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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Amygdala responses track affective intensity, especially for aversive stimuli like those photos used widely in reappraisal studies.
“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
The Results report that bilateral amygdala activation correlated with participants’ ratings of emotional intensity, and the Methods describe the stimuli as negative-to-neutral pictures. The Discussion says the study could not separate arousal from negative valence; it therefore does not establish that responses track intensity especially for aversive stimuli. The paper also does not establish how widely these photos are used in reappraisal studies. (LLM, conf=0.84)
Experimental — accuracy not yet measuredAmygdala response to emotionally intense negative scenes is predictive of subsequent recall.
“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)
Amygdala-hippocampus interactions strengthen encoding and consolidation of emotionally arousing material.
“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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Dolcos, F., & Cabeza, R. E. L. (2002) · Cognitive Affective & Behavioral Neuroscience · doi:10.3758/cabn.2.3.252 · Cited by 435 · see citing works
“& Phelps, 1998) and functional neuroimaging (Cahill et al., 1996; Canli et al., 2000; Canli et al., 1999; Hamann et al., 1999) studies on humans have supported the role of the amygdala in the formation of emotional memory.”
BackgroundInfluentialRoozendaal, B., & McGaugh, J. L. (2011) · Behavioral Neuroscience · doi:10.1037/a0026187 · Cited by 445 · see citing works
Neural correlates of individual ratings of emotional salience: A trial-related fMRI study
Phan, K. L., Taylor, S. F., Welsh, R. C., Ho, S.-H., Britton, J. C., & Liberzon, I. (2004) · NeuroImage · doi:10.1016/j.neuroimage.2003.09.072 · Cited by 416 · see citing works
“…in the amygdala (Breiter et al., 1996; Garavan et al., 2001; Hamann and Mao, 2002; Hamann et al., 2002; Liberzon et al., 2003; Pessoa et al., 2002), and that the amygdala activity reflects subjectively perceived emotional intensity (Anderson et al., 2003b; Canli et al., 2000; Phan et al., 2003).”
BackgroundSex-related difference in amygdala activity during emotionally influenced memory storage
Cahill, L., Haier, R. J., White, N. S., Fallon, J., Kilpatrick, L., Lawrence, C., Potkin, S. G., & Alkire, M. T. (2001) · Neurobiology of Learning and Memory · doi:10.1006/nlme.2000.3999 · Cited by 413 · see citing works
Impact of Sleep and Its Disturbances on Hypothalamo-Pituitary-Adrenal Axis Activity
Balbo, M., Leproult, R., & Van Cauter, E. (2010) · International Journal of Endocrinology · doi:10.1155/2010/759234 · Cited by 408 · see citing works
“Sleep complains in older adults are more common in women than in men and this could play a role in the greater female reduction of the quiescent period.”
BackgroundEcstasy 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 399 · see citing works
“2, MARCH 2002 lateralization of the amygdala activations across conditions is consistent with left-amygdala responses to negative picture stimuli reported in previous studies (Canli et al., 2000; Lane et al., 1997).”
ResultMackay, D. G., Shafto, M. A., Taylor, J. K., Marian, D. E., Abrams, L., & Dyer, J. R. (2004) · Memory & Cognition · doi:10.3758/bf03195840 · Cited by 346 · see citing works
Positive and negative emotional verbal stimuli elicit activity in the left amygdala
Hamann, S., & Mao, H. (2002) · Neuroreport · doi:10.1097/00001756-200201210-00008 · Cited by 385 · see citing works
Emotion and memory narrowing: A review and goal-relevance approach
Levine, L. J., & Edelstein, R. S. (2009) · Cognition & Emotion · doi:10.1080/02699930902738863 · Cited by 380 · see citing works
Aging and the Intersection of Cognition, Motivation, and Emotion
Carstensen, L. L., Mikels, J. A., & Mather, M. (2006) · Elsevier eBooks · doi:10.1016/b978-012101264-9/50018-5 · Cited by 372 · see citing works
“The study focused on the amygdala, a region of the brain that has been found to enhance memory for emotionally arousing information (e.g., Cahill et al., 1996; Canli et al., 2000; Phelps et al., 1998).”
BackgroundBREMNER, J. D., VERMETTEN, E., SCHMAHL, C., VACCARINO, V., VYTHILINGAM, M., AFZAL, N., GRILLON, C., & CHARNEY, D. S. (2005) · Psychological Medicine · doi:10.1017/s0033291704003290 · Cited by 370 · see citing works
“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…”
BackgroundStress and emotional memory: a matter of timing
Joëls, M., Fernández, G., & Roozendaal, B. (2011) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2011.04.004 · Cited by 372 · see citing works
Effect of Negative Emotional Content on Working Memory and Long-Term Memory.
