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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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“This is broadly consistent with the role of these regions in cognitive inhibition/control and executive function (Cabeza and Nyberg, 2000; Miller and Cohen, 2001), processes that are relevant to reappraisal-based affect regulation.”
Background
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Impairments of cognitive control in patients with somatoform disorders and their treatment
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Selective alterations of endocannabinoid system genes expression in obsessive compulsive disorder
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“We chose to analyse the Prefrontal Cortex (PFC) and the amygdala complex (AMY), brain regions showing a high distribution of the ECS [30], with strong connections between each other [31] and which interactions are relevant in emotions, motivations and cognitive processes [32 – 35].”
MethodCognition, emotion, and attention
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Happier People Show Greater Neural Connectivity during Negative Self-Referential Processing
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“Given the dense interconnectivity between neural regions associated with AC and NU (Banks et al. 2007) as well as data suggesting that affective context may be relevant for behaviorally-indexed AC deficits in OCD (Najmi et al. 2010), particularly for those with repugnant obsessions (Morein-Zamir et…”
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“…Delgado et al. 2008; van Stegeren et al. 2010), and emotion regulation, in which the PFC can downregulate emotional centers (Ochsner et al. 2004; Banks et al. 2007), we expect that a reciprocal influence of both cognitive and emotional centers is involved in associative cognitive--emotional…”
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“Examination of remitted MDD participants also reveals more negative functional connectivity between the amygdala and FG during the processing of sad expressions and more positive connectivity during the processing of happy expressions in comparison with healthy controls [40].”
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Padgaonkar, N. T., Uy, J. P., DePasque, S., Galván, A., & Peris, T. S. (2021) · Depression and Anxiety · doi:10.1002/da.23154 · Cited by 18
“In contrast, healthy adults with less negative affect demonstrate positive fronto‐limbic coupling during reappraisal (Banks et al., 2007).”
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“Highvagal tonemay reflect greater tonic inhibition of the amygdala by themPFC,which plays a critical role in effective regulation of negative emotion (Banks et al., 2007; Thayer et al., 2012).”
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“In addition, increased connectivity of the amygdala with regulation-related regions was found to correlate with reductions in negative affect following reappraisal among healthy participants (Banks et al. 2007).”
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“…functional connectivity of the lateral OFC could reflect the attempt to downregulate the emotional response which is automatically prompted by the trigger stimuli, given the role of this brain region in the reappraisal of stimuli associated with negative emotions (Banks et al., 2007).”
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“…including vmPFC have been shown to be involved in regulating emotional conflict (Etkin et al., 2006), directing attention away from emotional information that is irrelevant to the task (Mohanty et al., 2007), and modulating emotional response via strategies such as reappraisal (Banks et al., 2007).”
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“Overall, as stated in the Introduction, the DLPFC modulates emotional processing, both for stimuli identification and retrieval, and this is particularly true for the left hemisphere (Banks et al., 2007).”
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“The amygdala is integrated into a myriad of neural circuits, with strong reciprocal connections to the ventromedial prefrontal cortex, as well as the hippocampus (Banks et al. 2007).”
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Age and executive ability impact the neural correlates of race perception
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“Functional connections between the amygdala and regions of the PFC constitute a critical circuit for socioemotional processing (Banks et al. 2007; Phelps et al. 2004).”
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“…and right amygdalae were used as seed regions, in accordance with other studies on functional connectivity during emotion regulation in BD (e.g. Banks et al., 2007; Kanske et al., 2015; Morris et al., 2012; Townsend et al., 2013), given their key role in the processing of emotions (e.g.…”
MethodInfluentialSelf-citationTargeting VMPFC‐amygdala circuit with TMS in substance use disorder: A mechanistic framework
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CFC delta-beta is related with mixed features and response to treatment in bipolar II depression
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“The fMRI findings of the corticosubcortical coupling between the amygdala and the frontal cortex have been defined as the emotion regulation efficiency index (Banks et al., 2007).”
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“A growing body of evidence suggests that the mPFC is critical to emotional processing, including emotional arousal and personal salience (Banks et al., 2007; Phan et al., 2004), the integration of emotion–cognition interactions (Drevets, 2001; Ochsner and Gross, 2005), and the up-regulation and…”
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“Given the top-down regulatory influence of the PFC on the temporal lobe (Banks et al., 2007; Ghashghaei et al., 2007), the UF is implicated in regulating emotional responsivity to auditory and visual stimuli, as well as cognitive processes underlying emotion (Schmahmann et al.”
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“Gender: male, n (%) 15 (75) 18 (94) 5 (50) 18 (90) 10.”
