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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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Miller, E. K., & Cohen, J. D. (2001) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.24.1.167 · Cited by 12,803 · cited 2×
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“Reappraisal involves reinterpreting the meaning of an emotional event; for example, creating an alternative scenario or adopting a different attitude (Gross, 2002; Ochsner et al., 2004).”
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Wager, T. D., Davidson, M. L., Hughes, B. L., Lindquist, M. A., & Ochsner, K. N. (2008) · Neuron · doi:10.1016/j.neuron.2008.09.006 · Cited by 1,761 · cited 15×
“…amygdala and cEMG activity, and contrasts a more generic circuitry of reappraisal comprising lateral and dorsomedial regions (Kalisch, 2009) with the OFC-like regions usually found in individual difference analyses (Banks et al., 2007; Johnstone et al., 2007; Urry et al., 2006; Wager et al., 2008).”
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Thompson, R. A. (1994) · Monographs of the Society for Research in Child Development · doi:10.2307/1166137 · Cited by 1,366
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Banks, S. J., Eddy, K. T., Angstadt, M., Nathan, P. J., & Phan, K. L. (2007) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nsm029 · Cited by 1,187 · cited 10×
“…amygdala and cEMG activity, and contrasts a more generic circuitry of reappraisal comprising lateral and dorsomedial regions (Kalisch, 2009) with the OFC-like regions usually found in individual difference analyses (Banks et al., 2007; Johnstone et al., 2007; Urry et al., 2006; Wager et al., 2008).”
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“In Session 2, consistent with prior reports (Eippert et al., 2007; Ochsner et al., 2004; Urry et al., 2006; van Reekum et al., 2007), amygdala activationwasmodulated by the regulation instructions (enhance>maintain>suppress;”
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“…amygdala and cEMG activity, and contrasts a more generic circuitry of reappraisal comprising lateral and dorsomedial regions (Kalisch, 2009) with the OFC-like regions usually found in individual difference analyses (Banks et al., 2007; Johnstone et al., 2007; Urry et al., 2006; Wager et al., 2008).”
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“There are two plausible explanations: First, given prior finding that men show lower cEMG activity to negative pictures as compared to women (Bradley et al., 2001), our male-only sample might have a more limited range to increase cEMG activity above and beyond that already activated in response to…”
BackgroundInfluentialGender Differences in Emotion Regulation: An fMRI Study of Cognitive Reappraisal
McRae, K., Ochsner, K. N., Mauss, I. B., Gabrieli, J. J. D., & Gross, J. J. (2008) · Group Processes & Intergroup Relations · doi:10.1177/1368430207088035 · Cited by 910 · cited 1×
“…that emotion (Phelps and LeDoux, 2005), the PFC provides top-down control, such as inhibiting proponent responses, maintaining affective goals, and recruiting further resources (Miller and Cohen, 2001), that steers and potentially modifies activation in subcortical circuitry including the amygdala.”
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“…activity in the resolution of emotional conflicts (Egner et al., 2008; Etkin et al., 2006); OFC, through its extensive anatomical connections (Ghashghaei and Barbas 2002; Ongur and Price 2000), modulates the amygdala in the reappraisal of contextual value (Dolan, 2007); and lateral and…”
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Delgado, M. R., Nearing, K. I., LeDoux, J. E., & Phelps, E. A. (2008) · Neuron · doi:10.1016/j.neuron.2008.06.029 · Cited by 716
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Affective neuroscience and psychophysiology: Toward a synthesis
Davidson, R. J. (2003) · Psychophysiology · doi:10.1111/1469-8986.00067 · Cited by 535 · cited 2×
“Individual Differences in Emotion Regulation 19 In sum, this study complements and extends the extant group-based research by adopting a rigorous individual-differences approach (Braver et al., 2010; Kosslyn et al., 2002) and integrating psychophysiology and neuroimaging (Davidson, 2003).”
