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Emotion, plasticity, context, and regulation: Perspectives from affective neuroscience.
Abstract
The authors present an overview of the neural bases of emotion. They underscore the role of the prefrontal cortex (PFC) and amygdala in 2 broad approach- and withdrawal-related emotion systems. Components and measures of affective style are identified. Emphasis is given to affective chronometry and a role for the PFC in this process is proposed. Plasticity in the central circuitry of emotion is considered, and implications of data showing experience-induced changes in the hippocampus for understanding psychopathology and stress-related symptoms are discussed. Two key forms of affective plasticity are described--context and regulation. A role for the hippocampus in context-dependent normal and dysfunctional emotional responding is proposed. Finally, implications of these data for understanding the impact on neural circuitry of interventions to promote positive affect and on mechanisms that govern health and disease are considered.
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“Second, the time course of emotional reactions (“affective chronometry”) has been recently highlighted as important in the study of depression (Davidson, 2003; Davidson, Jackson, & Kalin, 2000).”
From Mindfulness-Based Cognitive Therapy Improves Emotional Reactivity to Social Stress: Results from a Randomized Controlled Trial (2012) · cites this paper as Davidson, Jackson, & Kalin, 2000
In the citing paper
“Given that positive and negative affect arise from partially distinct biobehavioral systems57, 58”
From Upregulating the positive affect system in anxiety and depression: Outcomes of a positive activity intervention: Taylor et al. (2017) · cites this paper as [58]
In the citing paper
“positive and negative emotions arise from at least partially distinct biobehavioral systems”
From The affective tie that binds: Examining the contribution of positive emotions and anxiety to relationship formation in social anxiety disorder (2017) · cites this paper as Davidson, Jackson, & Kalin, 2000
In the citing paper
“negative emotions (e.g., anxiety) and positive emotions are regulated by partially distinct biobehavioral systems (Davidson et al., 2000; Gable & Berkman, 2008)”
From The affective tie that binds: Examining the contribution of positive emotions and anxiety to relationship formation in social anxiety disorder (2017) · cites this paper as Davidson et al., 2000
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“Moreover, such asymmetries reflect both state and trait components (32, 33) with both phasic positive mood as well as dispositional positive affect associated with greater relative left-sided anterior activation.”
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“Reflecting a core motivational construct (e.g., Davidson et al. 2000), the approach-avoidance continuum maps easily onto broader theories of biobehavioral functioning.”
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“Over-excitation and deprivation can influence the affective system and may induce changes in the emotional circuitry of the brain that can contribute to stress-related psychopathology ( Davidson, Jackson, & Kalin, 2000 ).”
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“…on EEG measures of prefrontal asymmetry (Coan, 2003), we have suggested that environmental influences, particularly early in development, are likely to be present and to shape aspects of prefrontal function, including baseline measures of functional prefrontal asymmetry (Davidson et al., 2000a).”
BackgroundSelf-citationEmotion Regulation Flexibility
Aldao, A., Sheppes, G., & Gross, J. J. (2015) · Cognitive Therapy and Research · doi:10.1007/s10608-014-9662-4 · Cited by 981
“This conceptualization of ER flexibility draws upon basic research on affective chronometry (e.g., Thompson 1994; Gross 1998, 2013; Davidson et al. 2000; Sheppes and Gross 2011) and motivation (e.g., Bradley and Lang 2000; Magen and Gross 2010) as well as on the burgeoning literature on affective…”
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“Dysfunctions in this neural circuit may lead to susceptibility to depression and violence (Davidson, Jackson, & Kalin, 2000; Davidson, Putnam, & Larson, 2000) and therefore undermine successful cognitive functioning.”
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“More specifically, no one has ever convincingly presented coherent facial, vocal, gestural, physiological, or cerebral indexes that approximate a 1:1 relation to an emotional state ( Davidson, Jackson, & Kalin, 2000 ).”
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“Similar interaction might also sometimes occur in the reverse direction, when core processes of emotion are subject to voluntary regulation by cognitive systems (Davidson et al., 2000).”
