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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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Rimmele, U., Lackovic, S. F., Tobe, R. H., Leventhal, B., & Phelps, E. (2016) · Journal of Cognitive Neuroscience · doi:10.1162/jocn_a_00941 · Cited by 24
Spatial memory extinction: A c-Fos protein mapping study
Méndez‐Couz, M., Conejo, N. M., Vallejo, G., & Arias, J. L. (2013) · Behavioural Brain Research · doi:10.1016/j.bbr.2013.11.032 · Cited by 23
An executive function subtype of PTSD with unique neural markers and clinical trajectories
Jagger-Rickels, A. C., Rothlein, D., Stumps, A. D., Evans, T. C., Bernstein, J. P. K., Milberg, W., McGlinchey, R. E., Degutis, J. M., & Esterman, M. S. (2022) · Translational Psychiatry · doi:10.1038/s41398-022-02011-y · Cited by 27
Intrusive memories: A mechanistic signature for emotional memory persistence
Herz, N., Bar‐Haim, Y., Holmes, E. A., & Censor, N. (2020) · Behaviour Research and Therapy · doi:10.1016/j.brat.2020.103752 · Cited by 33
Makovac, E., Mancini, M., Fagioli, S., Watson, D. R., Meeten, F., Rae, C. L., Critchley, H., & Ottaviani, C. (2018) · Psychiatry Research Neuroimaging · doi:10.1016/j.pscychresns.2018.09.006 · Cited by 24
“Moreover, studies suggest that emotional events are better remembered compared to neutral events, in part because of the interaction between amygdala and hippocampus within medial temporal lobe (Dolcos et al., 2004).”
The effect of mild acute stress during memory consolidation on emotional recognition memory
Corbett, B., Weinberg, L., & Duarte, A. (2017) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2017.08.005 · Cited by 24
Bär, K., Herbsleb, M., Schumann, A., de la Cruz, F., Gabriel, H. W., & Wagner, G. (2016) · Frontiers in Neuroscience · doi:10.3389/fnins.2016.00145 · Cited by 27
Xiu, D., Geiger, M. J., & Klaver, P. (2015) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2015.00090 · Cited by 20
“…6, France Reviewed by: Inah Lee, Seoul National University, South Korea Jeffrey D. Johnson, University of Missouri, USA *Correspondence: Peter Klaver, Division of Abnormal Psychology and Clinical Intervention, Department of Psychology, University of Zurich, Binzmühlestrasse 14/17 – BIN 3.”
InfluentialBAIAP2 Is Related to Emotional Modulation of Human Memory Strength
Lukšys, G., Ackermann, S., Coynel, D., Fastenrath, M., Gschwind, L., Heck, A., Rasch, B., Spalek, K., Vogler, C., Papassotiropoulos, A., et al. (2014) · PLoS ONE · doi:10.1371/journal.pone.0083707 · Cited by 17
“A functional neuroimaging study [29] showed that posterior MTL areas were more sensitive to neutral subsequent memory and anterior ones to emotional subsequent memory, which was essentially replicated in our genotype-independent fMRI results (Tableô 3).”
ResultĆurĉić‐Blake, B., Swart, M., & Aleman, A. (2011) · Cerebral Cortex · doi:10.1093/cercor/bhr124 · Cited by 19
“Human functional studies have also investigated the connections among these areas involved in various emotional memory tasks (Dolcos et al. 2004; Summerfield et al. 2006; Depue et al. 2007).”
BackgroundBrain imaging investigation of the memory-enhancing effect of emotion.
Shafer, A. T., Iordan, A., Cabeza, R., & Dolcos, F. (2011) · Journal of Visualized Experiments · doi:10.3791/2433 · Cited by 23
Self-citationDahlén, A. D., Schofield, A., Schiöth, H., & Brooks, S. (2022) · Frontiers in Neuroscience · doi:10.3389/fnins.2022.868366 · Cited by 22
“Indeed, emotional arousal is a well-established mediator in memory consolidation via the amygdalohippocampal-parahippocampal network (Dolcos et al., 2004).”
BackgroundChaudhary, S., Zhornitsky, S., Chao, H., van Dyck, C., & Li, C. (2021) · Journal of Alzheimer's Disease · doi:10.3233/jad-215316 · Cited by 22
Do different salience cues compete for dominance in memory over a daytime nap?
