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Amygdala–prefrontal coupling underlies individual differences in emotion regulation
Open accessAbstract
Despite growing evidence on the neural bases of emotion regulation, little is known about the mechanisms underlying individual differences in cognitive regulation of negative emotion, and few studies have used objective measures to quantify regulatory success. Using a trait-like psychophysiological measure of emotion regulation, corrugator electromyography, we obtained an objective index of the ability to cognitively reappraise negative emotion in 56 healthy men (Session 1), who returned 1.3 years later to perform the same regulation task using fMRI (Session 2). Results indicated that the corrugator measure of regulatory skill predicted amygdala-prefrontal functional connectivity. Individuals with greater ability to down-regulate negative emotion as indexed by corrugator at Session 1 showed not only greater amygdala attenuation but also greater inverse connectivity between the amygdala and several sectors of the prefrontal cortex while down-regulating negative emotion at Session 2. Our results demonstrate that individual differences in emotion regulation are stable over time and underscore the important role of amygdala-prefrontal coupling for successful regulation of negative emotion.
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“deficits in this key voluntary emotion regulation circuit [58,60] may play an important role in impaired regulation of negative emotion in pediatric PTSD.”
From Trauma, PTSD, and the Developing Brain (2017) · cites this paper as [60]
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“03 7) ,w he re co nn ec tiv ity in ha pp ysh ap e w as sig ni fic an tly gr ea te r th an an gr ysh ap e w ith ⩾ 4 tr au m a ty pe s. Neuropsychopharmacology emotional responses through their connections with the amygdala (Kim et al, 2013; Lee et al, 2012).”
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“Moreover, better emotion downregulation was related to a stronger negative coupling between amygdala and dorsomedial/dorsolateral PFC (Lee et al., 2012) and ventromedial/ventrolateral PFC (Johnstone et al., 2007; Townsend et al., 2013) in healthy individuals, while patients with affective disorders…”
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“First, several studies have demonstrated that even though mean effects of task modulated connectivity with the amygdala were small, task modulated connectivity showed substantial individual differences (Cremers et al. 2010; Lee et al. 2012; Passamonti et al. 2008, 2009).”
BackgroundAmygdalar Function Reflects Common Individual Differences in Emotion and Pain Regulation Success
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“Finally, given the role of limbic-prefrontal circuits in self-regulation (Banks et al., 2007; Lee et al., 2012), poor amygdala-OFC neural connectivity may play a role in the well-established associations between externalizing personality traits, such as trait impulsivity, and alcohol use (e.”
BackgroundAmygdala–prefrontal connectivity modulates loss aversion bias in anxious individuals
Xu, P., Dam, N. T. V., van Tol, M., Shen, X., Cui, Z., Gu, R., Qin, S., Aleman, A., Fan, J., & Luo, Y. (2020) · NeuroImage · doi:10.1016/j.neuroimage.2020.116957 · Cited by 44
Holper, L., Scholkmann, F., & Wolf, M. (2014) · Behavioural Brain Research · doi:10.1016/j.bbr.2014.04.056 · Cited by 40
“[80] Lee H, Heller AS, van Reekum CM, Nelson B, Davidson RJ.”
BackgroundRamphal, B., DeSerisy, M., Pagliaccio, D., Raffanello, E., Rauh, V., Tau, G. Z., Posner, J. E., Marsh, R., & Margolis, A. E. (2020) · Cerebral Cortex Communications · doi:10.1093/texcom/tgaa033 · Cited by 47
“Whereas functional connectivity between the amygdala and the ventromedial prefrontal cortex normally decreases (shifts from positive to negative or near zero) over the course of child development to promote emotion regulation (Lee et al. 2012; Gee, Humphreys, et al. 2013b; Motzkin et al. 2015; Jalbrzikowski et al. 201…”
BackgroundDonati, G., Meaburn, E. L., & Dumontheil, I. (2021) · Cognition & Emotion · doi:10.1080/02699931.2021.1918644 · Cited by 50
“Neuroimaging studies in adults have shown an association between better down-regulation of emotions, measured behaviourally, and a greater inverse functional connectivity between the amygdala and parts of the prefrontal cortex during emotion regulation (Frank et al., 2014; Lee et al., 2012).”
Amygdala functional connectivity is reduced after the cold pressor task
Clewett, D., Schoeke, A., & Mather, M. (2013) · Cognitive Affective & Behavioral Neuroscience · doi:10.3758/s13415-013-0162-x · Cited by 41
How Affective Science Can Inform Clinical Science
Tracy, J. L., Klonsky, E. D., & Hajcak, G. (2014) · Clinical Psychological Science · doi:10.1177/2167702614537627 · Cited by 43
Pbert, L., Druker, S., Crawford, S., Frisard, C., Trivedi, M., Osganian, S. K., & Brewer, J. (2020) · Mindfulness · doi:10.1007/s12671-019-01273-w · Cited by 40
Cremers, H. R., Veer, I. M., Spinhoven, P., Rombouts, S. A. R. B., Yarkoni, T., Wager, T. D., & Roelofs, K. (2015) · Psychological Medicine · doi:10.1017/s0033291714002657 · Cited by 38
“…coupling and subjective or physiological responses during the instructed reappraisal of negative emotions (Urry et al. 2006; Wager et al. 2008; Lee et al. 2012) and indications of less cortical-amygdala connectivity during cognitive reappraisal in SAD patients (Goldin et al. 2009b).”
