Cited by 714Memory and Neural MechanismsMemory Processes and InfluencesNeural and Behavioral Psychology Studies

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Interaction between the Amygdala and the Medial Temporal Lobe Memory System Predicts Better Memory for Emotional Events

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Dolcos, Florin, LaBar, Kevin S, Cabeza, Roberto·2004·Neuron

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Abstract

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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The Medial Temporal Lobe Memory System
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Changes in blood glucose and salivary cortisol are not necessary for arousal to enhance memory in young or older adults.
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The Hippocampal System as the Cortical Resource Manager: A Model Connecting Psychology, Anatomy and Physiology
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“The amygdala, an evolutionarily conserved brain area, in humans encodes episodic memory and subjective evaluation of emotional faces rather than just visual elements (Dolcos et al., 2004; Wang et al., 2014).”
Awake ripples enhance emotional memory encoding in the human brain
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“2a, b, 3, 6, 8b, 9, 14), mitigating the possibility of outliers affecting the study conclusions.”
Negative emotions enhance memory-guided attention in a visual search task by increasing frontoparietal, insular, and parahippocampal cortical activity
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“…and parahippocampal cortices; Hamann, Ely, Grafton, & Kilts, 1999; Canli, Zhao, Brewer, Gabrieli, & Cahill, 2000; Kilpatrick & Cahill, 2003; Dolcos et al., 2004; Richardson, Strange, & Dolan, 2004; Dolcos & Denkova, 2014) or by indirect top-down (attention-related) mechanisms involving the…”
Effects of posed smiling on memory for happy and sad facial expressions
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“…(Bradley et al., 1992; Chiu et al., 2013), which, on a neural level, is associated with increased activity of the amygdala and the hippocampal formation during both encoding and retrieval (Dolcos et al., 2004, 2005, 2012; Kensinger and Schacter, 2005; Murty et al., 2010; Shafer and Dolcos, 2014).”
Background
Musicogenic seizures in temporal lobe epilepsy: Case reports based on ictal source localization analysis
Bratu, I., Nica, A. E., Oane, I., Daneasa, A., Stoica, S., Barborică, A., & Mı̂ndruță, I. (2023) · Frontiers in Neurology · doi:10.3389/fneur.2023.1072075 · Cited by 10
Resting-state functional connectivity does not predict individual differences in the effects of emotion on memory
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Distinct stress‐related changes in intrinsic amygdala connectivity predict subsequent positive and negative memory performance
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“…negative information: Whereas the successful encoding of negative information has been linked to increased recruitment of visuosensory regions, the successful encoding of positive information is associated with frontal recruitment (e.g., Dolcos et al., 2004; Mickley Steinmetz & Kensinger, 2009).”
Background
Greater hippocampal gray matter volume in subjective hyperosmia: a voxel-based morphometry study
Han, P., Stiller-Stut, F. P., Fjældstad, A. W., & Hummel, T. R. (2020) · Scientific Reports · doi:10.1038/s41598-020-75898-6 · Cited by 9
The neural influence of autobiographical memory related to the parent-child relationship on psychological health in adulthood
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“In particular, the amygdala has been implicated in the encoding of emotional memories [15] as well as retrieval of autobiographical memories [16].”
Method
Progressively analogous evidence of covert face recognition from functional magnetic resonance imaging and skin conductance responses studies involving a patient with dissociative amnesia
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Viewing one’s body during encoding boosts episodic memoryPreprint
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Memory Performance for Everyday Motivational and Neutral Objects Is Dissociable from Attention
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“The appetitive and aversive objects in this study received higher arousal ratings than the neutral objects, and arousal has been found to enhance memory (e.g., Hamann et al., 1999; Dolcos et al., 2004; Mather and Sutherland, 2009).”
Background
Fear-relevant outcomes modulate the neural correlates of probabilistic classification learning
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“Emotional stimuli have the capacity to alter both attention and memory (Anderson, 2005; LaBar and Cabeza, 2006) and typically enhance declarative memory and MTL activation (Dolcos et al., 2004, 2005; Kensinger and Corkin, 2004).”
BackgroundSelf-citation
The Amygdala in Post-Traumatic Stress Disorder
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Neural basis underlying the trait of attachment anxiety and avoidance revealed by the amplitude of low-frequency fluctuations and resting-state functional connectivity