Alger, S. E., Chen, S., & Payne, J. D. (2018) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2018.06.005 · Cited by 25
Brain Activation During Emotional Memory Processing Associated with Subsequent Course of Depression
Ai, H., Opmeer, E., Veltman, D., van der Wee, N. V. D., van Buchem, M., Aleman, A., & van Tol, M. (2015) · Neuropsychopharmacology · doi:10.1038/npp.2015.96 · Cited by 22
Justel, N. R., Psyrdellis, M., & Ruetti, E. (2014) · Suma Psicológica · doi:10.14349/sumapsi2013.1276 · Cited by 46
Salokangas, R. K. R., Hietala, J. A., Armio, R.-L., Laurikainen, H., From, T., Borgwardt, S., Riecher‐Rössler, A., Brambilla, P., Bonivento, C., Meisenzahl, E. M., et al. (2020) · Schizophrenia Research · doi:10.1016/j.schres.2020.05.041 · Cited by 25
Ruiz-Rizzo, A. L., Beissner, F., Finke, K., Müller, H., Zimmer, C., Pasquini, L., & Sorg, C. (2019) · bioRxiv · doi:10.1101/659854 · Cited by 21
“…takes place in a wide variety of functional domains, such as in fear-related unconditioned responses (Davis, 1992; Gross and Canteras, 2012), and emotional (Davis et al., 1994; Gross and Canteras, 2012; Tovote et al., 2015) or episodic memory (Kemppainen et al., 2002; Dolcos et al., 2004).”
BackgroundFace and gaze perception in borderline personality disorder: An electrical neuroimaging study
Berchio, C., Piguet, C., Gentsch, K., Küng, A., Rihs, T. A., Hasler, R., Aubry, J., Dayer, A. G., Michel, C. M., & Perroud, N. A. (2017) · Psychiatry Research Neuroimaging · doi:10.1016/j.pscychresns.2017.08.011 · Cited by 18
“The medial temporal gyrus is involved in face expression retrieval (Bonora et al., 2011; Dolcos et al., 2004; Geday et al., 2003; Holt et al., 2006), and abnormal activations in BPD patients have been previously reported during emotion discrimination tasks (Guitart-Masip et al., 2009).”
The Potentiation of Associative Memory by Emotions: An Event-Related FMRI Study
Luck, D., Leclerc, M.-È., & Lepage, M. (2014) · Advances in Neuroscience · doi:10.1155/2014/964024 · Cited by 21
“Such rostrocaudal dissociation has already been demonstratedwith IAPS pictures [27] and words [52].”
BackgroundInfluentialPorte, Y., & Morel, J. (2012) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2012.00064 · Cited by 25
“…components of memorized episodes (Desmedt et al., 1998; Bianchin et al., 1999; Ferry et al., 1999; Frey et al., 2001; Akirav and Richter-Levin, 2002; Quevedo et al., 2003; Dolcos et al., 2004), including in extreme situations that lead to psychopathologies such as PTSD (Kaouane et al., 2012).”
BackgroundSakaki, M., Niki, K., & Mather, M. (2011) · Journal of Cognitive Neuroscience · doi:10.1162/jocn_a_00057 · Cited by 22
Hippocampal Contributions to Declarative Memory Consolidation During Sleep
Antony, J. W., & Paller, K. A. (2017) · Springer eBooks · doi:10.1007/978-3-319-50406-3_9 · Cited by 27
“Furthermore, a complex set of hormonal factors (McGaugh 2000), interactions between the amygdala and the hippocampus (Dolcos et al. 2004) or vmPFC (Bennion et al.”