BackgroundResultSelf-citationDissociable Neural Systems Resolve Conflict from Emotional versus Nonemotional Distracters
Egner, T., Etkin, A., Gale, S. A., & Hirsch, J. (2007) · Cerebral Cortex · doi:10.1093/cercor/bhm179 · Cited by 521 · cited 2×
“…have previously been shown to exert regulatory influences on the amygdala—pgACC inhibits amygdala activity in the resolution of emotional conflicts (Egner et al., 2008; Etkin et al., 2006); OFC, through its extensive anatomical connections (Ghashghaei and Barbas 2002; Ongur and Price 2000),…”
BackgroundIndividual differences in emotion processing
Hamann, S. B., & Canli, T. (2004) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2004.03.010 · Cited by 489 · cited 1×
“In the domain of emotion, however, variation across individuals is the rule rather than the exception (Hamann and Canli, 2004), and such individual differences in the capacity to regulate negative emotion may determine vulnerability and resilience in the face of adversity (Davidson, 2004).”
BackgroundSuppression and enhancement of emotional responses to unpleasant pictures
Jackson, D. C., Malmstadt, J. R., Larson, C. L., & Davidson, R. J. (2000) · Psychophysiology · doi:10.1111/1469-8986.3740515 · Cited by 459 · cited 7×
“3 The terms ―enhance,‖ ―maintain‖ and ―suppress‖ were used based on prior instructions by Jackson et al. (2000).”
BackgroundResultInfluentialSelf-citationWell–being and affective style: neural substrates and biobehavioural correlates
Davidson, R. J. (2004) · Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences · doi:10.1098/rstb.2004.1510 · Cited by 446
Self-citationRegulation of emotional responses elicited by threat-related stimuli
Eippert, F., Veit, R., Weiskopf, N., Erb, M., Birbaumer, N., & Anders, S. (2007) · Human Brain Mapping · doi:10.1002/hbm.20291 · Cited by 419 · cited 5×
“In Session 2, consistent with prior reports (Eippert et al., 2007; Ochsner et al., 2004; Urry et al., 2006; van Reekum et al., 2007), amygdala activationwasmodulated by the regulation instructions (enhance>maintain>suppress;”
BackgroundMethodResultInfluentialThe functional neuroanatomy of reappraisal: Time matters
Kalisch, R. (2009) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2009.06.003 · Cited by 379 · cited 3×
“Over the past decade, neuroimaging studies of reappraisal have revealed converging evidence that reappraisal engages sectors of the prefrontal cortex (PFC) and subcortical structures such as the amygdala (for a meta-analysis, see Kalisch, 2009).”
BackgroundResultInfluentialEmotion Induction After Direct Intracerebral Stimulations of Human Amygdala
Lanteaume, L., Khalfa, S., Régis, J. M., Marquis, P., Chauvel, P., & Bartoloméi, F. (2006) · Cerebral Cortex · doi:10.1093/cercor/bhl041 · Cited by 332 · cited 2×
“, 2001a), and is increased by direct intracerebral stimulation of the human amygdala (Lanteaume et al., 2007).”
BackgroundMotion correction and the use of motion covariates in multiple‐subject fMRI analysis
Johnstone, T., Walsh, K. S. O., Greischar, L. L., Alexander, A. L., Fox, A. S., Davidson, R. J., & Oakes, T. R. (2006) · Human Brain Mapping · doi:10.1002/hbm.20219 · Cited by 326 · cited 2×
“Single-subject GLM included separate regressors for each regulation condition (negative pictures: enhance, maintain, suppress, and neutral pictures: maintain) to estimate hemodynamic response functions (HRFs; modeled by a set of tent basis functions), six motion estimate covariates (Johnstone et al., 2006), and a seco…”
BackgroundMethodSelf-citationSiegle, G. J., Ichikawa, N., & Steinhauer, S. R. (2008) · Psychophysiology · doi:10.1111/j.1469-8986.2008.00681.x · Cited by 317 · cited 1×
“In addition, pupil dilation was concurrently measured as an index of cognitive demand to ascertain the paradigm validity (Siegle et al., 2008).”
