The effect of exogenous cortisol during sleep on the behavioral and neural correlates of emotional memory consolidation in humans

Summary A host of animal work demonstrates that the retention benefit for emotionally aversive over neutral memories is regulated by glucocorticoid action during memory consolidation. Particularly, glucocorticoids may affect systems-level processes that promote the gradual reorganization of emotiona...

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Bibliographic Details
Published in:Psychoneuroendocrinology 2013-09, Vol.38 (9), p.1639-1649
Main Authors: van Marle, Hein J.F, Hermans, Erno J, Qin, Shaozheng, Overeem, Sebastiaan, Fernández, Guillén
Format: Article
Language:English
Subjects:
Adult
Amygdala
Amygdala - drug effects
Amygdala - physiology
Arousal
Behavioral psychophysiology
Biological and medical sciences
Cortisol
Double-Blind Method
Drug Administration Schedule
Emotion
Emotions - physiology
Endocrinology & Metabolism
fMRI
Fundamental and applied biological sciences. Psychology
Hormones and behavior
Humans
Hydrocortisone - administration & dosage
Hydrocortisone - analysis
Hydrocortisone - pharmacology
Hydrocortisone - physiology
Hydrocortisone - secretion
Magnetic Resonance Imaging
Male
Memory - physiology
Memory consolidation
Nootropic Agents - administration & dosage
Nootropic Agents - pharmacology
Polysomnography
Psychiatry
Psychology. Psychoanalysis. Psychiatry
Psychology. Psychophysiology
Recognition (Psychology) - drug effects
Recognition (Psychology) - physiology
Saliva - chemistry
Secretory Rate
Sleep
Sleep - drug effects
Sleep - physiology
Young Adult
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Summary:Summary A host of animal work demonstrates that the retention benefit for emotionally aversive over neutral memories is regulated by glucocorticoid action during memory consolidation. Particularly, glucocorticoids may affect systems-level processes that promote the gradual reorganization of emotional memory traces. These effects remain largely uninvestigated in humans. Therefore, in this functional magnetic resonance imaging study we administered hydrocortisone during a polysomnographically monitored night of sleep directly after healthy volunteers studied negative and neutral pictures in a double-blind, placebo-controlled, between-subjects design. The following evening memory consolidation was probed during a recognition memory test in the MR scanner by assessing the difference in brain activity associated with memory for the consolidated items studied before sleep and new, unconsolidated items studied shortly before test (remote vs. recent memory paradigm). Hydrocortisone administration resulted in elevated cortisol levels throughout the experimental night with no group difference at recent encoding or test. Behaviorally, we showed that cortisol enhanced the difference between emotional and neutral consolidated memory, effectively prioritizing emotional memory consolidation. On a neural level, we found that cortisol reduced amygdala reactivity related to the retrieval of these same consolidated, negative items. These findings show that cortisol administration during first post-encoding sleep had a twofold effect on the first 24 h of emotional memory consolidation. While cortisol prioritized recognition memory for emotional items, it reduced reactivation of the neural circuitry underlying emotional responsiveness during retrieval. These findings fit recent theories on emotional depotentiation following consolidation during sleep, although future research should establish the sleep-dependence of this effect. Moreover, our data may shed light on mechanisms underlying potential therapeutic effects of cortisol administration following psychological trauma.
ISSN:0306-4530
1873-3360
DOI:10.1016/j.psyneuen.2013.01.009