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“This approach-avoidance continuum also reflects a fundamental motivational construct (Carver & Scheier 1998, Davidson et al. 2000).”
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“Electroencephalographic (EEG) and neuroimaging data indicate that approach of incentives tends to relate to higher relative activation in areas of the left prefrontal cerebral cortex, suggesting that the circuitry underlying approach is partially localized in these areas (e.g., Harmon-Jones & Allen, 1997; Sobotka, Dav…”
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“A related, older methodology involves exposing participants to various ‘‘threats’’ such as a painful injection (Schachter, 1959), a difficult intelligence test (Braunstein-Bercovitz et al., 2001), electric shock (Cornelius and Averill, 1980), or speaking in public (Davidson et al., 2000b).”
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“To index the alpha power unique to each site, we regressed mean whole-head power from the alpha power for each individual site (see Davidson, Jackson, & Larson, 2000, for description of the method).”
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“Affect identification is the only test in this battery that measures social cognition, a domain of increased interest in behavioral neuroscience (Davidson et al., 2000).”
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“A second model has posited that the left frontal cortical region is involved in the experience and expression of approach-related emotions and that the right frontal cortical region is involved in experience and expression of withdrawal-related emotions ( Davidson, Jackson, & Kalin, 2000; Fox, 1991; Harmon-Jones & All…”
BackgroundFeelings change: Accounting for individual differences in the temporal dynamics of affect.
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“Lesions to the hippocampus abolish this context-dependent form of memory but have no effect on learning cue-punishment contingencies [109].”
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“Our focus was on power in the alpha band (8–13 Hz), though we extracted power in all frequency bands (for methodological discussions, see Davidson, Chapman, Chapman, & Henriques, 1990; Davidson, Jackson, & Larson, 2000 ).”
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“Contemporary views of motivation similarly emphasize approach and avoidance systems motivated by positive and negative affect (Carver, 2001; Davidson, Jackson, & Kalin, 2000).”
BackgroundThe neurobiology of positive emotions
Burgdorf, J., & Panksepp, J. (2006) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2005.06.001 · Cited by 677
“Approach based psychometric models of positive emotion have also been used to conceptualize stable PA traits states such as subjective well-being (Davidson et al., 2000; Panksepp et al., 2002) as well as the personality trait of extroversion which is associated with high levels of PA (Diener, 1998).”
MethodFrom emotion perception to emotion experience: Emotions evoked by pictures and classical music
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“The increased cortical activation at posterior clusters (measured at left- and rightsided occipital and parietal electrodes) in the combined conditions compared to the picture conditions is in line with findings from neuroimaging and electrophysiological studies showing that this part of the cortex is implicated in th…”
BackgroundResultInfluentialPerfusion functional MRI reveals cerebral blood flow pattern under psychological stress
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The neural substrates of affective processing in depressed patients treated with venlafaxine
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Self-citationInvestment behavior and the negative side of emotion
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“…15 target patients with chronic and stable focal lesions in specific components of a neural circuitry that has been shown to be critical for the processing of emotions (Damasio, 1994; Davidson et al., 2000; Dolan, 2002; LeDoux, 1996; Rahman et al., 2001; Sanfey, Hastie, Colvin, & Grafman, 2003).”
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“A wealth of evidence for structural plasticity in frontal and hippocampal regions due to environmental enrichment comes from research on animals (Davidson et al., 2000; Diamond, 2001; Kempermann et al., 2002).”
BackgroundFrom emotion resonance to empathic understanding: A social developmental neuroscience account
Decety, J., & Meyer, M. (2008) · Development and Psychopathology · doi:10.1017/s0954579408000503 · Cited by 597
“Davidson, Jackson, and Kalin (2000) have proposed that the mechanism underlying suppression of negative emotion is via an inhibitory connection from regions of the PFC to the amygdala.”
BackgroundCompetencies as a behavioral approach to emotional intelligence
Boyatzis, R. E. (2009) · Journal of Management Development · doi:10.1108/02621710910987647 · Cited by 533
Complex affect dynamics add limited information to the prediction of psychological well-being.
