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The Journal of Neuroscience, September 15, 2004, 24(37):8161-8169; doi:10.1523/JNEUROSCI.2574-04.2004

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Behavioral/Systems/Cognitive
Glucocorticoid Effects on Memory Retrieval Require Concurrent Noradrenergic Activity in the Hippocampus and Basolateral Amygdala

Benno Roozendaal,¹ Emily L. Hahn,¹ Sheila V. Nathan,¹ Dominique J.-F. de Quervain,² and James L. McGaugh¹

¹Center for the Neurobiology of Learning and Memory, Department of Neurobiology and Behavior, University of California, Irvine, California 92697-3800, and ²Division of Psychiatry Research, University of Zürich, 8029 Zürich, Switzerland

Previous findings indicate that administration of a-adrenoceptor antagonist systemically blocks glucocorticoid impairment of memory retrieval. Here, we report that -adrenoceptor activation in the hippocampus and the basolateral complex of the amygdala (BLA) is implicated in the impairing effects of glucocorticoids on memory retrieval. The specific glucocorticoid receptor (GR) agonist 11,17-dihydroxy-6,21-dimethyl-17-pregna-4,6-trien-20yn-3-one (RU 28362) (15 ng) infused into the hippocampus of male Sprague Dawley rats 60 min before water maze retention testing, 24 hr after training, impaired probe trial retention performance, as assessed by quadrant search time and initial latency to cross the platform location. Because we found previously that RU 28362 infused into the hippocampus does not affect water maze acquisition or immediate recall, the findings suggest that the GR agonist-induced retention impairment was attributable to a selective influence on long-term memory retrieval. Likewise, systemic injections of the ₁-adrenoceptor partial agonist xamoterol (3.0 or 10.0 mg/kg, s.c.) 60 min before the probe trial dose-dependently impaired retention performance. The -adrenoceptor antagonist propranolol (2.0 mg/kg) administered subcutaneously before retention testing did not affect retention performance alone, but blocked the memory retrieval impairment induced by concurrent intrahippocampal infusions of RU 28362. Pretest infusions of the ₁-adrenoceptor antagonist atenolol into either the hippocampus (1.25 µg in 0.5 µl) or the BLA (0.5 µg in 0.2 µl) also prevented the GR agonist-induced memory retrieval impairment. These findings suggest that glucocorticoids impair retrieval of long-term spatial memory by facilitating noradrenergic mechanisms in the hippocampus, and additionally, that norepinephrine-mediated BLA activity is critical in enabling hippocampal glucocorticoid effects on memory retrieval.

Key words: -adrenoceptor; corticosterone; emotional arousal; glucocorticoid receptor; norepinephrine; propranolol; atenolol; RU 28362; stress hormone; spatial memory; xamoterol

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Received May 11, 2004; revised July 26, 2004; accepted July 27, 2004.

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