., Mörkl, S., Holl, A. K., Achermann, P., Saletu, B., Saletu-Zyhlarz, G. M., Anderer, P., Dalkner, N., et al. (2019) · Clinical EEG and Neuroscience · doi:10.1177/1550059419893472 · Cited by 14
“nodes of the default mode network, the frontoparietal central executive network, and the 2 ventral prefrontal networks that have been associated with self-referencing, executive processes, and emotional regulation, respectively.(89,103,104)”
Background
Metadata
- Authors
- Wager, T. D., Davidson, M. L., Hughes, B. L., Lindquist, M. A., & Ochsner, K. N.
- Affiliations
- Columbia University (US)
- Corresponding author
- Wager, Tor D.
- Venue
- Neuron
- Publisher
- Elsevier BV
- Published
- 2008-09
- Volume
- 59
- Issue
- 6
- Pages
- 1037-1050
- ISSN
- 0896-6273 (ISSN-L)
- PMC
- PMC2742320
- OpenAlex
- W2049423401
- Cited by
- 1,761
- References
- 130
- Citations by year
- 2026: 65 · 2025: 84 · 2024: 68 · 2023: 91 · 2022: 94 · 2021: 122 · 2020: 210 · 2019: 103 · 2018: 129 · 2017: 105 · 2016: 105 · 2015: 97 · 2014: 106 · 2013: 104 · 2012: 90
- FWCI
- 31.97
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- www.elsevier.com/tdm/userlicense/1.0/ (tdm)
- www.elsevier.com/legal/tdmrep-license (tdm)
- www.elsevier.com/open-access/userlicense/1.0/ (vor, 1780 d)
- doi.org/10.15223/policy-017 (stm-asf)
- doi.org/10.15223/policy-037 (stm-asf)
- doi.org/10.15223/policy-012 (stm-asf)
- doi.org/10.15223/policy-029 (stm-asf)
- doi.org/10.15223/policy-004 (stm-asf)
- Locations
- Neuron (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Science Foundation (0631637)
- National Institutes of Health (MH076136, MH076137)
- 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
- emotion regulation, cognitive reappraisal, ventrolateral prefrontal cortex, nucleus accumbens, negative emotions, appraisal process, pathway mapping
- MeSH terms
- Adaptation, Psychological, Adult, Amygdala, Brain Mapping, Concept Formation, Emotions, Female, Humans, Magnetic Resonance Imaging, Male, Neural Pathways, Prefrontal Cortex, Comprehension
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