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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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“All participants provided written informed consent under a protocol approved by the Institutional Ethics Review Board.”
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“Indeed, emotion has been shown to impact attention [1], [2], [3], memory [4], [5], [6], [7], perception [8], [9], and decision-making [10], [11], [12].”
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“…account, which replicates many studies showing that the memory-enhancing effect of emotion is mediated by the process of recollection rather than familiarity (Ochsner, 2000; Kensinger and Corkin, 2003; Dolcos et al., 2004, 2005; Sharot et al., 2004, 2007; Weymar et al., 2009; Rimmele et al., 2012).”
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“…counterparts, the musical excerpts might induce both the encoding of novel information as well as the retrieval of episodes (Eldridge et al., 2005), which might particularly lead to increased activity in the hippocampus if themusic is associated with emotional events (Dolcos et al., 2004).”
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“A more recent study (Dolcos et al., 2004) supports the idea that interactions between the amygdala and the medial temporal lobe (MTL) memory system underlie the emotional enhancement of memory, and suggests that more anterior parts of the MTL have a specific role in encoding emotional information.”
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“…www.frontiersin.org May 2013 | Volume 7 | Article 42 | 7 (reviewed by Phelps, 2004), often focusing on the correlations or co-activations between the amygdala and the hippocampus during the formation or retrieval of an emotional memory (e.g., Dolcos et al., 2004; Kensinger and Corkin, 2004).”
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“…involved normalization to a template and smoothing, as typically performed for whole-brain analyses, defining structures based on stricter anatomical landmarks similar to our previous studies (e.g., Dolcos et al., 2004) was not necessary; hence, all activations were defined at the group level.”
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“…should be addressed to Bryan A. Strange, Wellcome Department of Imaging Neuroscience, Functioning Imaging Laboratory, 12 Queen Square, London WC1N 3BG, UK; e-mail: bstrange@fil.ion.ucl.ac.uk # 2006 Psychology Press Ltd http://www.psypress.com/cogneuropsychiatry DOI:10.1080/13546800500305096”
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“…thought to arise from the beneficial influence of emotion on the initial encoding of a memory trace (Canli, Zhao, Brewer, Gabrieli, & Cahill, 2000; Dolcos et al., 2004a; Kensinger & Corkin, 2004) and its consolidation, or strengthening, over time (Hamann, Ely, Grafton, & Kilts, 1999; Kleinsmith &…”
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“…especially for personally experienced traumatic events (Sharot, Martorella, Delgado, & Phelps, 2007). fMRI has revealed that memory recall is enhanced for emotional items (Kensinger & Schacter, 2005), especially when the amygdala and hippocampus show coactivation (Dolcos, LaBar, & Cabeza, 2004).”
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“Pleasurable experiences are particularly memorable because activations of the amygdala and hippocampus are involved in both emotional arousal and in passing information from short- to long-term memory (e.g., Dolcos, LaBar, and Cabeza 2004).”
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“The expected negative correlations were revealed between extraversion and BCi in bilateral MTG. MTG was found to participate in both emotional processing and encoding tasks (Critchley et al., 2000; Dolcos et al., 2004; Olson et al., 2007).”
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“Coupled activation of the amygdala and hippocampus in particular has been implicated in encoding and retrieval of emotional information (Dolcos et al., 2004; Erk et al., 2005; Richardson et al., 2004; Smith et al., 2006).”
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“Corresponding neuroimaging work has shown that this enhancement is associated with increased activity in the amygdala (Dolcos, LaBar, & Cabeza, 2004a; Dolcos et al., 2004b; Dolcos, LaBar, & Cabeza, 2005).”
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“We observed reliably greater recall for both positive and negative items which is consistent with a large body of literature (Dolcos et al., 2004; Kensinger & Schacter, 2006).”
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“According to previous studies, negative items attract more attention and lead to a facilitation in encoding, thus negative information can be elaborated better than neutral items into memory (Dolcos et al., 2004, 2005; Kensinger & Corkin, 2003).”
Emotional enhancement effect of memory: removing the influence of cognitive factors.Preprint
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“A consistent finding of positron emission tomography (PET) and functional magnetic resonance imaging (fMRI) studies is enhanced amygdala activity as well as amygdala–hippocampal connectivity for the subsequently remembered arousing stimuli (Cahill et al. 1996; Canli et al. 2000; Kilpatrick and Cahill 2003; Dolcos et a…”
BackgroundMental Imagery and Brain Regulation—New Links Between Psychotherapy and Neuroscience
Skottnik, L., & Linden, D. E. J. (2019) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2019.00779 · Cited by 70
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The role of the amygdala in bipolar disorder development
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Emotions and Memory in Borderline Personality Disorder
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“…(Lang et al., 1998), and has a strong effect on cognition, enhancing attention (Davis and Whalen, 2001; Fox et al., 2001) and also memory, via the increased activation of the amygdala and hippocampus (Cahill et al., 1996; Dolcos et al., 2004; Kensinger and Schacter, 2006; Richardson et al., 2004).”