Dejonckheere, E., Mestdagh, M., Houben, M., Rutten, I., Sels, L., Kuppens, P., & Tuerlinckx, F. (2019) · Nature Human Behaviour · doi:10.1038/s41562-019-0555-0 · Cited by 431
Siegle, G. J., Ghinassi, F., & Thase, M. E. (2007) · Cognitive Therapy and Research · doi:10.1007/s10608-006-9118-6 · Cited by 444
“The DLPFC has thus been implicated in emotion regulation (e.g., Davidson et al., 2000), and activates during tasks requiring conscious emotion regulation (e.g., Ochsner et al., 2004).”
BackgroundRubia, K. (2011) · Biological Psychiatry · doi:10.1016/j.biopsych.2010.09.023 · Cited by 440
“Together with ventromedial frontal cortex, including anterior cingulate, they mediate top-down affect regulation in their interconnection to underlying limbic areas (61,62,65,66).”
BackgroundGender difference in neural response to psychological stress
Wang, J., Korczykowski, M., Rao, H., Yong Fan, A., Pluta, J. B., Gur, R. C., McEwen, B. S., & Detre, J. A. (2007) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nsm018 · Cited by 447
“This hypothesis has several implications for the present study.”
BackgroundMethodFunctional neuroimaging studies of human emotions
Phan, K. L., Wager, T. D., Taylor, S. F., & Liberzon, I. (2004) · CNS Spectrums · doi:10.1017/s1092852900009196 · Cited by 433
“The medial prefrontal cortex has been hypothesized to have specific roles for emotion-related decision making(6) and emotional self-regulation.(7) The insula is thought of as the brain's "alarm center," integrating internal somatic cues with emotional experience,(8) and has been linked specifically to disgust.”
BackgroundLengua, L. J., Honorado, E., & Bush, N. R. (2006) · Journal of Applied Developmental Psychology · doi:10.1016/j.appdev.2006.10.001 · Cited by 426
Carver, C. S. (2005) · Personality and Social Psychology Review · doi:10.1207/s15327957pspr0904_2 · Cited by 442
“For example, as was noted earlier, there is evidence that experiences consistent with approach and positive affect are associated with relatively greater activation of left anterior cortical areas and that experiences consistent with avoidance and distress are associated with relatively greater activation of right ant…”
BackgroundCoping Through Emotional Approach: A New Look at Emotion, Coping, and Health‐Related Outcomes
Austenfeld, J. L., & Stanton, A. L. (2004) · Journal of Personality · doi:10.1111/j.1467-6494.2004.00299.x · Cited by 419
Neural and behavioral substrates of mood and mood regulation
Davidson, R. J., Lewis, D. A., Alloy, L. B., Amaral, D. G., Bush, G., Cohen, J. D., Drevets, W. C., Farah, M. J., Kagan, J., McClelland, J. L., et al. (2002) · Biological Psychiatry · doi:10.1016/s0006-3223(02)01458-0 · Cited by 411
Self-citationLearning to BREATHE: A Pilot Trial of a Mindfulness Curriculum for Adolescents
Broderick, P. C., & Metz, S. (2009) · Advances in School Mental Health Promotion · doi:10.1080/1754730x.2009.9715696 · Cited by 409
“Specific skills of emotion regulation might include awareness of emotional experience, identification of specific emotions and their intensity, constructive emotional expression, and distress tolerance (Cole et al, 2004; Davidson et al, 2000; Thompson, 1994).”
BackgroundThe Role of the Central Nucleus of the Amygdala in Mediating Fear and Anxiety in the Primate
Kalin, N. H., Shelton, S. E., & Davidson, R. J. (2004) · The Journal of Neuroscience · doi:10.1523/jneurosci.0292-04.2004 · Cited by 406
“, 1992; Fuster, 1997), and evidence suggests that these structures are an important part of the circuitry involved in regulation of emotion in humans (Davidson et al., 2000).”