BackgroundHippocampal Threat Reactivity Interacts with Physiological Arousal to Predict PTSD SymptomsPreprint
Tanrıverdi, B., Gregory, D. F., Olino, T., Ely, T., Harnett, N., van Rooij, S. V., Lebois, L., Seligowski, A. V., Jovanović, T., Ressler, K., et al. (2021) · Journal of Neuroscience · doi:10.31234/osf.io/xp5db · Cited by 20
Names and their meanings: A dual-process account of proper-name encoding and retrieval
O’Rourke, T. J., & de Diego‐Balaguer, R. (2019) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2019.11.005 · Cited by 38
Noradrenergic mechanisms of arousal’s bidirectional effects on episodic memory
Clewett, D., Sakaki, M., Nielsen, S. E., Petzinger, G. M., & Mather, M. (2016) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2016.10.017 · Cited by 26
“…emotion-related impairments is that the amygdala selectively modulates cortical and hippocampal activity to favor processing of emotional stimuli (Dolcos et al., 2004; Fastenrath et al., 2014; Kilpatrick & Cahill, 2003; Richardson et al., 2004; Strange & Dolan, 2004; Vuilleumier et al., 2004),…”
Baseline frontostriatal-limbic connectivity predicts reward-based memory formation
Hamann, J. M., Dayan, E., Hummel, F. C., & Cohen, L. G. (2014) · Human Brain Mapping · doi:10.1002/hbm.22594 · Cited by 18
Chainay, H., Michael, G., Vert-pré, M., Landré, L., & Plasson, A. (2012) · Advances in Cognitive Psychology · doi:10.2478/v10053-008-0121-1 · Cited by 20
Rezayof, A., Habibi, P., & Zarrindast, M. (2011) · Neuroscience · doi:10.1016/j.neuroscience.2010.12.006 · Cited by 20
How Emotional Arousal Enhances Episodic Memory
Baraly, K. T. A., Hot, P., Davidson, P. S. R., & Talmi, D. (2017) · Elsevier eBooks · doi:10.1016/b978-0-12-809324-5.21051-1 · Cited by 32
“Taken as a whole, these results suggest that successful encoding of emotional items is predicted by the co-activation of the amygdala and the hippocampus (Dolcos et al., 2004a).”
BackgroundMethodResultInfluentialLiu, S., Yin, N., Ma, R., Cao, H., Jing, C., Zhang, Y., Chen, D., Zhang, J., Wu, Y. F., Feng, J., et al. (2020) · International Journal of Neuroscience · doi:10.1080/00207454.2020.1813130 · Cited by 21
“The temporal brain regions were found to be involved in the emotion processing and the declarative memory [40].”
BackgroundThe Missing Link in Early Emotional Processing
Carretié, L., Yadav, R. K., & Méndez-Bértolo, C. (2020) · Emotion Review · doi:10.1177/17540739211022821 · Cited by 19
“…2000), vegetative (hypothalamus; LeDoux, 2000), subjective (e.g., fear feeling, in which the bed nucleus of the stria terminalis is involved; Walker et al., 2003) and cognitive changes (e.g., hippocampal complex [memory] and visual cortices [attention]; see Adolphs, 2004; Dolcos et al., 2004).”
BackgroundIn vivo-assessment of the human temporal network: Evidence for asymmetrical effective connectivity
Novitskaya, Y., Dümpelmann, M., Vlachos, A., Reinacher, P., & Schulze-Bonhage, A. (2020) · NeuroImage · doi:10.1016/j.neuroimage.2020.116769 · Cited by 19
The impact of focused attention on subsequent emotional recollection: A functional MRI investigation
Dolcos, F., Katsumi, Y., Bogdan, P. C., Shen, C., Jun, S., Buetti, S., Lleras, A., Bost, K. K., Weymar, M., & Dolcos, S. M. (2020) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2020.107338 · Cited by 20
Self-citationPreparing for the worst: Evidence that older adults proactively downregulate negative affect
Corbett, B., Rajah, M. N., & Duarte, A. (2018) · bioRxiv · doi:10.1101/359901 · Cited by 19
“The “modulation hypothesis of emotional memory” states that the emotional arousal of negative images induces the secretion of stress hormones that enhances activity in both the amygdala and medial temporal lobe, thereby modulating memory consolidation (Dolcos et al. 2004; McGaugh 2004), thus greater memory for negativ…”
BackgroundGender Differences of Brain Activity in the Conflicts Based on Implicit Self-Esteem
Miyamoto, R., & Kikuchi, Y. (2012) · PLoS ONE · doi:10.1371/journal.pone.0037901 · Cited by 18
“Hippocampus is also related to emotional memory retrieval [60][61], and its activity might be Figure 3.”
