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Amygdala–frontal connectivity during emotion regulation
Open accessAbstract
Successful control of affect partly depends on the capacity to modulate negative emotional responses through the use of cognitive strategies (i.e., reappraisal). Recent studies suggest the involvement of frontal cortical regions in the modulation of amygdala reactivity and the mediation of effective emotion regulation. However, within-subject inter-regional connectivity between amygdala and prefrontal cortex in the context of affect regulation is unknown. Here, using psychophysiological interaction analyses of functional magnetic resonance imaging data, we show that activity in specific areas of the frontal cortex (dorsolateral, dorsal medial, anterior cingulate, orbital) covaries with amygdala activity and that this functional connectivity is dependent on the reappraisal task. Moreover, strength of amygdala coupling with orbitofrontal cortex and dorsal medial prefrontal cortex predicts the extent of attenuation of negative affect following reappraisal. These findings highlight the importance of functional connectivity within limbic-frontal circuitry during emotion regulation.
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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 Banks, Eddy, Angstadt, Nathan, & Phan, 2007
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
“Alcohol disrupts functional connectivity between the amygdala and prefrontal areas—including the dorsolateral prefrontal cortex (DLPFC), orbitofrontal cortex (OFC), ventrolateral PFC (VLPFC), and anterior cingulate cortex (ACC)—regions critical for emotion regulation, behavioral inhibition, and social cognition (Harenski And Hamann 2006; Banks et al. 2007; Goldin et al. 2008; Prater et al. 2013).”
From Decoding the bidirectional links between alcohol misuse and aggression: toward a unified translational framework (2026) · cites this paper as Banks et al. 2007
Experimental — accuracy not yet measuredIn the citing paper
“neuroimaging studies in humans show an inverse relationship between the amygdala and multiple PFC regions including vmPFC,45,46 vlPFC,32,47,48 dmPFC,23,34,49–54 and dlPFC.25,34”
From Neural Substrates of Childhood Anxiety Disorders (2012) · cites this paper as [48]
In the citing paper
“Reciprocal connections between the BLA and mPFC are important for fear extinction, fear discrimination, and other processes requiring the resolution of conflicting information (47–50), and dendritic hypotrophy in mPFC neurons has been linked to stress and alcohol-related deficits in fear extinction (51,52).”
From Chronic Stress Remodels Synapses in an Amygdala Circuit-Specific Manner (2019) · cites this paper as [48]
In the citing paper
“specifically prefrontal down-regulation of amygdala activity has been associated with the attenuation of negative affect during emotion regulation (Banks et al., 2007).”
From Positive parenting predicts the development of adolescent brain structure: a longitudinal study (2014) · cites this paper as Banks et al., 2007
In the citing paper
“There is also evidence that the interaction between prefrontal structures and the amygdala is critical to emotion regulation”
From Positive parenting predicts the development of adolescent brain structure: a longitudinal study (2014) · cites this paper as Banks et al., 2007
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Citations
Cites
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Background
Research works printed but not linked: 2
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Amygdala activity related to perceived social support
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“…the VLPFC, which has strong anatomical connections to the amygdala (Etkin et al., 2015), as playing an inhibitory role during reappraisal (Ochsner et al., 2012), as reflected in a negative correlation between activity in the VLPFC and the amygdala (Banks et al., 2007; Ochsner et al., 2002).”
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An fMRI Pilot Study of Cognitive Reappraisal in Children: Divergent Effects on Brain and Behavior
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“This can also disrupt PFC-dependent executive control, which normally provides inhibitory regulation over the amygdala and overrides fear-related messages through top-down processing (Banks et al., 2007; De Raedt, 2006; Quirk & Mueller, 2007).”