MethodBoxtel, A. V. (2001) · Psychophysiology · doi:10.1111/1469-8986.3810022 · Cited by 304
Amygdala Volume and Nonverbal Social Impairment in Adolescent and Adult Males With Autism
Nacewicz, B. M., Dalton, K. M., Johnstone, T., Long, M. T., McAuliff, E. M., Oakes, T. R., Alexander, A. L., & Davidson, R. J. (2006) · Archives of General Psychiatry · doi:10.1001/archpsyc.63.12.1417 · Cited by 302
Self-citationvan Reekum, C. M., Johnstone, T., Urry, H. L., Thurow, M. E., Schaefer, H. S., Alexander, A. L., & Davidson, R. J. (2007) · NeuroImage · doi:10.1016/j.neuroimage.2007.03.052 · Cited by 271
Self-citationFrewen, P., Dozois, D. J. A., & Lanius, R. A. (2007) · Clinical Psychology Review · doi:10.1016/j.cpr.2007.05.002 · Cited by 260 · cited 2×
“It is the basis of cognitive therapy (Frewen et al., 2008), has been found to be more beneficial than suppressing emotions (Ochsner et al.”
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Ray, R. D., McRae, K., Ochsner, K. N., & Gross, J. J. (2010) · Emotion · doi:10.1037/a0019015 · Cited by 256 · cited 3×
“Furthermore, cEMG activity has been shown to be systematically modulated by regulation instructions (Jackson et al., 2000; Lee et al., 2009; Ray et al., 2010), such that cEMG magnitude increases and decreases in accordance with instructions to amplify or attenuate negative emotion, respectively.”
BackgroundResultInfluentialBridging psychology and biology: the analysis of individuals in groups.
Kosslyn, S. M., Cacioppo, J. T., Davidson, R. J., Hugdahl, K., Lovallo, W. R., Spiegel, D., & Rose, R. (2002) · American Psychologist · doi:10.1037/0003-066x.57.5.341 · Cited by 196 · cited 3×
“In sum, this study complements and extends the extant group-based research by adopting a rigorous individual-difference approach (Braver et al., 2010; Kosslyn et al., 2002) and integrating psychophysiology and neuroimaging (Davidson, 2003).”
BackgroundResultSelf-citationUrry, H. L., van Reekum, C. M., Johnstone, T., & Davidson, R. J. (2009) · NeuroImage · doi:10.1016/j.neuroimage.2009.05.069 · Cited by 196 · cited 2×
“…an index of regulatory success (Ochsner et al., 2002; Wager et al., 2008), or used measures reflecting non-specific arousal or effort such as eye-blink startle (Eippert et al., 2007), pupil dilation (Johnstone et al., 2007; Urry et al., 2009), and skin conductance response (Delgado et al., 2008).”
BackgroundMethodSelf-citationNeural correlates of emotion regulation in psychopathology
Taylor, S. F., & Liberzon, I. (2007) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2007.08.006 · Cited by 186 · cited 4×
“…et al., 2007; Ochsner et al., 2002; Urry et al., 2006; Wager et al., 2008) and affective disorders (Johnstone et al., 2007; Phillips et al., 2008; Taylor and Liberzon 2007), we specifically interrogated the amygdala-PFC circuit to examine whether amygdala-PFC functional connectivity was…”
BackgroundMethodInfluentialFear Is Fast in Phobic Individuals: Amygdala Activation in Response to Fear-Relevant Stimuli
Larson, C. L., Schaefer, H. S., Siegle, G. J., Jackson, C. A., Anderle, M. J., & Davidson, R. J. (2006) · Biological Psychiatry · doi:10.1016/j.biopsych.2006.03.079 · Cited by 156 · cited 1×
“We attempted to control for variance occurring prior to the instruction cue, such as the marked variable time to onset in the amygdala following an emotional stimulus (e.g., Larson et al., 2006), so as to obtain a more accurate estimate of the ―regulation effect‖ which was our main interest.”