BackgroundResultConnectome‐based model predicts individual differences in propensity to trust
Lu, X., Li, T., Xia, Z., Zhu, R., Wang, L., Luo, Y., Feng, C., & Krüeger, F. (2019) · Human Brain Mapping · doi:10.1002/hbm.24503 · Cited by 37
Alterations in Amygdala Connectivity in Internet Addiction Disorder
Cheng, H., & Liu, J. (2020) · Scientific Reports · doi:10.1038/s41598-020-59195-w · Cited by 40
Dulka, B. N., Bagatelas, E. D., Bress, K. S., Grizzell, J. A., Cannon, M. K., Whitten, C. J., & Cooper, M. A. (2020) · Scientific Reports · doi:10.1038/s41598-020-63879-8 · Cited by 38
Rab, S. L., & Admon, R. (2020) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2020.09.007 · Cited by 36
Wang, Z., Ocampo, M. A., Pang, R. D., Bota, M., Bradesi, S., Mayer, E. A., & Holschneider, D. P. (2013) · PLoS ONE · doi:10.1371/journal.pone.0059138 · Cited by 36
Well-being and Anticipation for Future Positive Events: Evidences from an fMRI Study
Luo, Y., Chen, X., Qi, S., You, X., & Huang, X. (2018) · Frontiers in Psychology · doi:10.3389/fpsyg.2017.02199 · Cited by 40
“…and LeDoux, 2005; Sergerie et al., 2008) and different functional coupling between amygdala and prefrontal areas in various emotion processing (Lee et al., 2012; Diano et al., 2016, 2017; Di et al., 2017), we conducted psychophysiological interaction (PPI) analysis using left and right…”
BackgroundMethodInfluentialWhat Mindfulness can learn about Dissociation and what Dissociation can learn from Mindfulness
Forner, C. (2019) · Journal of Trauma & Dissociation · doi:10.1080/15299732.2018.1502568 · Cited by 34
“This is valuable in raising our young and not getting “dragged under” by another’s dysregulation (Alexander & Brown, 2011; Cahn & Polich, 2013; Diorioi et al., 1993; Farb et al., 2007; Hyejeen et al., 2012; Siegel, 1999).”
BackgroundInfluentialWu, Y., Zhong, Y., Ma, Z., Lu, X., Zhang, N., Fox, P. T., & Wang, C. (2018) · Psychiatry Research Neuroimaging · doi:10.1016/j.pscychresns.2018.09.009 · Cited by 36
Picó‐Pérez, M., Ipser, J., Taylor, P. A., Alonso, P., López‐Solà, C., Real, E., Segalàs, C., Roos, A., Menchón, J. M., Stein, D. J., et al. (2018) · Depression and Anxiety · doi:10.1002/da.22845 · Cited by 32
Spielberg, J. M., Schwarz, J. M., & Matyi, M. A. (2019) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2019.100791 · Cited by 37
“, 2017) and the extent to which physiological correlates of negative affect are observed (Lee et al., 2012).”
BackgroundChrysikou, E. G., Wing, E. K., & van Dam, W. O. (2019) · Biological Psychiatry Cognitive Neuroscience and Neuroimaging · doi:10.1016/j.bpsc.2019.12.004 · Cited by 38
Vines, L., Bridgwater, M., Bachman, P., Hayes, R., Catalano, S., & Jalbrzikowski, M. (2022) · Early Intervention in Psychiatry · doi:10.1111/eip.13212 · Cited by 30
Ge, L., Hu, Z., Wang, W., Parco Ming-fai, S. I. U., & Wei, G. (2021) · Life · doi:10.3390/life11060577 · Cited by 37
“A greater ability to down-regulate negative emotions means a greater amygdala attenuation and greater inverse OFC/dlPFC-amygdala FC [41].”
BackgroundGao, W., Biswal, B. B., Chen, S., Wu, X., & Yuan, J. (2021) · NeuroImage · doi:10.1016/j.neuroimage.2021.117918 · Cited by 30
Machiavellian emotion regulation in a cognitive reappraisal task: An fMRI study
Deák, A., Bodrogi, B., Biró, B., Perlaki, G., Orsi, G., & Bereczkei, T. (2017) · Cognitive Affective & Behavioral Neuroscience · doi:10.3758/s13415-016-0495-3 · Cited by 34
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).”
BackgroundThe safety and efficacy of botulinum toxin A on the treatment of depression
Zhang, Q., Wu, W., Fan, Y., Li, Y., Liu, J., Xu, Y., Jiang, C., Tang, Z., Cao, C., Liu, T., et al. (2021) · Brain and Behavior · doi:10.1002/brb3.2333 · Cited by 27
“The afferent nerve fibers of peripheral muscle can transmit emotionrelated information to the brain and inform the brain of the current emotional state (Heller et al., 2014; Kim et al., 2014; Lee et al., 2012).”
