ReviewInteracting brain systems modulate memory consolidation
Highlights
► Stress hormones contribute to fight-or-flight response and enhance memory for important events. ► The vagus nerve bridges the peripheral stress response with memory processes in the brain. ► The amygdala influences synaptic strength in other areas of the brain that are involved in memory. ► Results reveal potential underlying causes of and therapies for stress-related memory disorders.
Introduction
“The usefulness of all the passions consists in their strengthening and prolonging in the soul thoughts which are good for it to conserve…”
Descartes, The Passions of the Soul, (1647)
The profound effect of emotion on memory storage was recognized long before the days of Descartes. In fact, it was said that throwing a child into a river after witnessing an important event, such as a wedding or granting of land to a township, was a medieval method for encouraging a lasting memory of the occasion (McGaugh, 2003). Considerable attention has been devoted to understanding the impact of emotional arousal on brain systems that store new experiences into long-term memory. Emotional arousal serves an important role in memory processing by first initiating attentional (Revelle and Loftus, 1992, Walker, 1958) and metabolic (Ekman et al., 1983, Witvliet and Vrana, 1995) resources that permit organisms to adapt rapidly to environmental challenges. Physiological changes recruited to mobilize resources for immediate responses also serve a second crucial function. They modulate brain processes to ensure that significant experiences are stored effectively into long-term memory. Thus, emotional arousal serves an important adaptive role in initiating rapid responses to momentary fluctuations in environmental conditions, and in regulating neural representations of these changes. This review discusses experimental approaches and relevant findings that provide the foundation for current understanding of coordinated interactions between arousal activated peripheral hormones and brain processes that modulate memory formation.
Section snippets
Effects of arousal on peripheral hormones and central norepinephrine
Emotional arousal produced by aversive stressors or highly rewarding events results in the release of epinephrine (adrenalin) and glucocorticoids (cortisol; corticosterone in rats) from the adrenal glands (Roozendaal et al., 2009a). Drugs and other treatments that increase concentrations of epinephrine or glucocorticoids during, or following, learning enhance memory in rats and mice (Gold and van Buskirk, 1978, Introini-Collison et al., 1992, Jurado-Berbel et al., 2010, King and Williams, 2009,
Pathways for conveying effects of arousal hormones on the brain
Findings indicating that amygdala norepinephrine levels are sensitive to epinephrine secretion provide strong evidence suggesting that emotion-induced secretion of epinephrine facilitates memory by direct actions on the amygdala. However, this implication is complicated by evidence that, even in highly stressful situations, epinephrine does not pass from the peripheral circulation into the brain (Arai et al., 1981, Pluta et al., 1994). As such, an understanding of how emotional arousal affects
The amygdala modulates memory consolidation by interacting with other brain regions
As discussed above, extensive evidence indicates that activation of the amygdala by stress hormones modulates the consolidation of emotionally arousing memories. It does not follow, however, that memory should be impaired by the loss of the amygdala, or that the amygdala is the site of storage of emotionally arousing memories. Inactivation of the amygdala prior to training or retention does not impair performance on a spatial water maze task, or a spatial win-shift or win-stay,
Synaptic mechanisms of amygdala modulation of long-term memory
As discussed above, considerable evidence indicates that amygdala modulation of memory consolidation involves influences on other brain regions, but little is known about the synaptic mechanisms of this interaction. One way to observe the effects of BLA activity on synaptic activity elsewhere in the brain is to measure expression of immediate early genes (IEGs) that are rapidly induced in response to synaptic activity. The IEG Arc (also Arg 3.1) is of particular interest as it appears to be a
Clinical relevance
“The usefulness of all the passions consists in their strengthening and prolonging in the soul thoughts which are good for it to conserve… and all the harm they can do consists in their strengthening and conserving these thoughts more than is necessary”
Descartes, The Passions of the Soul, (1647)
The knowledge garnered from the studies described above may contribute to the development of treatments for individuals suffering from memory and anxiety disorders. Firstly, it informs research designed
Conclusions
The amygdala is well-positioned to translate sympathetic arousal into synaptic plasticity that is distributed throughout the brain. A physiological mechanism to promote brain plasticity and rapid consolidation of memory for events that have a bearing on survival and well-being can have both adaptive and maladaptive implications. Here, we propose that the sympathetic “fight or flight” response goes beyond the peripheral nervous system by implementing epinephrine stimulation of the vagus nerve,
Acknowledgements
This work was supported by National Institute of Mental Health grants MH 12526-43 (JLM) and MH 086960-01A1 (CKM), and the National Science Foundation, through grant NSF-0720170 (CLW). CKM is also supported by MicroTransponder.
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