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Event-Related Activation in the Human Amygdala Associates with Later Memory for Individual Emotional Experience
Open accessAbstract
The role of the amygdala in enhancing declarative memory for emotional experiences has been investigated in a number of animal, patient, and brain imaging studies. Brain imaging studies, in particular, have found a correlation between amygdala activation during encoding and subsequent memory. Because of the design of these studies, it is unknown whether this correlation is based on individual differences between participants or within-subject variations in moment-to-moment amygdala activation related to individual stimuli. In this study, participants saw neutral and negative scenes and indicated how emotionally intense they found each scene. Separate functional magnetic resonance imaging responses in the amygdala for each scene were related to the participants' report of their experience at study and to performance in an unexpected memory test 3 weeks after scanning. The amygdala had the greatest response to scenes rated as most emotionally intense. The degree of activity in the left amygdala during encoding was predictive of subsequent memory only for scenes rated as most emotionally intense. These findings support the view that amygdala activation reflects moment-to-moment subjective emotional experience and that this activation enhances memory in relation to the emotional intensity of an experience.
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“Furthermore, prior work shows that amygdala responses track affective intensity, especially for aversive stimuli like those photos used widely in reappraisal studies (Canli et al. 2000;Williams et al. 2001;Anderson et al. 2003;Cunningham et al. 2004;Ochsner et al. 2004Ochsner et al. , 2009;;Phan et al. 2004).”
From Cognitive Reappraisal of Emotion: A Meta-Analysis of Human Neuroimaging Studies (2014) · cites this paper as Canli et al. 2000
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“Canli et al. (2000) reported that amygdala response to emotionally intense negative scenes was predictive of subsequent recall.”
From Affective Cognition and its Disruption in Mood Disorders (2011) · cites this paper as Canli et al. (2000)
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“Considerable research has shown that interactions between the amygdala and hippocampus enhance encoding and consolidation of emotionally arousing information (Cahill 2000;Canli et al. 2000;Packard and Cahill 2001;Phelps 2004).”
From Stress administered prior to encoding impairs neutral but enhances emotional long-term episodic memories. (2007) · cites this paper as Canli et al. 2000
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“Studies using functional magnetic resonance imaging (fMRI) and positron emission tomography (PET) measurement of correlates of brain blood flow found increased amygdala activity with emotional paradigms including conditioning, exposure to angry faces, and negative pictures (Cahill et al. 1996; Buchel et al. 1998; LaBa…”
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“In support of this idea, comparisons across studies suggest that emotional enhancement increases as retention interval increases (Cahill et al., 1996; Canli, Zhao, Desmond, Glover, & Gabrieli, 1999; Canli, Zhao, Brewer, Gabrieli, & Cahill, 2000; Tabert et al., 2001).”
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“The stimuli were those described by Canli et al. (2000), with some modifications in the manner in which they were presented.”
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“In addition, these studies also found significant correlations between episodic memory performance and the level of amygdala activation during encoding of negative and positive stimuli (Canli et al., 2000; Dolcos et al., 2004; Hamann et al., 1999).”
BackgroundInfluentialNeural Substrates of Increased Memory Sensitivity for Negative Stimuli in Major Depression
Hamilton, J. P., & Gotlib, I. H. (2008) · Biological Psychiatry · doi:10.1016/j.biopsych.2007.12.015 · Cited by 345
Effects of normal aging and Alzheimer's disease on emotional memory.
Kensinger, E. A., Brierley, B., Medford, N., Growdon, J. H., & Corkin, S. (2002) · Emotion · doi:10.1037/1528-3542.2.2.118 · Cited by 350
Arana, F. S., Parkinson, J. A., Hinton, E. C., Holland, A. J., Owen, A. M., & Roberts, A. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-29-09632.2003 · Cited by 347
“Specifically, amygdala activity correlates with an individuals subjective rating of intensity of both extrinsically determined (present study) as well as homeostatically controlled incentive value (Morris and Dolan, 2001), with the arousing content of emotional stimuli and its subsequent mnemonic impact (Canli et al.,…”
BackgroundDe Quervain, D. J. ‐., Henke, K., Aerni, A., Treyer, V., McGaugh, J. L., Berthold, T., Nitsch, R. M., Buck, A., Roozendaal, B., & Hock, C. (2003) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2003.02542.x · Cited by 342
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“studies have further illustrated that amygdala and hippocampus activation during encoding of emotional stimuli is related to better recollection of those stimuli (Cahill et al., 2001; Hamann et al., 1999; Canli et al., 2000; Dolcos et al., 2004, 2005).”
