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The Journal of Neuroscience, December 8, 2004, 24(49):11029-11034; doi:10.1523/JNEUROSCI.3968-04.2004

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Behavioral Stress Modifies Hippocampal Synaptic Plasticity through Corticosterone-Induced Sustained Extracellular Signal-Regulated Kinase/Mitogen-Activated Protein Kinase Activation

Chih-Hao Yang,^1,2 Chiung-Chun Huang,¹ and Kuei-Sen Hsu^1,2

¹Department of Pharmacology and ²Institute of Basic Medical Sciences, College of Medicine, National Cheng Kung University, Tainan 701, Taiwan

The induction of hippocampal long-term synaptic plasticity is exquisitely sensitive to behavioral stress, but the underlying mechanisms are still unclear. We report here that hippocampal slices prepared from adult rats that had experienced unpredictable and inescapable restraint tail-shock stress showed marked impairments of long-term potentiation (LTP) in the CA1 region. The same stress promoted the induction of long-term depression (LTD). These effects were prevented when the animals were given the glucocorticoid receptor antagonist 11, 17-11[4-(dimethylamino)phenyl]-17-hydroxy-17-(1-propynyl)-estra-4-9-dien-3-one before the stress. Immunoblotting analyses revealed that stress induced a profound and prolonged extracellular signal-regulated kinase/mitogen-activated protein kinase (ERK1/2 MAPK) hyperphosphorylation through small GTPase Ras, Raf-1, and MAPK kinase 1/2 (MEK1/2). Furthermore, the stress effects were obviated by the intrahippocampal injection of specific inhibitors of MEK1/2 (U0126), protein kinase C (bisindolylmaleimide I), tyrosine kinase (K252a), and BDNF antisense oligonucleotides. These results suggest that the effects of stress on LTP and LTD originate from the corticosterone-induced sustained activation of ERK1/2-coupled signaling cascades.

Key words: stress; long-term potentiation; long-term depression; extracellular signal-related kinase; mitogen-activated protein kinase; glucocorticoid receptor; hippocampus

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Received May 12, 2004; revised October 29, 2004; accepted October 29, 2004.

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