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Interaction between the Amygdala and the Medial Temporal Lobe Memory System Predicts Better Memory for Emotional Events
Open accessAbstract
Emotional events are remembered better than neutral events possibly because the amygdala enhances the function of medial temporal lobe (MTL) memory system (modulation hypothesis). Although this hypothesis has been supported by much animal research, evidence from humans has been scarce and indirect. We investigated this issue using event-related fMRI during encoding of emotional and neutral pictures. Memory performance after scanning showed a retention advantage for emotional pictures. Successful encoding activity in the amygdala and MTL memory structures was greater and more strongly correlated for emotional than for neutral pictures. Moreover, a double dissociation was found along the longitudinal axis of the MTL memory system: activity in anterior regions predicted memory for emotional items, whereas activity in posterior regions predicted memory for neutral items. These results provide direct evidence for the modulation hypothesis in humans and reveal a functional specialization within the MTL regarding the effects of emotion on memory formation.
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“neuroimaging studies have provided strong support for the idea that the conjoint activation of the hippocampus and amygdala under arousing counditions is a critical component of emotional memory storage and retrieval processes (Maratos et al. [191]; Dolcos et al. [192]; Dolcos et al. [193]).”
From The Temporal Dynamics Model of Emotional Memory Processing: A Synthesis on the Neurobiological Basis of Stress-Induced Amnesia, Flashbulb and Traumatic Memories, and the Yerkes-Dodson Law (2007) · cites this paper as Dolcos et al. [192]
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Prenatal maternal depression alters amygdala functional connectivity in 6-month-old infants
Qiu, A., Anh, T. T., Li, Y., Chen, H., Rifkin-Graboi, A., Broekman, B. F. P., Kwek, K., Saw, S.-M., Chong, Y.-S., Gluckman, P. D., et al. (2015) · Translational Psychiatry · doi:10.1038/tp.2015.3 · Cited by 282
Emotion enhances remembrance of neutral events past
Anderson, A. K., Wais, P. E., & Gabrieli, J. D. E. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0506308103 · Cited by 301
Greenberg, D. L., Rice, H. J., Cooper, J. J., Cabeza, R., Rubin, D. C., & LaBar, K. S. (2005) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2004.09.002 · Cited by 273
Self-citationMcGaugh, J. L. (2015) · Annual Review of Psychology · doi:10.1146/annurev-psych-010814-014954 · Cited by 271
“Importantly, other studies reported that emotionally arousing learning experiences induce interactions of the amygdala with other brain regions, including the hippocampus (Dolcos et al. 2004, Kilpatrick & Cahill 2003).”
BackgroundWorkgroup, M.-A. M., Brown, V. M., LaBar, K. S., Haswell, C. C., Gold, A. L., McCarthy, G., & Morey, R. A. (2013) · Neuropsychopharmacology · doi:10.1038/npp.2013.197 · Cited by 274
“Information from multiple sensory modalities that facilitate the encoding of fear memories associated with sensory information (Dolcos et al, 2004) enters the BLA and signals its threat value to cortical targets (Myers and Davis, 2007).”
BackgroundSelf-citationHolt, D. J., Kunkel, L., Weiss, A. P., GOFF, D. C., Wright, C. I., Shin, L. M., Rauch, S. L., Hootnick, J., & Heckers, S. (2005) · Schizophrenia Research · doi:10.1016/j.schres.2005.09.021 · Cited by 247
Task and Content Modulate Amygdala-Hippocampal Connectivity in Emotional Retrieval
Smith, A. P. R., Stephan, K. E., Rugg, M. D., & Dolan, R. J. (2006) · Neuron · doi:10.1016/j.neuron.2005.12.025 · Cited by 252
Amygdala 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
“Likewise, studies in humans have confirmed that the amygdala modulates other medial temporal lobe structures during encodin”
Human vulnerability to stress depends on amygdala's predisposition and hippocampal plasticity
Admon, R., Lubin, G., Stern, O., Rosenberg, K., Sela, L., Ben‐Ami, H., & Hendler, T. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0903183106 · Cited by 241
Sharot, T., & Yonelinas, A. (2008) · Cognition · doi:10.1016/j.cognition.2007.03.002 · Cited by 246
“…studies showing that amygdala activation at encoding is related to subsequent memory for emotional items (Kensinger & Schacter, 2006b) and ‘‘remember’’ judgments for those items (Dolcos et al., 2004), but not to subsequent memory for the task performed during encoding (Kensinger & Schacter, 2006b).”