BackgroundXu, L., Sun, X.-R., Depoortere, I., Lu, J., Guo, F.-F., & Peeters, T. (2008) · Peptides · doi:10.1016/j.peptides.2007.12.002 · Cited by 19
Wang, H., Zhao, Q., Zhang, Y., Ma, J., Lei, M., Zhang, Z., Xue, H., Liu, J., Sun, Z., Xu, J., et al. (2024) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2024.111121 · Cited by 21
The role of value in the attentional boost effect
Swallow, K. M., & Atir, S. (2018) · Quarterly Journal of Experimental Psychology · doi:10.1177/1747021818760791 · Cited by 21
“…2014; Wittmann et al., 2005), and the interaction of systems involved in learning and representing value and those involved in episodic memory (Dolcos et al., 2004; Euston, Gruber, & McNaughton, 2012; Koster, Guitart-Masip, Dolan, & Düzel, 2015; Shohamy & Adcock, 2010; Tompary, Duncan, &…”
BackgroundResultInfluentialDew, I. T. Z., Ritchey, M., LaBar, K., & Cabeza, R. (2013) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2013.12.012 · Cited by 18
“The current fMRI study investigated the neural mechanisms of this effect by testing how neural activations during emotional memory retrieval are influenced by the prior encoding strategy.”
BackgroundSelf-citationTowards a Theoretical Neuroscience: from Cell Chemistry to Cognition
Coward, L. (2013) · Springer Series in Cognitive and Neural Systems · doi:10.1007/978-94-007-7107-9 · Cited by 18
Risk for Eating Disorders Modulates Startle-Responses to Body Words
Herbert, C., Kübler, A., & Vögele, C. (2013) · PLoS ONE · doi:10.1371/journal.pone.0053667 · Cited by 18
“Reading of body words lead to activity changes in the amygdala and in parahippocampal brain regions involved in autobiographical memory retrieval [16], while these activity changes were correlated with participants’ scores on the Eating Disorder Inventory, see also [17].”
ResultPersonality traits predict response to novel and familiar stimuli in the hippocampal region
Naghavi, H. R., Lind, J., Nilsson, L., Adolfsson, R., & Nyberg, L. H. (2009) · Psychiatry Research Neuroimaging · doi:10.1016/j.pscychresns.2008.09.011 · Cited by 18
“This viewwas supported by subsequent genetic studies, although the results were not replicated in all investigations (reviewed in Ebstein, 2006).”
Reiterer, S., Kogan, V. V., Seither-Preisler, A., & Pesek, G. (2020) · The Psychology of learning and motivation/The psychology of learning and motivation · doi:10.1016/bs.plm.2020.02.003 · Cited by 18
Cruz-Garza, J. G., Sujatha-Ravindran, A., Kopteva, A. E., Rivera-Garza, C., & Contreras-Vidal, J. (2020) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2020.577651 · Cited by 17
“…areas involved in the processing of multisensory inputs (Perrodin et al., 2014; Schapiro et al., 2014) and episodic emotional memory integration (Dolcos et al., 2004, 2005; Lech and Suchan, 2013) in the temporal lobe as participants explore their surroundings actively engaging the frontal…”
BackgroundPedale, T., Macaluso, E., & Santangelo, V. (2019) · Brain Structure and Function · doi:10.1007/s00429-019-01873-1 · Cited by 20
“, the dorsolateral prefrontal cortex; Uddin 2015), short- and long-term memories (e.g., the medial temporal lobe and the hippocampus; Dolcos et al. 2004), and decision-making (e.”
Li, X.-Z., Weissman, M., Talati, A., Svob, C., Wickramaratne, P., Posner, J., & Xu, D.-R. (2019) · Brain and Behavior · doi:10.1002/brb3.1209 · Cited by 17
Xu, H.-F., Zhang, Q., Li, B.-B., & Guo, C.-Y. (2015) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2015.00650 · Cited by 17
“…in encoding stage at midline central areas and topographic maps of “high-arousal”—“low-arousal” difference from 500–800 ms. whereas neutral and pleasant stimuli are recognized only based on familiarity (Ochsner, 2000; Dolcos et al., 2004; Johansson et al., 2004; Kensinger and Corkin, 2004).”
Torres, I., Keedy, S., Marlow-O’Connor, M., Beenken, B., & Goldman, M. (2009) · Neuropsychology · doi:10.1037/a0014481 · Cited by 17
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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