BackgroundSelf-citationEcstasy and Agony: Activation of the Human Amygdala in Positive and Negative Emotion
Hamann, S. B., Ely, T. D., Hoffman, J. M., & Kilts, C. D. (2002) · Psychological Science · doi:10.1111/1467-9280.00425 · Cited by 406
“Consistent with this view, the human amygdala’s role in negative emotion has been amply demonstrated by a wealth of data from a range of methods and domains (see Aggleton, 2000, and Davidson et al., 2000, for reviews), but little evidence exists for a corresponding role in positive emotion.”
BackgroundFixing our focus: Training attention to regulate emotion
Wadlinger, H. A., & Isaacowitz, D. M. (2011) · Personality and Social Psychology Review · doi:10.1177/1088868310365565 · Cited by 396
“…left anterior cortical activation increase in MBSR participants may indicate emotion regulatory processes are taking place as activation in this area is correlated with positive emotional expression and higher levels of dispositional positive affect (R. J. Davidson et al., 2000; Urry et al., 2004).”
BackgroundFacial expressions and complex IAPS pictures: Common and differential networks
Britton, J. C., Taylor, S. F., Sudheimer, K. D., & Liberzon, I. (2006) · NeuroImage · doi:10.1016/j.neuroimage.2005.12.050 · Cited by 425
“, 1997a), and medial prefrontal activation reflecting emotion regulation (Davidson et al., 2000)).”
BackgroundDeveloping Sustainable Leaders Through Coaching and Compassion
Boyatzis, R. E., Smith, M. L., & Blaize, N. (2006) · Academy of Management Learning & Education · doi:10.5465/amle.2006.20388381 · Cited by 389
Linking Students’ Emotions and Academic Achievement: When and Why Emotions Matter
Valiente, C., Swanson, J., & Eisenberg, N. (2011) · Child Development Perspectives · doi:10.1111/j.1750-8606.2011.00192.x · Cited by 466
“If a consistently sad or anxious student continually withdraws from aversive stimuli (such as negative experiences while participating in learning groups), he or she is likely to miss out on the benefits of working with peers (Davidson et al., 2000).”
BackgroundAllostasis and the human brain: Integrating models of stress from the social and life sciences.
Ganzel, B. L., Morris, P., & Wethington, E. (2010) · Psychological Review · doi:10.1037/a0017773 · Cited by 415
“Further, this control is primarily localized within a limited number of brain regions that function together as a neural circuit or set of interconnected circuits (see below; e.g., Davidson et al., 2000; Gregg & Siegel, 2001; Ishai.”
Amir, N., Elias, J., Klumpp, H., & Przeworski, A. (2003) · Behaviour Research and Therapy · doi:10.1016/s0005-7967(03)00039-1 · Cited by 406
Guyer, A. E., Lau, J. Y. F., McClure-Tone, E. B., Parrish, J., Shiffrin, N. D., Reynolds, R. C., Chen, G., Blair, R. J. R., Leibenluft, E., Fox, N. A., et al. (2008) · Archives of General Psychiatry · doi:10.1001/archpsyc.65.11.1303 · Cited by 371
Control Processes and Self-Organization as Complementary Principles Underlying Behavior
Carver, C. S., & Scheier, M. F. (2002) · Personality and Social Psychology Review · doi:10.1207/s15327957pspr0604_05 · Cited by 388
“It is interesting, however, that the general sense of these ideas is echoed in a family of neurobiological motive theories that currently are receiving considerable attention from personality and social psychologists (e.g., Cloninger, 1998; Davidson, 1998; Davidson, Jackson, & Kalin, 2000; Depue & Collins, 1999; Depue…”
BackgroundJackson, D. C., Mueller, C. J., Dolski, I., Dalton, K. M., Nitschke, J. B., Urry, H. L., Rosenkranz, M. A., Ryff, C. D., Singer, B. H., & Davidson, R. J. (2003) · Psychological Science · doi:10.1046/j.0956-7976.2003.psci_1473.x · Cited by 368
Self-citationShort-term emotion assessment in a recall paradigm
Chanel, G., Kierkels, J. J. M., Soleymani, M., & Pun, T. (2009) · International Journal of Human-Computer Studies · doi:10.1016/j.ijhcs.2009.03.005 · Cited by 367
“It has been shown that correlates of emotions can be observed from brain activity, especially in the pre-frontal cortex and the amygdala (Adolphs et al., 2003; Damasio et al., 2000; Davidson, 2003; Davidson et al., 2000; Rolls, 2000).”