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Mindfulness Induces Changes in Anterior Alpha Asymmetry in Healthy Older Adults
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A subcortical network for implicit visuo-spatial attention: Implications for Parkinson's Disease
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“They found that, in non-human primates, there are neurons within the Amg that are activated differently by the emotional context, based on the specific valence acquired through experience (e.g., dangerous vs. safe contexts).”
InfluentialNamkung, H., Thomas, K. L., Hall, J., & Sawa, A. (2021) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2021.12.025 · Cited by 17
Ladouceur, C. D., Henry, T. R., Ojha, A., Shirtcliff, E. A., & Silk, J. S. (2023) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2023.101236 · Cited by 18
“…given the regulatory role of the vmPFC on amygdala activity based on evidence from animal models (Quirk and Beer, 2006) and studies in adults (Banks et al., 2007), findings indicate that vmPFC-amygdala connectivity changes during adolescence and have been interpreted as reflecting increases…”
Mao, Y., Li, L., Li, Y., Hou, X., & Duan, S. (2023) · Biological Psychology · doi:10.1016/j.biopsycho.2023.108716 · Cited by 15
Neacsiu, A. D., Beynel, L., Gerlus, N., LaBar, K. S., Bukhari‐Parlakturk, N., & Rosenthal, M. Z. (2024) · Journal of Affective Disorders · doi:10.1016/j.jad.2024.01.120 · Cited by 18
“…with the dlPFC targeting) and other research shows contralateral connectivity tends to be strongest between limbic and prefrontal regions (Banks et al., 2007), and, finally, when affective processing is lateralized to one side of the insula, it tends to be the left side (Duerden et al.,…”
Amygdala fMRI—A Critical Appraisal of the Extant Literature
Varkevisser, T., Geuze, E., & van Honk, J. (2024) · Neuroscience Insights · doi:10.1177/26331055241270591 · Cited by 19
“In many of these studies, amygdala PPI was examined while participants were performing some form of emotion regulation training (eg, 100,104,105 ; see Berboth & Morawetz 106 for a meta-analysis).”
BackgroundPiel, J. H. A., Lett, T. A. P., Wackerhagen, C., Plichta, M. M., Mohnke, S., Grimm, O., Romanczuk‐Seiferth, N., Degenhardt, F., Tost, H., Witt, S. H., et al. (2018) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2017.12.014 · Cited by 15
Kjærstad, H. L., Damgaard, V., Knudsen, G. M., Vinberg, M., Kessing, L. V., Macoveanu, J., & Miskowiak, K. W. (2022) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2022.04.010 · Cited by 15
Neural mechanisms associated with reappraisal and attentional deployment
Ferri, J. M., & Hajcak, G. (2015) · Current Opinion in Psychology · doi:10.1016/j.copsyc.2015.01.010 · Cited by 20
“Greater coupling between the amygdala and prefrontal regions and the DMPFC has also been associated with reduced negative affect [27].”
Neuroimaging and facial affect processing: implications for traumatic brain injury
Neumann, D. M., Keiski, M. A., McDonald, B. C., & Wang, Y. (2013) · Brain Imaging and Behavior · doi:10.1007/s11682-013-9285-5 · Cited by 15
“Many of these regions in the brain are also involved in other higher aspects of social cognition and emotion regulation (Adolphs 2001; Banks et al. 2007).”
BackgroundPrincipal component analysis and neural predictors of emotion regulation
Klumpp, H., Bhaumik, R., Kinney, K. L., & Fitzgerald, J. M. (2017) · Behavioural Brain Research · doi:10.1016/j.bbr.2017.10.024 · Cited by 16
Functional connectome fingerprint of holistic–analytic cultural style
Luo, S., Zhu, Y., & Han, S. (2021) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nsab080 · Cited by 18
“Another explanation is that East Asians are more likely to regulate their emotions by suppressing their emotions (Matsumoto et al., 2008), and the AMYG contributes to emotion regulation (Hare et al., 2005; Banks et al., 2007; Frank et al., 2014).”
