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The Journal of Neuroscience, November 11, 2009, 29(45):14299-14308; doi:10.1523/JNEUROSCI.3626-09.2009

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Behavioral/Systems/Cognitive
Glucocorticoid Effects on Memory Consolidation Depend on Functional Interactions between the Medial Prefrontal Cortex and Basolateral Amygdala

Benno Roozendaal,¹ Jayme R. McReynolds,² Eddy A. Van der Zee,³ Sangkwan Lee,⁴ James L. McGaugh,⁴ and Christa K. McIntyre²

¹Department of Neuroscience, Section Anatomy, University Medical Center Groningen, University of Groningen, 9713 AV Groningen, The Netherlands, ²School of Behavioral and Brain Sciences, University of Texas, Dallas, Dallas, Texas 75083, ³Department of Molecular Neurobiology, University of Groningen, 9750 AA Haren, The Netherlands, and ⁴Center for the Neurobiology of Learning and Memory, Department of Neurobiology and Behavior, University of California, Irvine, Irvine, California 92697-3800

Correspondence should be addressed to Benno Roozendaal, Department of Neuroscience, Section Anatomy, University Medical Center Groningen, University of Groningen, Antonius Deusinglaan 1, 9713 AV Groningen, The Netherlands. Email: b.roozendaal{at}med.umcg.nl

Considerable evidence indicates that the basolateral complex of the amygdala (BLA) interacts with efferent brain regions in mediating glucocorticoid effects on memory consolidation. Here, we investigated whether glucocorticoid influences on the consolidation of memory for emotionally arousing training depend on functional interactions between the BLA and the medial prefrontal cortex (mPFC), a brain region involved in higher-order cognitive and affective processing. The glucocorticoid receptor (GR) agonist 11β,17β-dihydroxy-6,21-dimethyl-17-pregna-4,6-trien-20yn-3-one (RU 28362) administered unilaterally into the left mPFC of male Sprague Dawley rats immediately after inhibitory avoidance training enhanced 48 h retention performance. An ipsilateral, but not contralateral, lesion of the BLA blocked the memory enhancement. In a second experiment, RU 28362 infused into the mPFC after inhibitory avoidance training increased BLA levels of phosphorylated extracellular signal-regulated kinase 1/2 (pErk1/2). Blockade of this pErk1/2 activity in the BLA with the mitogen-activated protein kinase kinase inhibitor PD98059 [2-(2-amino-3-methoxyphenyl)-4H-1-benzopyran-4-one] prevented the memory enhancement, suggesting that GR agonist administration into the mPFC enhances memory consolidation via modulation of BLA activity. Conversely, GR agonist infusions administered into the BLA posttraining increased pErk1/2 levels in the mPFC in regulating memory consolidation. Moreover, as assessed with a two-phase inhibitory avoidance procedure designed to separate modulatory influences on memory of context and footshock, posttraining GR agonist infusions into either the BLA or mPFC enhanced memory of the contextual as well as aversive information acquired during inhibitory avoidance training. These findings indicate that glucocorticoid effects on memory consolidation depend on bidirectional interactions between the BLA and mPFC.

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Received July 27, 2009; revised Sept. 15, 2009; accepted Sept. 29, 2009.

Correspondence should be addressed to Benno Roozendaal, Department of Neuroscience, Section Anatomy, University Medical Center Groningen, University of Groningen, Antonius Deusinglaan 1, 9713 AV Groningen, The Netherlands. Email: b.roozendaal{at}med.umcg.nl

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