Deng, M., Zhang, X., Bi, X.-Y., & Gao, C.-H. (2021) · BMC Neuroscience · doi:10.1186/s12868-021-00617-4 · Cited by 8
Memory of my victory and your defeat: Contributions of reward- and memory-related regions to the encoding of winning events in competitions with others
Sugimoto, H., Dolcos, F., & Tsukiura, T. (2020) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2020.107733 · Cited by 8
Self-citation
Emotional scene processing in children and adolescents with attention deficit/hyperactivity disorder: a systematic review
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Predicting emotional arousal and emotional memory performance from an identical brain network
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“activation in the left medial prefrontal cortex (mPFC), including the rostral anterior cingulate cortex (rACC) as well as in the bilateral hippocampus and the left amygdala, regions that are typically involved in processing emotional content (Dolcos et al., 2004; Murty et al., 2010) and which are supposed to be dysfun…”
The role of the ventrolateral prefrontal cortex in emotional enhancement of memory: a TMS study
Weintraub-Brevda, R. R., & Chua, E. F. (2018) · Cognitive neuroscience · doi:10.1080/17588928.2018.1496905 · Cited by 8
“One possibility is that when full cognitive resources are less available, such as under divided attention, the main neural pathway supporting the EEM is the more automatic route, the amygdalar-hippocampal route (Dolcos et al., 2004a; Kensinger & Corkin, 2004; for review, Kensinger & Schacter, 2008).”
BackgroundInfluential
Influence of Temporal Expectations on Response Priming by Subliminal Faces
Pichon, S., Guex, R., & Vuilleumier, P. (2016) · PLoS ONE · doi:10.1371/journal.pone.0164613 · Cited by 8
Influence of empathetic pain processing on cognition in schizophrenia
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Background
Emotion, Stress, and Memory
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Background
Highly Superior Autobiographical Memory
Mcgaugh, J. (2017) · Elsevier eBooks · doi:10.1016/b978-0-12-809324-5.21047-x · Cited by 8
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“…in rats (Gomez-Chacon et al., 2012; Perugini et al., 2012; Santos et al., 2023), cats (Bauer et al., 2007; Collins et al., 2001; Paz et al., 2006), monkeys (Mogami & Tanaka, 2006; Ohyama, 2012) and people (Cooper et al., 2023; Dolcos et al., 2004; Mochizuki et al., 2020; Ritchey et al., 2008).”
Hippocampal subfield volumes in treatment resistant depression and serial ketamine treatment
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“Subfields within the anterior hippocampus, including CA3 and CA4/dentate, have been shown to be involved in pattern separation of emotionally charged stimuli (20), with fMRI research reporting activation in the anterior hippocampus in response to emotionally charged faces (45).”
Background
Phonaesthetics and personality—Why we do not only prefer Romance languages
Winkler, A.-M., Kogan, V. V., & Reiterer, S. (2023) · Frontiers in Language Sciences · doi:10.3389/flang.2023.1043619 · Cited by 7
“events, thanks to the amygdala, which enhances the function of the medial temporal lobe memory system (Dolcos et al., 2004).”
Background
Fisiología del estrés y su integración al sistema nervioso y endocrino.
Romero, E. E. R., Young, J., & Salado-Castillo, R. (2020) · doi:10.37416/rmc.v32i1.535 · Cited by 7
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Background
BOLD Activity During Correct-Answer Feedback in Cued Recall Predicts Subsequent Retrieval Performance: An fMRI Investigation Using a Partial Trial Design
Gilmore, A. W., Nelson, S. M., Naaz, F., Shaffer, R. A., & McDermott, K. (2018) · Cerebral Cortex · doi:10.1093/cercor/bhx264 · Cited by 7
“Importantly, the specific regions whose activity can predict SM performance are not fixed, but depend upon the nature of the encoding task or type of retrieval test (Otten and Rugg 2001a; Dolcos et al. 2004; Uncapher et al. 2006; Otten 2007).”
Background
Anatomical Variations of the Temporomesial Structures in Normal Adult Brain - A Cadaveric Study
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“Our initial hypothesis regarding the effect of arousal was derived from studies using free-recall paradigms that had consistently found memory to be better for high-arousal than low-arousal materials (Bradley et al., 1992; Bradley & Lang, 2000; Dolcos et al., 2004a,b; Palomba et al., 1997).”
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Authors: Dolcos, F., LaBar, K. S., & Cabeza, R.
Affiliations: University of Alberta (CA)
Duke University (US)
Corresponding author: Dolcos, Florin
ORCID: Dolcos, Florin
LaBar, Kevin S
Cabeza, Roberto
Venue: Neuron
Publisher: Elsevier BV
Published: 2004-06
Volume: 42
Issue: 5
Pages: 855-863
ISSN: 0896-6273 (ISSN-L)
DOI: 10.1016/s0896-6273(04)00289-2
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: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/open-access/userlicense/1.0/ (vor, 3333 d)
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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Interaction between the Amygdala and the Medial Temporal Lobe Memory System Predicts Better Memory for Emotional Events

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