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Cognitive neuroscience of emotional memory

Abstract

Emotional events often attain a privileged status in memory. Cognitive neuroscientists have begun to elucidate the psychological and neural mechanisms underlying emotional retention advantages in the human brain. The amygdala is a brain structure that directly mediates aspects of emotional learning and facilitates memory operations in other regions, including the hippocampus and prefrontal cortex. Emotion–memory interactions occur at various stages of information processing, from the initial encoding and consolidation of memory traces to their long-term retrieval. Recent advances are revealing new insights into the reactivation of latent emotional associations and the recollection of personal episodes from the remote past.

Key Points

  • Amygdala damage in humans reduces the memory-enhancing benefits of emotional arousal on consolidation processes and on attentional focusing during encoding.

  • Memories for stressful and emotionally arousing events benefit from moderate doses of adrenaline and cortisol released acutely at the time of encoding. These effects have been linked to amygdala function in human and non-human animal studies.

  • By contrast, chronic stress or high levels of acute stress hormones impair memory retrieval and hippocampal function, as exemplified by post-traumatic stress disorder.

  • Encoding of emotionally arousing events recruits amygdala activity and elicits greater functional interactions between the amygdala and medial temporal lobe memory regions, which result in enhanced long-term memory.

  • The interactions between the amygdala and medial temporal lobe memory regions extend to retrieval of remote memories, including those from the remote personal past.

  • Emotional memories are retrieved with an accompanying sense of recollection rather than familiarity, an effect that depends on co-activation of the amygdala and hippocampus.

  • The prefrontal cortex also has a role in the encoding and retrieval of emotional events and shows regional specialization for arousal and valence effects on memory.

  • Across various species, the acquisition of conditioned fear depends on the integrity of the amygdala and its interactions with the thalamus and cortical structures.

  • The extinction of fear behaviour requires a suppressive influence of the prefrontal cortex on amygdala function, and contextual cues processed by the hippocampus can reinstate extinguished fears. These cortical control mechanisms over emotional learning are thought to contribute to relapse of fears and phobias in anxiety disorders.

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Acknowledgements

Research was supported by grants from US National Institutes of Health and a US National Science Foundation CAREER award.

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Competing interests

The authors declare no competing financial interests.

Correspondence to Kevin S LaBar.

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Glossary

Arousal

A dimension of emotion that varies from calm to excitement.

Valence

A dimension of emotion that varies from unpleasant (negative) to pleasant (positive), with neutral often considered an intermediate value.

Declarative memory

(Or explicit memory). Conscious memories for events and facts that depend on the integrity of the MTL.

Non-declarative memory

(Or implicit memory). Various non-conscious memories that are independent of MTL function and are expressed as a facilitation in behavioural performance due to previous exposure.

Recollection

Episodic retrieval that is accompanied by recovery of specific contextual details about a past event.

Urbach–Wiethe syndrome

(Or lipoid proteinosis). A rare, hereditary, congenital disorder characterized by systemic deposits of hyaline material that are prominent in the skin, oral mucosa and pharynx. About 50% of all cases have additional intracranial deposits in the MTL, which occasionally target the amygdala selectively.

Working memory

A form of memory in which stimulus representations are actively maintained and/or manipulated in conscious awareness over a short period of time.

Dm effect

An index of brain activity at encoding that distinguishes subsequently remembered from subsequently forgotten items and is assumed to reflect successful encoding processes.

Familiarity

Episodic retrieval that is accompanied by a feeling that an event happened in the past, although no contextual details are available.

Biological preparedness theory

A theory proposed by Martin Seligman that considers phobias as arising from a selective set of biological associations that the organism is evolutionarily tuned ('prepared') to learn, which leads to rapid fear acquisition and persistence of fear.

Visual masking

A psychophysical technique that can be used to reduce perceptual awareness of visual stimuli by presenting them briefly (for typically <33 msec) on a computer screen or tachistoscope and immediately displaying another stimulus of equal or greater complexity ('backward' masking). Participants report seeing only the second stimulus, although the visual system processes aspects of the masked stimulus.

Renewal

After extinction training, conditioned fear can be renewed by presenting the conditioned stimulus in a novel context.

Reinstatement

After extinction training, conditioned fear can be reinstated by presenting the conditioned stimulus in a context in which a noxious or stressful stimulus was recently encountered.

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Figure 1: Potential mechanisms by which the amygdala mediates the influence of emotional arousal on memory.
Figure 2: β-Adrenergic receptor blockade in healthy adults during encoding produces similar deficits to amygdala damage on a test of emotional memory.
Figure 3: Two routes to emotional remembering: arousal- and valence-mediated subsequent memory effects.
Figure 4: Interactions between the amygdala and medial temporal lobe memory system during encoding predict emotional retention advantages and recollection-based emotional retrieval.
Figure 5: Successful retrieval of emotionally arousing memories from long-term storage depends on the amygdala and medial temporal lobe memory system.
Figure 6: Studies of patients with rare brain lesions reveal dissociable contributions of the amygdala and hippocampus to conditioned fear learning.
Figure 7: Functional neuroimaging of healthy adults during conditioned fear acquisition reveals activation in a thalamo–amygdalo–cingulate network.