BackgroundInfluentialThe role of REM sleep theta activity in emotional memory
Hutchison, I. C., & Rathore, S. (2015) · Frontiers in Psychology · doi:10.3389/fpsyg.2015.01439 · Cited by 245
“Noradrenaline has been shown to suppress excitatory feedback transmissionwithin the somatosensory and piriform cortex (Dodt et al., 1991; Hasselmo et al., 1997; Hasselmo, 1999), but not the hippocampus (Mueller et al., 1981).”
BackgroundThe Locus Ceruleus Is Involved in the Successful Retrieval of Emotional Memories in Humans
Sterpenich, V., D'Argembeau, A., Desseilles, M., Balteau, E., Albouy, G., Vandewalle, G., Degueldre, C., Luxen, A., Collette, F., & Maquet, P. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.1001-06.2006 · Cited by 245
“The bias toward a better recollection of emotional events has been primarily explained by a direct modulation of hippocampal responses by the amygdala, at encoding (Kilpatrick and Cahill, 2003; Dolcos et al., 2004; Richardson et al., 2004) and during retrieval (Strange and Dolan, 2004; Fenker et al.”
BackgroundArbib, M. A., & Fellous, J. (2004) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2004.10.004 · Cited by 257
The role of attention and relatedness in emotionally enhanced memory.
Talmi, D., Schimmack, U., Paterson, T. S. E., & Moscovitch, M. (2007) · Emotion · doi:10.1037/1528-3542.7.1.89 · Cited by 256
“Activation in the amygdala is also associated with subsequent EEM with delays as short as 10 minutes (Kensinger & Corkin, 2004) and with delays of about 1 hr (Dolcos et al., 2004a, 2004b; LaBar & Phelps, 1998).”
InfluentialHow (and Why) Emotion Enhances the Subjective Sense of Recollection
Phelps, E. A., & Sharot, T. (2008) · Current Directions in Psychological Science · doi:10.1111/j.1467-8721.2008.00565.x · Cited by 236
Interacting brain systems modulate memory consolidation
McIntyre, C. K., McGaugh, J. L., & Williams, C. L. (2011) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2011.11.001 · Cited by 243
“…indicate that successful encoding of emotional material is associated with enhanced functional connectivity between the amygdala and the hippocampus (Dolcos et al., 2004; Hamann et al., 1999; Kensinger and Corkin, 2004; Murty et al., 2010; Murty et al., 2009; St Jacques et al., 2009).”
BackgroundThe coupling of emotion and cognition in the eye: introducing the pupil old/new effect.
Võ, M., Jacobs, A., Kuchinke, L., Hofmann, M., Conrad, M., Schacht, A., & Hutzler, F. (2007) · Psychophysiology · doi:10.1111/j.1469-8986.2007.00606.x · Cited by 228
The Emotional Brain as a Predictor and Amplifier of Chronic Pain
Vachon‐Presseau, É., Centeno, M. V., Ren, W., Berger, S., Tétreault, P., Ghantous, M. E., Baria, A. T., Farmer, M., Baliki, M. N., Schnitzer, T. J., et al. (2016) · Journal of Dental Research · doi:10.1177/0022034516638027 · Cited by 253
“The amygdala and the hippocampus are central to the consolidation of emotional memories, such as those pertaining to a painful or stressful event (Cahill et al. 1994; Dolcos et al. 2004; Phelps 2004; Richardson et al. 2004).”