BackgroundOuthred, T., Das, P., Felmingham, K. L., Bryant, R. A., Nathan, P. J., Malhi, G. S., & Kemp, A. H. (2014) · Journal of Psychiatry and Neuroscience · doi:10.1503/jpn.130118 · Cited by 28
Scheffel, C., Diers, K., Schönfeld, S., Brocke, B., Strobel, A., & Dörfel, D. (2019) · Personality Neuroscience · doi:10.1017/pen.2019.11 · Cited by 24
Mao, C., Yang, H. J., Yang, Q. X., Sun, H. H., Zhang, G. R., & Zhang, Q. J. (2021) · Neuroscience · doi:10.1016/j.neuroscience.2021.12.003 · Cited by 26
Zhang, Z., Wang, S., Du, X., Qi, Y., Wang, L., & Dong, G. (2023) · Journal of Behavioral Addictions · doi:10.1556/2006.2023.00039 · Cited by 25
“In particular, individuals who were better able to down-regulate negative emotion showed stronger FC between the prefrontal regions and amygdala (H. Lee, Heller, Van Reekum, Nelson, & Davidson, 2012).”
Parrish, M. H., Inagaki, T. K., Muscatell, K., Byrne-Haltom, K. E., Leary, M., & Eisenberger, N. (2018) · Self and Identity · doi:10.1080/15298868.2018.1490344 · Cited by 25
“ulation abilities as measured by fMRI (Morawetz, Bode, Baudewig & Heekeren, 2017) and objective psychophysiological measures, such as corrugator electromyography (Lee et al., 2012).”
Farber, M. J., Kim, M. J., Knodt, A. R., & Hariri, A. R. (2019) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2019.100711 · Cited by 28
Gee, D. G., Hanson, C., Caglar, L. R., Fareri, D. S., Gabard-Durnam, L. J., Mills‐Finnerty, C., Goff, B., Caldera, C., Lumian, D. S., Flannery, J., et al. (2022) · Developmental Science · doi:10.1111/desc.13238 · Cited by 29
“Individual differences in the strength of connectivity between these regions predict behaviors associated with emotion regulation and anxiety in healthy adults (Banks et al., 2007;M. J. Kim et al., 2011; Lee et al., 2012; Pezawas et al., 2005).”
BackgroundGrossman, Y. S., Fillinger, C., Manganaro, A., Voren, G., Waldman, R. N., Zou, T., Janssen, W. G. M., Kenny, P. J., & Dumitriu, D. (2021) · Neuropsychopharmacology · doi:10.1038/s41386-021-01229-6 · Cited by 26
Beach, P. A., Huck, J. T., Zhu, D. C., & Bozoki, A. (2017) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2017.00297 · Cited by 26
“…mechanism to regulate both pain and general affect through inhibition of the amgydala via dense medial temporal projections (Quirk and Gehlert, 2003; Ghashghaei et al., 2007; Bingel et al., 2008; Kunz et al., 2011; Shackman et al., 2011; Lee et al., 2012; Etkin et al., 2015; Motzkin et al., 2015).”
Background
Metadata
- Authors
- Lee, H., Heller, A. S., van Reekum, C. M., Nelson, B., & Davidson, R. J.
- Affiliations
- University of Wisconsin–Madison (US)
- University of Illinois Chicago (US)
- Corresponding author
- Davidson, Richard J.
- Venue
- NeuroImage
- Publisher
- Elsevier BV
- Published
- 2012-09
- Volume
- 62
- Issue
- 3
- Pages
- 1575-1581
- ISSN
- 1053-8119 (ISSN-L)
- PMC
- PMC3408571
- OpenAlex
- W2155444575
- Cited by
- 219
- References
- 56
- Citations by year
- 2026: 3 · 2025: 17 · 2024: 9 · 2023: 11 · 2022: 14 · 2021: 23 · 2020: 22 · 2019: 16 · 2018: 20 · 2017: 19 · 2016: 23 · 2015: 13 · 2014: 16 · 2013: 12
- FWCI
- 6.71
- Type
- journal article
- Language
- en
- Open access
- Locations
- NeuroImage (publishedVersion)
- PubMed (publishedVersion)
- CentAUR (University of Reading) (acceptedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institute of Mental Health (R01-MH43454, P50-MH069315)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
- Social Sciences › Psychology › Experimental and Cognitive Psychology › Anxiety, Depression, Psychometrics, Treatment, Cognitive Processes
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Keywords
- emotion regulation, individual differences, amygdala, prefrontal cortex, cognitive reappraisal, negative emotions, longitudinal stability
- MeSH terms
- Amygdala, Brain Mapping, Electromyography, Emotions, Humans, Individuality, Magnetic Resonance Imaging, Male, Neural Pathways, Prefrontal Cortex, Young Adult
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