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“Similar dysfunction in this circuitry is associated with anxiety disorders, including altered circuit connectivity (Banks et al., 2007; Prater et al., 2013), hyperactivity in the amygdala (Etkin and Wager, 2007), and hyperactivity and hypoactivity in the prefrontal and cingulate cortex (Shin and…”
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“Indeed, slower breathing can modulate the anxiety level, which is reflected by changes in amygdala activation, as well as the connectivity between the amygdala and prefrontal areas (Banks et al., 2007; Kim et al., 2011; Doll et al., 2016).”
BackgroundDynamic changes of large-scale resting-state functional networks in major depressive disorder
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“Functional brain imaging studies on the cognitive re-interpretation of aversive stimuli to reduce negative affect have consistently demonstrated that this type of reappraisal provoked increased DMPFC activation together with reduced amygdala recruitment (e.g., Banks et al., 2007).”
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BackgroundFunctional connectivity during masked and unmasked face emotion processing in bipolar disorder
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Representation of Cognitive Reappraisal Goals in Frontal Gamma Oscillations
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“This inverse relationship between frontal cortical and subcortical areas was predominantly observed in cognitive reappraisal tasks [15,21,22], and was directly related to the performance of emotion regulation [23].”
BackgroundResultThe Dialectic Between Empathy and Violence: An Opportunity for Intervention?
Chialant, D., Edersheim, J. G., & Price, B. H. (2016) · Journal of Neuropsychiatry · doi:10.1176/appi.neuropsych.15080207 · Cited by 33
Meeten, F., Davey, G. C. L., Makovac, E., Watson, D. R., Garfinkel, S. N., Critchley, H., & Ottaviani, C. (2016) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2016.00553 · Cited by 30
Transcranial magnetic stimulation for treatment of major depression during pregnancy: a review
Felipe, R. D. M., Ferrão, Y. A., & UFCSPA, B. (2016) · Trends in Psychiatry and Psychotherapy · doi:10.1590/2237-6089-2015-0076 · Cited by 30
Sulpizio, S., Doi, H., Bornstein, M. H., Cui, J., Esposito, G., & Shinohara, K. (2018) · Infant Behavior and Development · doi:10.1016/j.infbeh.2018.05.009 · Cited by 30
Kisspeptin as a Behavioral Hormone
Mills, E., O'Byrne, K. T., & Comninos, A. N. (2019) · Seminars in Reproductive Medicine · doi:10.1055/s-0039-3400239 · Cited by 31
Moral competence and brain connectivity: A resting-state fMRI study
Jung, W. H., Prehn, K., Fang, Z., Korczykowski, M., Kable, J. W., Rao, H., & Robertson, D. C. (2016) · NeuroImage · doi:10.1016/j.neuroimage.2016.07.045 · Cited by 35
“…of altered amygdala activity and amygdala-vmPFC/subgenual anterior cingulate cortex (sgACC) connectivity during emotion regulation (Ochsner et al., 2002; 2004; Banks et al. 2007), increased amygdala-vmPFC coupling in HCSG may be related to increased regulation of negative emotion in this group.”
Extended‐amygdala intrinsic functional connectivity networks: A population study
Berry, S. C., Wise, R. G., Lawrence, A. D., & Lancaster, T. M. (2020) · Human Brain Mapping · doi:10.1002/hbm.25314 · Cited by 29
Katyal, S., Hajcak, G., Flora, T., Bartlett, A., & Goldin, P. (2019) · Cognitive, Affective, & Behavioral Neuroscience · doi:10.3758/s13415-020-00771-y · Cited by 23
Mapping common grey matter volume deviation across child and adolescent psychiatric disorders
Li, T., Wang, L., Camilleri, J. A., Chen, X., Li, S., Stewart, J. L., Jiang, Y., Eickhoff, S. B., & Feng, C. (2020) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2020.05.015 · Cited by 30
Probing fMRI brain connectivity and activity changes during emotion regulation by EEG neurofeedback
Dehghani, A., Soltanian-Zadeh, H., & Hossein-Zadeh, G. (2020) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2022.988890 · Cited by 31
“The higher co-activation pattern between the limbic system (amygdala, insula, ventral striatum, and thalamus) and prefrontal and frontal cortex (DMPFC, OFC, and VLPFC) was associated with the effectiveness of emotion regulation and less intensity of negative affect and lower level of anxiety, especially lower function…”
BackgroundCarpenter, K. L. H., Angold, A. C., Chen, N., Copeland, W., Gaur, P., Pelphrey, K. A., Song, A. W., & EGGER, H. L. (2015) · PLoS ONE · doi:10.1371/journal.pone.0116854 · Cited by 31
Wang, Z., Zhang, M., Han, Y., Song, H., Guo, R., & Li, K. (2016) · Journal of X-Ray Science and Technology · doi:10.3233/xst-160556 · Cited by 32
“The amygdala–frontal interactions has been shown to be the primary neural substrate of emotion processing and regulation [37].”