BackgroundRottenberg, J. A., Kasch, K. L., Gross, J. J., & Gotlib, I. H. (2002) · Emotion · doi:10.1037/1528-3542.2.2.135 · Cited by 360
“…compared with nondepressed controls, depressed individuals have been found to exhibit less positive expressive behavior in response to pleasant film and pleasant drink stimuli (Berenbaum & Oltmanns, 1992) and to be less behaviorally responsive to reward contingencies (Henriques & Davidson, 2000).”
BackgroundTHE SIMILARITY-IN-TOPOGRAPHY PRINCIPLE: RECONCILING THEORIES OF CONCEPTUAL DEFICITS
Simmons, W. K., & Barsalou, L. W. (2003) · Cognitive Neuropsychology · doi:10.1080/02643290342000032 · Cited by 359
“Following A. R. Damasio’s (1994) somatic marker theory, various researchers have similarly found that orbito-frontal cortex integrates emotional and conceptual information (e.g., Davidson, 2000; Davidson, Jackson, & Kalin, 2000 ).”
MethodDambrun, M., & Ricard, M. (2011) · Review of General Psychology · doi:10.1037/a0023059 · Cited by 390
“According to Donahue (1985), the latter is a “religion of comfort and social convention, a self-serving, instrumental approach shaped to suit oneself” (p.”
BackgroundHippocampus and Amygdala Morphology in Attention-Deficit/Hyperactivity Disorder
Plessen, K. J., Bansal, R., Zhu, H., Whiteman, R., Amat, J., Quackenbush, G. A., Martin, L., Durkin, K., Blair, C., Royal, J., et al. (2006) · Archives of General Psychiatry · doi:10.1001/archpsyc.63.7.795 · Cited by 347
Panksepp, J. (2003) · Brain and Cognition · doi:10.1016/s0278-2626(03)00003-4 · Cited by 346
Loewenstein, G. F., Rick, S. I., & Cohen, J. D. (2007) · Annual Review of Psychology · doi:10.1146/annurev.psych.59.103006.093710 · Cited by 373
Dandeneau, S. D., Baldwin, M. W., Baccus, J. R., Sakellaropoulo, M., & Pruessner, J. C. (2007) · Journal of Personality and Social Psychology · doi:10.1037/0022-3514.93.4.651 · Cited by 341
Metadata
- Authors
- Davidson, R. J., Jackson, D. C., & Kalin, N. H.
- Affiliations
- University of Wisconsin System (US)
- Venue
- Psychological Bulletin
- Published
- 2000-11
- Volume
- 126
- Issue
- 6
- Pages
- 890-909
- ISSN
- 0033-2909 (ISSN-L)
- 1939-1455
- OpenAlex
- W2045914666
- Cited by
- 1,322
- References
- 228
- Citations by year
- 2026: 17 · 2025: 30 · 2024: 32 · 2023: 30 · 2022: 34 · 2021: 50 · 2020: 54 · 2019: 51 · 2018: 36 · 2017: 59 · 2016: 57 · 2015: 62 · 2014: 51 · 2013: 59 · 2012: 66
- FWCI
- 18.99
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Psychological Bulletin (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health (5r01mh040747-14, 5r01mh046792-04)
- National Institute of Mental Health (MH40747, MH 43454, MH46792)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Keywords
- prefrontal cortex, amygdala, affective style, hippocampus, emotion regulation, psychopathology, stress, neural circuits
- MeSH terms
- Affect, Affective Symptoms, Animals, Brain, Brain Mapping, Emotions, Humans, Neuronal Plasticity, Neurosciences, Social Environment
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