BackgroundDaselaar, S. M., Rice, H. J., Greenberg, D. L., Cabeza, R., LaBar, K. S., & Rubin, D. C. (2008) · Cerebral Cortex · doi:10.1093/cercor/bhm048 · Cited by 341
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Affective Cognition and its Disruption in Mood Disorders
Elliott, R., Zahn, R., Deakin, J. F. W., & Anderson, I. M. (2011) · Neuropsychopharmacology · doi:10.1038/npp.2010.77 · Cited by 330
“Thus, Canli et al (2000) reported that amygdala response to Affective cognition and mood disorder R Elliott et al ...............................................................................................................................................................…”
Brain Activation during Facial Emotion Processing
Gur, R. C., Schroeder, L. F., Turner, T. H., McGrath, C., Chan, R. M., Turetsky, B. I., Alsop, D. C., Maldjian, J. A., & Gur, R. E. (2002) · NeuroImage · doi:10.1006/nimg.2002.1097 · Cited by 339
The slow forgetting of emotional episodic memories: an emotional binding account
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Emotion and Memory Research: A Grumpy Overview
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Early Amygdala Reaction to Fear Spreading in Occipital, Temporal, and Frontal Cortex
Krolak‐Salmon, P., Hénaff, M., Vighetto, A., Bertrand, O., & Mauguı̀ere, F. (2004) · Neuron · doi:10.1016/s0896-6273(04)00264-8 · Cited by 307
Beta-adrenergic modulation of emotional memory-evoked human amygdala and hippocampal responses.
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fMRI studies of successful emotional memory encoding: A quantitative meta-analysis
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“…to emphasize either (1) replicating the patterns of amygdala and MTL interactions identified by behavioral neuroscience approaches in animals (e.g., Canli et al., 2000; Dolcos et al., 2004b; Hamann et al., 1999), or (2) targeting a specific cognitive process during memory encoding, such as…”
Age-related differences in brain activation during emotional face processing
Gunning‐Dixon, F. M., Gur, R. C., Perkins, A. C., Schroeder, L. F., Turner, T. H., Turetsky, B. I., Chan, R. M., Loughead, J., Alsop, D. C., Maldjian, J. A., et al. (2002) · Neurobiology of Aging · doi:10.1016/s0197-4580(02)00099-4 · Cited by 315
“Functional neuroimaging studies have used diverse paradigms to examine emotion processing, including emotion discrimination [29,30,41], mood induction [24,59,68–70], fear conditioning [44,52], prosodic identification [9], reward and punishment conditions [42,57,80] and viewing of emotionally provocative stimuli [7,14,…”
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Neuroanatomical circuits modulating fear and anxiety behaviors
Charney, D. S. (2003) · Acta Psychiatrica Scandinavica · doi:10.1034/j.1600-0447.108.s417.3.x · Cited by 293
“Human neuroimaging, electrophysiologic and lesion analysis studies have also demonstrated that the amygdala is involved in the recall of emotional or arousing memories (1, 19, 20).”
BackgroundRole of the basolateral amygdala in memory consolidation
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“Moreover, imaging studies have found a high correlation between long-term recall of emotionally arousing or neutral material and the amount of amygdala activation observed when these stimuli were first presented (Cahill et al., 1996; Canli et al., 2000; Hamann et al., 1999).”