Schuette, S. R. M., Fernández‐Fernández, D., Lamla, T., Rosenbrock, H., & Hobson, S. (2016) · Journal of Neuroscience · doi:10.1523/jneurosci.3600-15.2016 · Cited by 29
“Both structures are involved in providing emotional significance to an aversive situation (LeDoux, 2000; Banks et al., 2007; Meloni et al., 2008), as measured in CFC.”
BackgroundChen, S., Chen, C., Yang, J., & Yuan, J. (2017) · Scientific Reports · doi:10.1038/s41598-017-00073-3 · Cited by 33
Ismaylova, E., Lévesque, M. L., Pomares, F. B., Moshe Szyf, A., Nemoda, Z., Fahim, C., Vitaro, F., Brendgen, M. R., Dionne, G., Boivin, M., et al. (2018) · Translational Psychiatry · doi:10.1038/s41398-018-0195-6 · Cited by 28
Bryant, R. A., Erlinger, M., Felmingham, K. L., Klimova, A., Williams, L. M., Malhi, G. S., Forbes, D., & Korgaonkar, M. S. (2020) · Psychological Medicine · doi:10.1017/s0033291720001129 · Cited by 32
Liang, X., Zebrowitz, L. A., & Aharon, I. (2008) · Social Neuroscience · doi:10.1080/17470910802453105 · Cited by 28
“There also is evidence that OFC may modulate amygdala reactivity in the regulation of negative emotions (Banks, Eddy, Angstadt, Nathan, & Phan, 2007 ).”
Lamm, C., Granic, I., Zelazo, P. D., & Lewis, M. D. (2011) · Brain and Cognition · doi:10.1016/j.bandc.2011.06.008 · Cited by 28
The role of the basolateral amygdala in the perception of faces in natural contexts
Hortensius, R., Terburg, D., Morgan, B. E., Stein, D. J., van Honk, J., & de Gelder, B. (2016) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2015.0376 · Cited by 29
“For example, a study in humans found that coupling between the subgenual part of the ACC and the AMG was related to emotion regulation [76].”
BackgroundWetherill, R. R., Jagannathan, K., Hager, N., Childress, A. R., & Franklin, T. R. (2015) · Experimental and Clinical Psychopharmacology · doi:10.1037/pha0000036 · Cited by 28
Sulpizio, S., Grecucci, A., & Job, R. (2020) · European Journal of Neuroscience · doi:10.1111/ejn.15013 · Cited by 19
“Notably, previous studies used reappraisal (in the form of reinterpretation) and distraction, two well-known strategies 918 | SULPIZIO et aL. able to regulate emotions (Banks et al., 2007; Kanske et al., 2011; Ochsner et al., 2004; Schulze et al., 2011).”
