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. 2006 Apr 25;103(17):6741-6.
doi: 10.1073/pnas.0601874103. Epub 2006 Apr 12.

Glucocorticoid enhancement of memory requires arousal-induced noradrenergic activation in the basolateral amygdala

Benno Roozendaal  1 , Shoki Okuda, Eddy A Van der Zee, James L McGaugh
Affiliations

Glucocorticoid enhancement of memory requires arousal-induced noradrenergic activation in the basolateral amygdala

Benno Roozendaal et al. Proc Natl Acad Sci U S A. .

Abstract

Considerable evidence indicates that glucocorticoid hormones enhance the consolidation of long-term memories for emotionally arousing experiences but not that for less arousing or neutral information. However, previous studies have not determined the basis of such arousal-induced selectivity. Here we report the finding that endogenous noradrenergic activation of the basolateral complex of the amygdala (BLA) induced by emotional arousal is essential in enabling glucocorticoid memory enhancement. Corticosterone administered immediately after object recognition training enhanced 24-h memory of naïve male rats but not that of rats previously habituated to the training context in order to reduce novelty-induced emotional arousal. The beta-adrenoceptor antagonist propranolol administered either systemically or into the BLA blocked the corticosterone-induced memory enhancement. Further, in habituated rats, corticosterone activated BLA neurons, as assessed by phosphorylated cAMP response element binding (pCREB) immunoreactivity levels, and enhanced memory only when norepinephrine release was stimulated by administration of the alpha(2)-adrenoceptor antagonist yohimbine. These findings strongly suggest that synergistic actions of glucocorticoids and emotional arousal-induced noradrenergic activation of the BLA constitute a neural mechanism by which glucocorticoids may selectively enhance memory consolidation for emotionally arousing experiences.

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Conflict of interest statement

Conflict of interest statement: No conflicts declared.

Figures

Fig. 1.
Fig. 1.
Glucocorticoid effects on memory consolidation for object recognition training require noradrenergic activation. Data represent discrimination index (%) on a 24-h retention trial, expressed as mean ± SEM. (A) Effects of immediate posttraining administration of the β-adrenoceptor antagonist propranolol (3.0 mg/kg, s.c.) on corticosterone-induced enhancement of object recognition memory in naïve rats. ∗∗, P < 0.0001 vs. vehicle (n = 8–12 per group). (B) Effect of coadministration of the α2-adrenoceptor antagonist yohimbine (0.3 mg/kg, s.c.) with corticosterone on object recognition memory in habituated rats. ∗∗, P < 0.0001 vs. vehicle (n = 9–17 per group). (B Inset) Effect of posttraining injections of yohimbine (0.3 mg/kg, s.c.) and corticosterone (1.0 mg/kg, s.c.) separated by a 4-h delay. Y→C, yohimbine administered immediately after training and corticosterone 4 h later; C→Y, corticosterone administered immediately after training and yohimbine 4 h later.
Fig. 2.
Fig. 2.
Activation of β-adrenoceptors in the BLA, but not the hippocampus, is required for enabling corticosterone effects on object recognition memory. Data represent discrimination index (%) on a 24-h retention trial, expressed as mean ± SEM. (A and B) Diagram and photomicrograph illustrating placement of infusion needle tip in the BLA and hippocampus. The arrow points to the needle tip. (C) Effect of posttraining administration of the β-adrenoceptor antagonist propranolol (0.5 μg per hemisphere) into the BLA on corticosterone-induced enhancement of object recognition memory in nonhabituated rats. ∗∗, P < 0.0001 vs. vehicle (n = 8–11 per group). (D) Effect of posttraining administration of the β-adrenoceptor antagonist propranolol (1.25 μg per hemisphere) into the hippocampus on corticosterone-induced enhancement of object recognition memory in nonhabituated rats. ∗, P < 0.05; ∗∗, P < 0.0001 vs. vehicle (n = 10–14 per group).
Fig. 3.
Fig. 3.
Prior habituation attenuates the effects of object recognition training and corticosterone (Cort) injection on noradrenergic activity within the BLA. (A) Photomicrographs of the amygdala depicting pTHSer19 and pCREB immunostaining as assessed 3 h after training. Overviews of the amygdala of home cage controls (no prior habituation) (Top), and pTH (Middle) and pCREB (Bottom) in the BLA. (Top) The delineated areas indicate the regions analyzed for optical density (pTH) or cell counts (pCREB). (B and C) Summary of the immunocytochemistry data for the BLA and dentate gyrus (mean ± SEM). ∗, P < 0.05; ∗∗, P < 0.01 vs. home cage (for pTH) or vehicle/yohimbine (for pCREB); ♦♦, P < 0.001 prior habituation vs. corresponding no prior habituation group (n = 5–6 per group). CEA, central amygdala.
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