BackgroundAltered Cingulostriatal Coupling in Obsessive–Compulsive Disorder
Beucke, J. C., Kaufmann, C., Linnman, C., Grützmann, R., Endraß, T., Deckersbach, T., Dougherty, D. D., & Kathmann, N. (2012) · Brain Connectivity · doi:10.1089/brain.2012.0078 · Cited by 17
“In healthy individuals, PPIs have been applied to study amygdala–prefrontal interactions in the context of fear (Banks et al., 2007; Das et al., 2005; Williams et al., 2006), and periaqueductal gray connectivity during pain (Linnman et al., 2012) and defensive fear (Mobbs et al., 2009).”
van Dam, W. O., & Chrysikou, E. G. (2021) · Cognitive Affective & Behavioral Neuroscience · doi:10.3758/s13415-020-00830-4 · Cited by 16
Gerván, P., Bunford, N., Utczás, K., Tróznai, Z., Oláh, G., Szakács, H., Kriston, P., Gombos, F., & Kovács, I. (2022) · Journal of Pediatric Nursing · doi:10.1016/j.pedn.2022.08.017 · Cited by 17
“, 2003) and the frontolimbic system (Banks et al., 2007) implicated in emotion generation and regulation.”
Kaplun, A., Alperovitch‐Najenson, D., & Kalichman, L. (2021) · Current Pain and Headache Reports · doi:10.1007/s11916-021-00991-y · Cited by 14
Le, T. M., Malone, T., & Li, C. R. (2022) · Drug and Alcohol Dependence · doi:10.1016/j.drugalcdep.2021.109248 · Cited by 15
Dissociable Self Effects for Emotion Regulation: A Study of Chinese Major Depressive Outpatients
Wang, X., Feng, Z., Zhou, D., Lei, X., Liao, T., Zhang, L., Ji, B., & Li, J. (2014) · BioMed Research International · doi:10.1155/2014/390865 · Cited by 15
“correction for multiple comparisons [35].”
Cross, K. A., & Iacoboni, M. (2011) · Human Brain Mapping · doi:10.1002/hbm.21428 · Cited by 16
“Second, previous studies have used a similar strategy to examine potential targets of top-down control in a wide variety of tasks [Banks et al., 2007; Egner and Hirsch, 2005; Wolbers et al., 2006].”
MethodComment vaincre l’anxiété en situation extrême ?
Sala, G., & Haag, C. (2016) · Revue française de gestion · doi:10.3166/rfg.2016.00039 · Cited by 14
Abnormal fronto-limbic engagement in incarcerated stimulant users during moral processing
Fede, S. J., Harenski, C. L., Borg, J. S., Sinnott-Armstrong, W. P., Rao, V. R., Caldwell, B. M., Nyalakanti, P. K., Koenigs, M. R., Decety, J., Calhoun, V. D., et al. (2016) · Psychopharmacology · doi:10.1007/s00213-016-4344-4 · Cited by 16
“that the amygdala and ACC are functionally connected during emotion regulation (Banks et al. 2007), fear (Williams et al. 2006), and during resting state (Roy et al. 2009) as well as structurally connected by projections from the amygdala (JohansenBerg et al. 2008; Kim et al. 2011a, b).”
BackgroundEffective Connectivity Between Broca’s Area and Amygdala as a Mechanism of Top-Down Control in Worry
Guha, A., Spielberg, J. M., Lake, J. I., Popov, T. G., Heller, W., Yee, C. M., & Miller, G. A. (2019) · Clinical Psychological Science · doi:10.1177/2167702619867098 · Cited by 14
Smet, S. D., Baeken, C., Raedt, R. D., Pulopulos, M. M., Razza, L. B., Damme, S. V., Witte, S. D., Brunoni, A. R., & Vanderhasselt, M. (2021) · Clinical Neurophysiology · doi:10.1016/j.clinph.2021.01.025 · Cited by 13
Kilpatrick, L. A., Mayer, E. A., Labus, J. S., Gupta, A., Hamaguchi, T., Mizuno, T., Komuro, H., Kano, M., Kanazawa, M., Aoki, M., et al. (2015) · PLoS ONE · doi:10.1371/journal.pone.0123183 · Cited by 16
“In particular, prelimbic mPFC projections in rodents to the BLA are involved in fear renewal, whereas infralimbic mPFC projections to intercaleted cells, which in turn inhibit central nucleus of the amygdala (CeA) output, are involved in suppressing the expression of fear in response to an extinguished conditional sti…”
BackgroundDistinctive amygdala subregions involved in emotion-modulated Stroop interference
Han, H. J., Lee, K.-H., Kim, H. T., & Kim, H. (2013) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nst021 · Cited by 16
“, 2008) connectivity with the amygdala, and it appears to play a key role in the processing of integrating emotional signals that are conveyed through the amygdala and in the regulation of conflicts due to emotional distractors (Compton, 2003; Etkin et al., 2006; Banks et al., 2007; Egner et al., 2008).”