BackgroundAdaptation to Conflict via Context-Driven Anticipatory Signals in the Dorsomedial Prefrontal Cortex
Horga, G., Maia, T. V., Wang, P., Wang, Z., Marsh, R., & Peterson, B. S. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.2783-11.2011 · Cited by 57
“We used case-wise exclusion of missing values for all behavioral analyses.”
MethodMental Hoop Diaries: Emotional Memories of a College Basketball Game in Rival Fans
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Self-citationThe Cognitive Neuroscience of True and False Memories
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“Consistent with previous studies in healthy samples (Dolcos et al., 2004; Hamann et al., 1999), we observed an enhancing effect of emotion on cued recall performance, such that participants recalled more negative and positive than neutral items.”
BackgroundResultInfluentialZhao, K., Xie, H., Fonzo, G. A., Tong, X., Carlisle, N. B., Chidharom, M., Etkin, A., & Zhang, Y. (2023) · Molecular Psychiatry · doi:10.1038/s41380-023-01958-8 · Cited by 45
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“…effect of pain on cognitive processes (Eccleston and Crombez, 1999) is a well-established phenomenon induced by both acute and chronic pain states (Eccleston, 1995; Kuhajda et al., 2002; Grisart et al., 2007; Moore et al., 2012) and has been shown to affect different cognitive domains such as…”
Schwabe, L., Nader, K., & Pruessner, J. C. (2012) · Biological Psychology · doi:10.1016/j.biopsycho.2012.10.003 · Cited by 54
Shafer, A. T., & Dolcos, F. (2012) · Frontiers in Integrative Neuroscience · doi:10.3389/fnint.2012.00070 · Cited by 47
“…AMY-HC engagement is associated with emotional memory following a shallow level of processing during encoding, whereas areas previously shown to be modulated by attention were more sensitive to emotional memory under a deep level of processing (Dolcos et al., 2004a,b, 2011; Ritchey et al., 2011).”
BackgroundMethodResultInfluentialSelf-citationIs the content of confabulation positive? An experimental study.
Fotopoulou, A., Conway, M., Tyrer, S., Birchall, D., Griffiths, P., & Solms, M. (2008) · Cortex; a journal devoted to the study of the nervous system and behavior · doi:10.1016/j.cortex.2007.03.001 · Cited by 47
“…control and regulation of both positive and negative emotions, while emotionally arousing memory is mediated by an amygdala-based neural substrate (for discussions see Bechara et al., 2000; Dolcos et al., 2004; Hurlemann et al., 2005; Kensinger and Corkin, 2004; Rolls, 2000; Piefke et al., 2003).”
BackgroundHuang, M., Risling, M., & Baker, D. G. (2015) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2015.02.008 · Cited by 49
“Corcoran and Maren, 2001) and reduced connectivity to the mygdala (Dolcos et al., 2004; McGaugh, 2004) may underie impairments in contextual memory processing and the bility to inhibit intrusive memories (Shin et al., 2004a), lthough findings have been mixed (Hughes and Shin, 2011). recent…”
BackgroundDissociable medial temporal pathways for encoding emotional item and context information
Ritchey, M., Wang, S.-F., Yonelinas, A. P., & Ranganath, C. (2018) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2018.12.015 · Cited by 49
“…is correlated with that in the hippocampus (Dolcos et al., 2004; Hamann et al., 1999; Kensinger & Corkin, 2004) and entorhinal or perirhinal cortex (Dolcos et al., 2004; Ritchey et al., 2008), but these relationships have not been directly related to trial-specific recollection and source memory…”
InfluentialStructural connectivity of the developing human amygdala
Saygin, Z. M., Osher, D. E., Koldewyn, K., Martin, R. E., Finn, A., Saxe, R., Gabrieli, J. D. E., & Sheridan, M. (2015) · PLoS ONE · doi:10.1371/journal.pone.0125170 · Cited by 45
“Given the functional role of these regions in contextual processing and memory formation, these findings may imply an increasing role for the amygdala in integrating emotional content during contextual processing and memory encoding ([59]; [60]; [61]; [62].”