BackgroundMaking lasting memories: Remembering the significant
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Emotion enhances remembrance of neutral events past
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Self-citationEmotional context modulates subsequent memory effect
Erk, S., Kiefer, M., Grothe, J., Wunderlich, A. P., Spitzer, M., & Walter, H. (2003) · NeuroImage · doi:10.1016/s1053-8119(02)00015-0 · Cited by 278
“been extensively demonstrated with functional neuroimag- ing methods (for example, Canli et al., 2000; Hamann et al., 1999).”
BackgroundMethodAn emotion-induced retrograde amnesia in humans is amygdala- and β-adrenergic-dependent
Strange, B. A., Hurlemann, R., & Dolan, R. J. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1635116100 · Cited by 273
Abnormalities in emotion processing within cortical and subcortical regions in criminal psychopaths
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“…studies using pictures from the IAPS reported on significant emotion-induced brain activation within an extended circuitry, including the amygdala (Canli et al 2000; Paradiso et al 1999), the insula (Canli et al 1998), the right inferior frontal gyrus (Canli et al 1998; Paradiso et al 1999), the…”
BackgroundMcGaugh, J. L. (2015) · Annual Review of Psychology · doi:10.1146/annurev-psych-010814-014954 · Cited by 271
“Subsequent studies using PET as well as functional magnetic resonance imaging confirmed this finding and found that the correlation between amygdala activity and subsequent memory varied directly with the degree of emotional arousal induced during learning (Canli et al. 2000, Hamann et al. 1999).”
BackgroundPayne, J. D., Jackson, E. D., Hoscheidt, S., Ryan, L., Jacobs, W. J., & Nadel, L. (2007) · Learning & Memory · doi:10.1101/lm.743507 · Cited by 248
“Considerable research has shown that interactions between the amygdala and hippocampus enhance encoding and consolidation of emotionally arousing information (Cahill 2000; Canli et al. 2000; Packard and Cahill 2001; Phelps 2004).”
BackgroundAmygdala damage impairs emotional memory for gist but not details of complex stimuli
Adolphs, R., Tranel, D., & Buchanan, T. W. (2005) · Nature Neuroscience · doi:10.1038/nn1413 · Cited by 250
Space, time, and episodic memory: The hippocampus is all over the cognitive map
Ekstrom, A. D., & Ranganath, C. (2017) · Hippocampus · doi:10.1002/hipo.22750 · Cited by 278
“Scenes are routinely considered as “items” in memory studies (Canli et al., 2000; Ryan et al., 2000), and in many studies, scenes include multiple objects.”
BackgroundHaas, B. W., Omura, K., Constable, R. T., & Canli, T. (2007) · Behavioral Neuroscience · doi:10.1037/0735-7044.121.2.249 · Cited by 253
Self-citationCanli, T. (2004) · Journal of Personality · doi:10.1111/j.1467-6494.2004.00292.x · Cited by 254
Self-citation
Metadata
- Authors
- Canli, T., Zhao, Z., Brewer, J., Gabrieli, J. D. E., & Cahill, L.
- Affiliations
- Stanford University (US)
- University of California, Irvine (US)
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2000-10-01
- Volume
- 20
- Issue
- 19
- Pages
- RC99-RC99
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC6772800
- OpenAlex
- W2140577010
- Semantic Scholar
- f2872c2fe0383096f50aaf7a47a5104508c425b8
- Cited by
- 697
- References
- 25
- Citations by year
- 2026: 3 · 2025: 6 · 2024: 12 · 2023: 8 · 2022: 13 · 2021: 20 · 2020: 11 · 2019: 17 · 2018: 21 · 2017: 34 · 2016: 17 · 2015: 25 · 2014: 33 · 2013: 39 · 2012: 35
- FWCI
- 14.56
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Journal of Neuroscience (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory Processes and Influences
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
- Keywords
- amygdala, emotional memory, memory encoding, emotional intensity, subjective emotional experience, individual differences, declarative memory, scene perception, memory enhancement
- MeSH terms
- Amygdala, Brain Mapping, Emotions, Evoked Potentials, Visual, Female, Humans, Magnetic Resonance Imaging, Psychological Tests, Repression, Psychology
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