BackgroundFollowing the Crowd: Brain Substrates of Long-Term Memory Conformity
Edelson, M. G., Sharot, T., Dolan, R. J., & Dudai, Y. (2011) · Science · doi:10.1126/science.1203557 · Cited by 236
Ritchey, M., Dolcos, F., & Cabeza, R. E. L. (2008) · Cerebral Cortex · doi:10.1093/cercor/bhm262 · Cited by 204
“Interestingly, the MTL memory regions showing emotionand delay-specific connectivity with the amygdala are bilaterally located within the anterior PHG, not within the hippocampus proper.”
BackgroundResultInfluentialSelf-citationNoradrenaline mediates amygdala activation in men and women during encoding of emotional material
van Stegeren, A. H., Goekoop, R., Everaerd, W., Scheltens, P., Barkhof, F., Kuijer, J. P. A., & Rombouts, S. A. R. B. (2005) · NeuroImage · doi:10.1016/j.neuroimage.2004.09.011 · Cited by 212
Maheu, F. S., Dozier, M., Guyer, A. E., Mandell, D. S., Peloso, E. D., Poeth, K., Jenness, J. L., Lau, J. Y. F., Ackerman, J. P., Pine, D. S., et al. (2010) · Cognitive Affective & Behavioral Neuroscience · doi:10.3758/cabn.10.1.34 · Cited by 223
“Reduced medial temporal lobe volume (De Bellis et al., 2002) and altered hippocampal volume (reduced volume, Carrion et al., 2007; increased volume, Tupler & De Bellis, 2006) the processing of emotional cues per se (Bannerman et al., 2004; Dolcos et al., 2004; LeDoux, 2000).”
Dissociable effects of conscious emotion regulation strategies on explicit and implicit memory.
Dillon, D., Ritchey, M., Johnson, B., & LaBar, K. (2007) · Emotion · doi:10.1037/1528-3542.7.2.354 · Cited by 206
“Ninety unpleasant and 90 neutral pictures were selected from the International Affective Picture Set (Lang, Bradley, & Cuthbert, 2001) and an in-house database (Dolcos et al., 2004).”
MethodSelf-citationDolcos, F., Katsumi, Y., Moore, M., Berggren, N., de Gelder, B., Derakshan, N., Hamm, A. O., Koster, E. H. W., Ladouceur, C. D., Okon‐Singer, H., et al. (2019) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2019.08.017 · Cited by 247
Self-citationHayes, J. P., LaBar, K. S., McCarthy, G., Selgrade, E. S., Nasser, J. D., Dolcos, F., & Morey, R. A. (2010) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2010.10.007 · Cited by 190
“The hippocampus and parahippocampal gyruswere further divided into anterior and posterior portions based on evidence for different functions along the longitudinal axis of these structures (Dolcos et al., 2004).”
InfluentialSelf-citationQuantifying the impact of recent negative life events on suicide attempts
Bagge, C. L., Glenn, C. R., & Lee, H.-J. (2013) · Journal of Abnormal Psychology · doi:10.1037/a0030371 · Cited by 201
How personal experience modulates the neural circuitry of memories of September 11
Sharot, T., Martorella, E. A., Delgado, M. R., & Phelps, E. A. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0609230103 · Cited by 200
Neural Correlates of Recall of Life Events in Conversion Disorder
Aybek, S., Nicholson, T. R., Zelaya, F. O., O’Daly, O., Craig, T., David, A. S., & Kanaan, R. (2013) · JAMA Psychiatry · doi:10.1001/jamapsychiatry.2013.2842 · Cited by 219
Jacques, P. L. S., Dolcos, F., & Cabeza, R. (2009) · Psychology Science · doi:10.1111/j.1467-9280.2008.02258.x · Cited by 193
“Previous studies in young adults have found that amygdalar-hippocampal interactions enhance subsequent memory (Dolcos et al., 2004b), and the current results suggest that this modulation is reduced in aging.”