MethodSelf-citationThe human amygdala and orbital prefrontal cortex in behavioural regulation
Dolan, R. J. (2007) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2007.2088 · Cited by 150 · cited 2×
“, 2006); OFC, through its extensive anatomical connections (Ghashghaei and Barbas, 2002; Ongur and Price, 2000), modulates the amygdala in the reappraisal of contextual value (Dolan, 2007); and lateral and dorsal PFC regions have also been found to influence amygdala function, possibly mediated via the OFC/vmPFC, in r…”
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“In the first session, EMG sensors were placed on the corrugator supercilii muscle (Tassinary et al., 1989), and 6 negative and 4 neutral pictures were presented to familiarize participants with the protocol.”
MethodVive les differences! Individual variation in neural mechanisms of executive control
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“In sum, this study complements and extends the extant group-based research by adopting a rigorous individual-difference approach (Braver et al., 2010; Kosslyn et al., 2002) and integrating psychophysiology and neuroimaging (Davidson, 2003).”
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“The use of subjective self-report measures of regulatory success can also be problematic because of demand characteristics and other biases such as inaccurate recall that plague the validity of such measures (Davidson, 1992).”
BackgroundSelf-citationStartle modulation before, during and after exposure to emotional stimuli
Dichter, G. S., Tomarken, A. J., & Baucom, B. (2002) · International Journal of Psychophysiology · doi:10.1016/s0167-8760(01)00170-2 · Cited by 80
Test‐retest reliability of voluntary emotion regulation
Lee, H., Shackman, A. J., Jackson, D. C., & Davidson, R. J. (2009) · Psychophysiology · doi:10.1111/j.1469-8986.2009.00830.x · Cited by 56 · cited 10×
“…5.30 ± 0.93; set 2: valence, 2.98 ± 0.69, arousal, 5.29 ± 0.91) and 42 neutral pictures (set 1: valence, 5.02 ± 0.36, arousal, 2.75 ± 0.57; set 2: valence, 5.04 ± 0.47, arousal, 2.81 ± 0.50) 2 were matched on valence and 1 This finding was assessed with eyeblink startle EMG (Lee et al., 2009).”
BackgroundMethodResultInfluentialSelf-citationAmygdalar Function Reflects Common Individual Differences in Emotion and Pain Regulation Success
Lapate, R. C., Lee, H., Salomons, T. V., van Reekum, C. M., Greischar, L. L., & Davidson, R. J. (2011) · Journal of Cognitive Neuroscience · doi:10.1162/jocn_a_00125 · Cited by 56 · cited 2×
“We focused on the amygdala as a downstream target region of regulatory efforts for its activity has consistently been found to covary with regulatory goal (e.g., Eippert et al., 2007; Lapate et al., 2012; Ochsner et al., 2004; Urry et al., 2006; van Reekum et al., 2007).”
BackgroundSelf-citationMental Health Services: A Public Health Perspective
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The Epidemiology of Adult Mental Disorders
Kessler, R. C., Koretz, D. S., Merikangas, K. R., & Wang, P. S. (2004) · doi:10.1093/oso/9780195153958.003.0008 · Cited by 4
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“, 2012), and the strength of these functional connections has predicted emotional behaviors of healthy adults (Banks et al., 2007; Lee et al., 2012).”
Kral, T. R. A., Schuyler, B. S., Mumford, J. A., Rosenkranz, M. A., Lutz, A., & Davidson, R. J. (2018) · NeuroImage · doi:10.1016/j.neuroimage.2018.07.013 · Cited by 326
“, 2006), possibly through functional coupling with the amygdala (Banks et al., 2007; Lee et al., 2012).”
Self-citationStress and the adolescent brain
Tottenham, N., & Galván, A. (2016) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2016.07.030 · Cited by 324
“This pattern is more typical of healthy adults (e.g., Lee et al., 2012), suggesting an acceleration or temporary enhancement of function during development.”
The prefrontal cortex, pathological anxiety, and anxiety disorders
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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
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
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