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Stress, memory and the amygdala

Key Points

  • Emotionally arousing experiences tend to form strong memories and the amygdala has a pivotal role in this process.

  • Stress hormones and stress-activated neurotransmitter systems in the basolateral amygdala are crucially important in the consolidation of emotional memories.

  • A growing body of evidences points to a central role for noradrenaline in mediating the enhancing effects of adrenal stress hormones, such as adrenaline and glucocorticoids, on the consolidation of emotional memories.

  • Basolateral amygdala activity affects memory consolidation and neural plasticity in other brain regions (for example, the hippocampus and various neocortical regions).

  • The basolateral amygdala, and its interactions with the hippocampus and prefrontal cortex, also plays a part in the stress-induced impairment of memory retrieval and working memory.

  • The same amygdala mechanisms that facilitate the robust encoding of emotionally salient memories can become maladaptive under conditions of traumatic and chronic stress.

  • Chronic stress triggers patterns of structural plasticity in the basolateral amygdala, which are strikingly different from those seen in the hippocampus and prefrontal cortex. Chronic immobilization stress leads to dendritic growth and spinogenesis in principal neurons of the basolateral amygdala.

  • Stress-induced neuronal remodelling in animal models reveals unique features of structural plasticity in the amygdala that could be of relevance to studies of humans with mood disorders and post-traumatic stress disorder.

Abstract

Emotionally significant experiences tend to be well remembered, and the amygdala has a pivotal role in this process. But the efficient encoding of emotional memories can become maladaptive — severe stress often turns them into a source of chronic anxiety. Here, we review studies that have identified neural correlates of stress-induced modulation of amygdala structure and function — from cellular mechanisms to their behavioural consequences. The unique features of stress-induced plasticity in the amygdala, in association with changes in other brain regions, could have long-term consequences for cognitive performance and pathological anxiety exhibited in people with affective disorders.

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Figure 1: The main subdivisions of the amygdala and their intrinsic and extrinsic connections.
Figure 2: Glucocorticoid effects on memory consolidation for object recognition training require arousal-induced noradrenergic activation.
Figure 3: Emotional arousal-induced modulation of memory consolidation.
Figure 4: A brief exposure to stress triggers a delayed increase in anxiety and spine density in the BLA.
Figure 5: Effects of acute and chronic stress on BLA principal neurons.

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Acknowledgements

Research was supported by National Science Foundation Grant IOS-0618211 (B.R.), United States Public Health Service Grants MH41256 and MH58911 (B.Mc.), the National Centre for Biological Sciences (S.C.) and an International Senior Research Fellowship from The Wellcome Trust (S.C.).

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Correspondence to Benno Roozendaal.

Glossary

Inhibitory avoidance task

A learning task in which animals are placed in a small starting compartment or on a small platform and receive a single footshock after entering a larger compartment or stepping down from the platform. Memory of the one-trial training experience is usually tested by placing the animals back in the same position and recording the delay before they move to the place where they received the footshock.

Contextual fear conditioning

A learning paradigm in which animals are placed in a piece of apparatus and given a series of footshocks. Memory of the training experience is typically assessed by measuring how long the animals freeze when they are subsequently replaced in the apparatus.

Water-maze task

A spatial learning and memory task that depends on the hippocampus. Rodents are trained to learn the location of an escape platform that is hidden beneath the surface in a pool of water. The cued version of the water maze task measures a form of implicit learning and memory that depends on the caudate nucleus; here, animals are trained to swim to a visible platform that is moved from one location to another across trials.

Pavlovian or classical fear conditioning

A robust learning paradigm in which an animal rapidly learns to associate a previously neutral or innocuous sensory stimulus (conditioned stimulus), such as light or an auditory tone, with a coincident aversive stimulus (unconditioned stimulus) such as a mild footshock. Subsequent exposure to the same conditioned stimulus or cue alone elicits a conditioned response (freezing) that provides a measure of the learned association.

Iontophoresis

A process by which charged molecules are ejected onto tissue by passing electric current through the electrolyte solution containing the molecules. This causes a spurt of charged molecules to be transported out of the pipette tip.

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Roozendaal, B., McEwen, B. & Chattarji, S. Stress, memory and the amygdala. Nat Rev Neurosci 10, 423–433 (2009). https://doi.org/10.1038/nrn2651

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