BackgroundSelf-citationNEVER forget: negative emotional valence enhances recapitulation
Bowen, H. J., Kark, S. M., & Kensinger, E. A. (2017) · Psychonomic Bulletin & Review · doi:10.3758/s13423-017-1313-9 · Cited by 249
The neural basis of implicit moral attitude—An IAT study using event-related fMRI
Luo, Q., Nakic, M., Wheatley, T., Richell, R., Martin, A., & Blair, R. J. R. (2006) · NeuroImage · doi:10.1016/j.neuroimage.2005.11.005 · Cited by 191
Vaisvaser, S., Lin, T., Admon, R., Podlipsky, I., Greenman, Y., Stern, N., Fruchter, E., Wald, I., Pine, D. S., Tarrasch, R., et al. (2013) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2013.00313 · Cited by 193
“Furthermore, enhancement in amygdalahippocampal connectivity was suggested to be required for both emotional memory encoding and consolidation (Richter-Levin and Akirav, 2000; Roozendaal et al., 2003; Dolcos et al., 2004; Phelps, 2004; Smith et al., 2006).”
BackgroundMenstrual cycle modulation of medial temporal activity evoked by negative emotion
Andreano, J. M., & Cahill, L. F. (2010) · NeuroImage · doi:10.1016/j.neuroimage.2010.07.011 · Cited by 187
“Several studies have shown that activity at encoding in the amygdala (Kensinger & Schacter, 2006; Dolcos et al., 2004; Cahill et al., 1996) and hippocampus (Spaniol et al.”
Roozendaal, B., McReynolds, J. R., van der Zee, E. A., Lee, S., McGaugh, J. L., & McIntyre, C. K. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.3626-09.2009 · Cited by 175
Jacques, P. L. S., Dolcos, F., & Cabeza, R. E. L. (2008) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2008.03.012 · Cited by 198
Self-citationOn the role of general system theory for functional neuroimaging
Stephan, K. (2004) · Journal of Anatomy · doi:10.1111/j.0021-8782.2004.00359.x · Cited by 174
“Indeed, even in recent papers the finding that several areas are jointly correlated to some task component is still sometimes interpreted as a reflection of mutual correlation and thus of functional connectivity among the areas (e.g. Gold & Buckner, 2002; Dolcos et al. 2004).”
BackgroundHow Negative Emotion Enhances the Visual Specificity of a Memory
Kensinger, E., Garoff-Eaton, R. J., & Schacter, D. (2007) · Journal of Cognitive Neuroscience · doi:10.1162/jocn.2007.19.11.1872 · Cited by 173
“These regions are very consistent with those shown in previous studies to be more predictive of successful encoding of emotional information than of neutral information (e.g., Kensinger & Schacter, 2005a; Dolcos et al., 2004; reviewed by LaBar & Cabeza, 2006).”
ResultNoradrenergic Modulation of Emotion-Induced Forgetting and Remembering
Hurlemann, R., Hawellek, B., Matusch, A., Kölsch, H., Wollersen, H., Madea, B., Vogeley, K. T., Maier, W., & Dolan, R. J. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.0228-05.2005 · Cited by 165
Wang, G.-J., Yang, J., Volkow, N. D., Telang, F., Ma, Y., Zhu, W., Wong, C. T., Tomasi, D., Thanos, P. K., & Fowler, J. S. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0601977103 · Cited by 168
Neural basis of interpersonal traits in neurodegenerative diseases
Sollberger, M., Stanley, C. M., Wilson, S. M., Gyurak, A., Beckman, V., Growdon, M., Jang, J., Weiner, M. W., Miller, B. L., & Rankin, K. P. (2009) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2009.06.006 · Cited by 167
Direct electrical stimulation of the amygdala enhances declarative memory in humans
Inman, C. S., Manns, J. R., Bijanki, K. R., Bass, D. I., Hamann, S. B., Drane, D. L., Fasano, R. E., Kovach, C. K., Gross, R. E., & Willie, J. T. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1714058114 · Cited by 191
Neural Signature of Reconsolidation Impairments by Propranolol in Humans
Schwabe, L., Nader, K., Wolf, O. T., Beaudry, T., & Pruessner, J. C. (2011) · Biological Psychiatry · doi:10.1016/j.biopsych.2011.10.028 · Cited by 188
Tendolkar, I., Beek, M. H. C. T. V., van Oostrom, I., Mulder, M., Janzing, J., Voshaar, R. C. O., & van Eijndhoven, P. (2013) · Psychiatry Research Neuroimaging · doi:10.1016/j.pscychresns.2013.09.004 · Cited by 165
“The amygdala has strong modulatory impact on the hippocampus (McGaugh, 2000) and functional imaging studies have supported this at the human system level in healthy controls (Dolcos et al., 2004) and in depressed patients (van Eijndhoven et al., 2011).”