Kensinger, E. A., & Corkin, S. (2003) · Emotion · doi:10.1037/1528-3542.3.4.378 · Cited by 364 · see citing works
“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).”
ResultCahill, L. F., Uncapher, M. R., Kilpatrick, L. A., Alkire, M. T., & Turner, J. A. (2004) · Learning & Memory · doi:10.1101/lm.70504 · Cited by 362 · see citing works
“The stimuli were those described by Canli et al. (2000), with some modifications in the manner in which they were presented.”
BackgroundMethodResultInfluentialSelf-citationThe emotional power of music: How music enhances the feeling of affective pictures
Baumgartner, T., Lutz, K., Schmidt, C. F., & Jäncke, L. (2006) · Brain Research · doi:10.1016/j.brainres.2005.12.065 · Cited by 354 · see citing works
“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 · see citing works
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 · see citing works
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 342 · see citing works
“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 · see citing works
Banich, M. T., Mackiewicz, K. L., Depue, B. E., Whitmer, A. J., Miller, G. A., & Heller, W. (2009) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2008.09.010 · Cited by 343 · see citing works
“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 · see citing works
“…of memories not recently accessed as done here, we might expect to see more effects of the right PFC because participants are attempting to access the memories for longer Cerebral Cortex January 2008;18:217--229 doi:10.1093/cercor/bhm048 Advance Access publication June 4, 2007 The Author 2007.”
BackgroundInfluentialUncapher, M. R., & Wagner, A. D. (2008) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2008.10.011 · Cited by 338 · see citing works
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 · see citing works
“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 326 · see citing works
The slow forgetting of emotional episodic memories: an emotional binding account
Yonelinas, A. P., & Ritchey, M. (2015) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2015.02.009 · Cited by 322 · see citing works
Emotion and Memory Research: A Grumpy Overview
Levine, L. J., & Pizarro, D. A. (2004) · Social Cognition · doi:10.1521/soco.22.5.530.50767 · Cited by 318 · see citing works
Paulus, M. P., Feinstein, J. S., Castillo, G., Simmons, A. N., & Stein, M. B. (2005) · Archives of General Psychiatry · doi:10.1001/archpsyc.62.3.282 · Cited by 314 · see citing works
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 · see citing works
Beta-adrenergic modulation of emotional memory-evoked human amygdala and hippocampal responses.
Strange, B., & Dolan, R. (2004) · Proceedings of the National Academy of Sciences of the United States of America · doi:10.1073/pnas.0404282101 · Cited by 329 · see citing works
fMRI studies of successful emotional memory encoding: A quantitative meta-analysis
Murty, V. P., Ritchey, M., Adcock, R. A., & LaBar, K. S. (2010) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2010.07.030 · Cited by 293 · see citing works
“…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 295 · see citing works
“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,…”
BackgroundKilpatrick, L. A. (2003) · NeuroImage · doi:10.1016/j.neuroimage.2003.08.006 · Cited by 294 · see citing works
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 291 · see citing works
“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
Paré, D. (2003) · Progress in Neurobiology · doi:10.1016/s0301-0082(03)00104-7 · Cited by 288 · see citing works
“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
McGaugh, J. D. (2013) · Proceedings of the National Academy of Sciences of the United States of America · doi:10.1073/pnas.1301209110 · Cited by 291 · see citing works
Emotion enhances remembrance of neutral events past
Anderson, A., Wais, P. E., & Gabrieli, J. (2006) · Proceedings of the National Academy of Sciences of the United States of America · doi:10.1073/pnas.0506308103 · Cited by 275 · see citing works
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 280 · see citing works
“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 · see citing works
Abnormalities in emotion processing within cortical and subcortical regions in criminal psychopaths
Müller, J. L., Sommer, M., Wagner, V., Lange, K., Taschler, H., Röder, C. H., Schuierer, G., Klein, H. E., & Hajak, G. (2003) · Biological Psychiatry · doi:10.1016/s0006-3223(02)01749-3 · Cited by 272 · see citing works
“…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 · see citing works
“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 · see citing works
“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 · see citing works
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 250 · see citing works
“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 242 · see citing works
Self-citationCanli, T. (2004) · Journal of Personality · doi:10.1111/j.1467-6494.2004.00292.x · Cited by 241 · see citing works
Self-citation
- 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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