Galván, A., & Tottenham, N. (2016) · Wiley eBooks · doi:10.1002/9781119125556.devpsy218 · Cited by 14
Gerhardt, S., Berhe, O., Moessnang, C., Horning, M., Kiefer, F., Tost, H., & Vollstädt-Klein, S. (2022) · Addiction Biology · doi:10.1111/adb.13251 · Cited by 12
Effect of Phase Clustering Bias on Phase-Amplitude Coupling for Emotional EEG
Sheng, T., Feng, Q., Luo, Z., Zhao, S., Xu, M., Ming, D., Yan, Y., & Yin, E. (2024) · Journal of Integrative Neuroscience · doi:10.31083/j.jin2302033 · Cited by 13
“As the frontal lobe is associated with emotions [43], comodulograms of channels in the frontal lobe were averaged.”
BackgroundKaratayev, O., Collier, A. D., Targoff, S. R., & LEIBOWITZ, S. F. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25158341 · Cited by 18
“Nicotine use also has some sex-dependent effects, with female more than male smokers exhibiting a smaller gray matter volume in the amygdala involved in emotion regulation and stress mitigation [403], a finding suggesting that women smoke for different reasons than men [404].”
BackgroundDiagnostic value of structural, functional and effective connectivity in bipolar disorder
Gencheva, T. M., Valkov, B. V., Kandilarova, S., Maes, M. H. J., & Stoyanov, D. (2024) · Acta Psychiatrica Scandinavica · doi:10.1111/acps.13742 · Cited by 13
MEDIAL PREFRONTAL CORTEX AND COGNITIVE REGULATION
Nakao, T., Takezawa, T., Miyatani, M., & Ohira, H. (2009) · PSYCHOLOGIA · doi:10.2117/psysoc.2009.93 · Cited by 13
“Banks et al. (2007) reported that the strength of functional coupling between the amygdala and the MPFC predict successful emotion regulation.”
BackgroundBiology and American Sociology, Part II: Developing a Unique Evolutionary Sociology
Turner, J. H., Schutt, R. K., & Keshavan, M. S. (2020) · The American Sociologist · doi:10.1007/s12108-020-09448-y · Cited by 13
Transcranial Direct Current Stimulation (tDCS) in Anxiety Disorders
Vicario, C. M., Salehinejad, M. A., Avenanti, A., & Nitsche, M. A. (2020) · Springer eBooks · doi:10.1007/978-3-030-43356-7_21 · Cited by 13
“This pattern of results is in line with a model proposed in a recent systematic review of our group [14], where we suggested that the stimulation of both the left and right DLPFC with anodal and cathodal tDCS, respectively, might counteract maladaptive plasticity of the cortico-meso-limbic network [57] in anxiety diso…”
ResultHua, Y. Q., Li, M., Qiaoting, W. A. N. G., Feng, C., & Zhang, J. (2020) · Acta Psychologica Sinica · doi:10.3724/sp.j.1041.2020.01048 · Cited by 14
Neural correlates of emotional reactivity and regulation in traumatized North Korean refugees
Lee, K. H., Lee, H. Y., Park, I., Lee, Y. J., Kim, N., Jeon, S., Kim, S., Jeon, J. E., & Kim, S. J. (2021) · Translational Psychiatry · doi:10.1038/s41398-021-01579-1 · Cited by 15
Deng, K., Jin, W., Jiang, K., Li, Z., Im, H., Chen, S., Du, H., Guan, S., Ge, W. H., Wei, C., et al. (2023) · Behavioral and Brain Functions · doi:10.1186/s12993-023-00223-w · Cited by 13
“Both brain regions are known to be involved in emotional perception and regulation, with the top-down control network inhibiting amygdala reactivity to negative stimuli [7, 39, 77].”
BackgroundThe relationships between perceived control and episodic memory in adulthood: a review
Maggio, C., Soubelet, A., Faure, S., & Fort, I. (2018) · Aging Neuropsychology and Cognition · doi:10.1080/13825585.2017.1423022 · Cited by 12
Antonucci, L. A., Pergola, G., Passiatore, R., Taurisano, P., Quarto, T., Dispoto, E., Rampino, A., Bertolino, A., Cassibba, R., & Blasi, G. (2019) · European Archives of Psychiatry and Clinical Neuroscience · doi:10.1007/s00406-019-01062-5 · Cited by 12
Working memory load reduces the electrocortical processing of positive pictures
Barley, B. K., Bauer, E. A., Wilson, K., & MacNamara, A. (2021) · Cognitive, Affective, & Behavioral Neuroscience · doi:10.3758/s13415-021-00875-z · Cited by 13
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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