BackgroundHöistad, M., & Barbas, H. (2008) · NeuroImage · doi:10.1016/j.neuroimage.2007.12.043 · Cited by 160
Amygdala activation during reading of emotional adjectives—an advantage for pleasant content
Herbert, C., Ethofer, T., Anders, S., Junghöfer, M., Wildgruber, D., Grodd, W., & Kissler, J. M. (2008) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nsn027 · Cited by 168
“20 hippocampus (anterior PHG), a region which has recently been related to enhanced memory encoding of emotional salient visual stimuli (Dolcos et al., 2004).”
BackgroundMcDonald, A. J., & Mott, D. D. (2016) · Journal of Neuroscience Research · doi:10.1002/jnr.23709 · Cited by 189
“Functional imaging studies in humans have shown that the formation of memories of emotional stimuli involves interactions of the basolateral amygdala with the entorhinal cortex and anterior portions of the hippocampus (Dolcos et al., 2004), and that these areas are also activated by retrieval of emotional memories (Do…”
Adrenal stress hormones, amygdala activation, and memory for emotionally arousing experiences
Roozendaal, B., Barsegyan, A., & Lee, S. (2007) · Progress in Brain Research · doi:10.1016/s0079-6123(07)67006-x · Cited by 154
Pharmacotherapy of PTSD: premises, principles, and priorities.
Ravindran, L. N., & Stein, M. B. (2009) · Brain Research · doi:10.1016/j.brainres.2009.03.037 · Cited by 153
“With evidence from functional neuroimaging studies (Dolcos et al., 2004; Kensinger and Corkin, 2004; Kilpatrick and Cahill, 2003; Richardson et al., 2004) suggesting that encoding of emotional episodes involves a functional coupling between the amygdala and hippocampus, it has been suggested that…”
BackgroundHow the amygdala affects emotional memory by altering brain network properties
Hermans, E. J., Battaglia, F. P., Atsak, P., de Voogd, L. D., Fernández, G., & Roozendaal, B. (2014) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2014.02.005 · Cited by 173
Metadata
- Authors
- Dolcos, F., LaBar, K. S., & Cabeza, R.
- Affiliations
- University of Alberta (CA)
- Duke University (US)
- Corresponding author
- Dolcos, Florin
- Venue
- Neuron
- Publisher
- Elsevier BV
- Published
- 2004-06
- Volume
- 42
- Issue
- 5
- Pages
- 855-863
- ISSN
- 0896-6273 (ISSN-L)
- OpenAlex
- W2156322511
- Cited by
- 714
- References
- 0
- Citations by year
- 2026: 22 · 2025: 24 · 2024: 22 · 2023: 18 · 2022: 18 · 2021: 21 · 2020: 34 · 2019: 27 · 2018: 29 · 2017: 46 · 2016: 34 · 2015: 41 · 2014: 39 · 2013: 40 · 2012: 40
- FWCI
- 15.97
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Neuron (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institute on Aging (R01AG019731, R01 AG19731)
- National Institute on Drug Abuse (R01DA014094, R01 DA14094)
- 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, emotional pictures, memory encoding, functional specialization, event-related fMRI
- MeSH terms
- Adult, Amygdala, Analysis of Variance, Brain Mapping, Emotions, Female, Humans, Image Processing, Computer-Assisted, Magnetic Resonance Imaging, Memory, Models, Neurological, Photic Stimulation, Temporal Lobe, Recognition, Psychology
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