BackgroundAversive memory formation in humans involves an amygdala-hippocampus phase code
Costa, M., Lozano‐Soldevilla, D., Gil‐Nagel, A., Toledano, R., Oehrn, C. R., Kunz, L., Yebra, M., Méndez‐Bértolo, C., Stieglitz, L. H., Sarnthein, J., et al. (2022) · Nature Communications · doi:10.1038/s41467-022-33828-2 · Cited by 52
The limits of arousal's memory impairing effects on nearby information
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“However, encoding of emotional stimuli increases functional activation in the anterior, rather than posterior, subregion of the hippocampus (Dolcos et al., 2004; Small et al., 2011), whereas the present study found that altered hippocampal volume was associated with functional activity in a more…”
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“For biologically salient information, amygdala activation enhances hippocampal dependent memory functions (Dolcos et al., 2004). van Wingen et al. (2010) investigated memory formation and retrieval of happy and neutral face stimuli in depression.”
A comprehensive protocol for manual segmentation of the medial temporal lobe structures.
Moore, M., Hu, Y., Woo, S., O'Hearn, D., Iordan, A., Dolcos, S., & Dolcos, F. (2014) · Journal of Visualized Experiments · doi:10.3791/50991 · Cited by 43
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“For instance, Greenberg et al. (2005) showed that the retrieval of pleasant autobiographical memories in response to personally tailored cue words elicited activation of the amygdala, hippocampus, and frontal lobes.”
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Eye movement during retrieval of emotional autobiographical memories
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The Influence of Menstrual Cycle and Androstadienone on Female Stress Reactions: An fMRI Study
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Emotion enhanced retention of cognitive skill learning.
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Quantitative evaluation of persuasive appeals using comparative meta-analysis
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Working and short-term memories are impaired in postpartum depression.
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Distinct Medial Temporal Lobe Network States as Neural Contexts for Motivated Memory Formation
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“Similarly, studies directly investigating interactions of the amygdala and MTL have demonstrated that successful encoding of emotional memories were associated with amygdala-cortical MTL functional interactions (Dolcos et al. 2004; Ritchey et al. 2008), but not amygdalahippocampus interactions.”
Żurawicki, L. (2010) · Springer eBooks · doi:10.1007/978-3-540-77829-5_1 · Cited by 73
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The neural fate of neutral information in emotion-enhanced memory.
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Emotional memory in schizophrenia.
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“…neuroimaging studies have shown that activation of the lateral prefrontal cortex accompanies memory enhancement for affectively valenced stimuli even if these are of low arousal (Kensinger & Corkin, 2004), an effect that may be enhanced for emotionally arousing stimuli (Dolcos et al., 2004a).”
BackgroundMoscovitch, M., Westmacott, R., Gilboa, A., Addis, D. R., Rosenbaum, R. S., Viskontas, I. V., Priselac, S., Svoboda, E., Ziegler, M., Black, S. E., et al. (2006) · Springer eBooks · doi:10.1007/4-431-27431-6_14 · Cited by 29
“Concurrently, neuroimaging studies appeared which showed that the hippocampus was activated preferentially during recognition of items that were recollected as compared to those which were only considered familiar (Dolcos et al., 2002; Eldridge, Knowlton, Furmanski, Bookheimer, & Engel, 2000; Davachi, Mitchell, & Wagn…”
BackgroundEnhanced right amygdala activity in adolescents during encoding of positively-valenced pictures
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Neural correlates of emotional recognition memory in schizophrenia: effects of valence and arousal.
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“…activations in all experimental conditions (positive, negative, high and low arousal) in medial temporal cortex, as well as prefrontal regions previously implicated in emotion processing and memory (medial, middle frontal and orbitofrontal cortex) (LeDoux, 1993; Dolcos et al., 2004a, 2004b).”
BackgroundNoradrenergic-glucocorticoid modulation of emotional memory encoding in the human hippocampus
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“…between emotion and memory processes may be attributable to interaction of brain structures in the medial temporal lobe (MTL) including the amygdala and hippocampus, which are known to be important for emotion and declarative memory, respectively (Dolcos et al., 2004; Richardson et al., 2004).”
BackgroundLinking enhancing and impairing effects of emotion—the case of PTSD
Dolcos, F. (2013) · Frontiers in Integrative Neuroscience · doi:10.3389/fnint.2013.00026 · Cited by 37
“It is also possible that increased distraction from ongoing goals produced by task-irrelevant emotional stimuli may lead to better memory for the distracting information itself.”
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The Memory Enhancing Effect of Emotion: Functional Neuroimaging Evidence
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“Moreover, Dolcos et al. (2004a) found that emotional arousal enhanced successful encoding activity (Dm) in two subregions of the left lateral PFC: one ventral (BA 47) and the other dorsal (BA 9/6).”
BackgroundMethodInfluentialSelf-citationAstrocyte Role in Temporal Lobe Epilepsy and Development of Mossy Fiber Sprouting
Twible, C., Abdo, R., & Zhang, Q. (2021) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2021.725693 · Cited by 44
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Meaningful inhibition: Exploring the role of meaning and modality in response inhibition
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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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