MethodEffect of MAOA Genotype on Resting-State Networks in Healthy Participants
Clemens, B., Voss, B., Pawliczek, C. M., Mingoia, G., Weyer, D., Repple, J., Eggermann, T., Zerres, K., Reetz, K., & Habel, U. (2014) · Cerebral Cortex · doi:10.1093/cercor/bht366 · Cited by 29
“Such an interpretation would be supported by 1) previous neuroimaging findings showing that the dACC is specifically responsible for regulating and controlling motivational impulses (Banks et al. 2007; Pezawas et al. 2005), and 2) clinical studies showing that disrupted ACC activity is linked to increased aggressive b…”
ResultDissociable Neural Mechanisms Underlying the Modulation of Pain and Anxiety? An fMRI Pilot Study
Wiech, K., Edwards, R. R., Moseley, G. L., Berna, C., Ploner, M., & Tracey, I. (2014) · PLoS ONE · doi:10.1371/journal.pone.0110654 · Cited by 29
“This observation deviates from previous findings that showed an increased connectivity between lateral prefrontal regions including the DLPFC and the amygdala during emotion regulation [51, 52].”
ResultThe neurobiology of mindfulness meditation.
Zeidan, F. Z. (2014) · Cited by 27
Dopamine effects on stress-induced working memory deficits
Bahari, Z., Meftahi, G. H., & Meftahi, M. A. (2018) · Behavioural Pharmacology · doi:10.1097/fbp.0000000000000429 · Cited by 29
“As the amygdala is an important region for expression of negative emotions (such as fear memory) and motivational aspects of behavior, the BLA is in a strategic position to mediate our cognitive processes (Davis and Whalen, 2001; Adolphs, 2002; Amaral et al., 2003; Phelps, 2004; Banks et al., 2007).”
BackgroundSex differences in somatomotor representations of others’ pain: a permutation-based analysis
Christov‐Moore, L., & Iacoboni, M. (2018) · Brain Structure and Function · doi:10.1007/s00429-018-1814-y · Cited by 27
“This sensitivity to context is likely the result of top-down control processes carried out by control systems that include medial and dorsolateral prefrontal cortex (MPFC and DLPFC) and perhaps the temporoparietal junction (TPJ) (Banks et al.”
Lamers, A., Toepper, M., Fernando, S., Schlosser, N., Bauer, E., Woermann, F., Driessen, M., & Beblo, T. (2019) · Journal of Psychiatry & Neuroscience · doi:10.1503/jpn.180077 · Cited by 25
Lloyd, W. K., Morriss, J., Macdonald, B., Joanknecht, K., Sigurðardottir, J. N., & van Reekum, C. M. (2020) · NeuroImage · doi:10.1016/j.neuroimage.2020.117488 · Cited by 28
Long term effects of early life stress on HPA circuit in rodent models
Babicola, L., Ventura, R., D’Addario, S. L., Ielpo, D., Andolina, D., & Segni, M. D. (2020) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2020.111125 · Cited by 31
Gao, Z., Cui, X., Wan, W., Zheng, W., & Gu, Z. (2021) · Biomedical Signal Processing and Control · doi:10.1016/j.bspc.2021.103291 · Cited by 27
The dark side of creativity: Neural correlates of malevolent creative idea generation
Gao, Z., Cheng, L., Li, J., Chen, Q., & Hao, N. (2022) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2022.108164 · Cited by 28
“Emotion control has been linked to activation in the pre-frontal cortex (PFC) (i.e., dorsal PFC and ventral PFC) and amygdala (Banks et al., 2007; Perlman et al., 2012).”
Ensink, K., Biberdzic, M., Normandin, L., & Clarkin, J. F. (2015) · Journal of Infant Child and Adolescent Psychotherapy · doi:10.1080/15289168.2015.1007715 · Cited by 32
Horáček, J., Mikoláš, P., Tintěra, J., Novák, T., Páleníček, T., Brunovský, M., Höschl, C., & Alda, M. (2015) · Journal of Psychiatry and Neuroscience · doi:10.1503/jpn.140044 · Cited by 27
Outhred, 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
Self-citationExtraversion modulates functional connectivity hubs of resting‐state brain networks
Pang, Y., Cui, Q., Duan, X., Chen, H., Zeng, L., Zhang, Z., Lu, G., & Chen, H. (2015) · Journal of Neuropsychology · doi:10.1111/jnp.12090 · Cited by 26
Intentional and Incidental Self-Control in Ventrolateral Prefrontal Cortex
Cohen, J. R., Berkman, E. T., & Lieberman, M. D. (2013) · Oxford University Press eBooks · doi:10.1093/med/9780199837755.003.0030 · Cited by 30
“Additionally, there is evidence that the rVLPFC is functionally connected to the amygdala, possibly via the mPFC, which has reciprocal connections with both structures (Banks et al., 2007; Hariri et al., 2000, 2003; Lieberman et al., 2007).”
BackgroundFitzgerald, J. M., MacNamara, A., DiGangi, J. A., Kennedy, A. E., Rabinak, C. A., Patwell, R., Greenstein, J. E., Proescher, E., Rauch, S. A. M., Hajcak, G., et al. (2015) · Psychiatry Research Neuroimaging · doi:10.1016/j.pscychresns.2015.12.001 · Cited by 31
“, 2014) and reductions in amygdala responding have been found to correlate with reappraisal-related increases in prefrontal cortical activity (Banks et al., 2007).”
BackgroundInfluentialSelf-citationBerkers, R. M. W. J., Klumpers, F., & Fernández, G. (2016) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2016.01.016 · Cited by 28
“Connectivity between the mPFC and amygdala have been found to be important for regulating emotions (Banks et al., 2007; Quirk & Beer, 2006).”
BackgroundThe effect of constraining eye-contact during dynamic emotional face perception—an fMRI study
Hadjikhani, N. K., Zürcher, N. R., Lassalle, A., Hippolyte, L., Ward, N., & Johnels, J. Å. (2017) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nsx046 · Cited by 33
“, 2007) and the dynamic interaction of the amygdala with the social brain modulates the recognition and modulation of affective states (Banks et al., 2007; Miyahara et al., 2013).”
BackgroundKim, J. U., Weisenbach, S., & Zald, D. (2018) · International Journal of Geriatric Psychiatry · doi:10.1002/gps.4982 · Cited by 23
“In other words, closer linkage between lateral OFC and amygdala activity predicted more successful ER.(27)”
Background
Metadata
- Authors
- Banks, S. J., Eddy, K. T., Angstadt, M., Nathan, P. J., & Phan, K. L.
- Affiliations
- University of Chicago (US)
- Venue
- Social Cognitive and Affective Neuroscience
- Publisher
- Oxford University Press (OUP)
- Published
- 2007-07-21
- Volume
- 2
- Issue
- 4
- Pages
- 303-312
- ISSN
- 1749-5016 (ISSN-L)
- 1749-5024
- PMC
- PMC2566753
- OpenAlex
- W2146828510
- Cited by
- 1,187
- References
- 92
- Citations by year
- 2026: 39 · 2025: 61 · 2024: 44 · 2023: 57 · 2022: 69 · 2021: 100 · 2020: 92 · 2019: 104 · 2018: 87 · 2017: 78 · 2016: 98 · 2015: 75 · 2014: 76 · 2013: 49 · 2012: 44
- FWCI
- 10.92
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- cc-by-nc
- Locations
- Social Cognitive and Affective Neuroscience (publishedVersion, cc-by-nc)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institute of Mental Health (MH076198, K23MH076198)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
- Life Sciences › Neuroscience › Cognitive Neuroscience › Functional Brain Connectivity Studies
- Social Sciences › Psychology › Experimental and Cognitive Psychology › Anxiety, Depression, Psychometrics, Treatment, Cognitive Processes
- Keywords
- amygdala, prefrontal cortex, emotion regulation, cognitive reappraisal, orbitofrontal cortex, dorsomedial prefrontal cortex, anterior cingulate cortex, dorsolateral prefrontal cortex, negative affect, amygdala reactivity
- MeSH terms
- Adult, Affect, Amygdala, Facial Expression, Female, Frontal Lobe, Humans, Male, Nerve Net, Expressed Emotion, Young Adult
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