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The Journal of Neuroscience, March 10, 2004, 24(10):2412-2420; doi:10.1523/JNEUROSCI.5544-03.2004

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Development/Plasticity/Repair
Stress Enables Synaptic Depression in CA1 Synapses by Acute and Chronic Morphine: Possible Mechanisms for Corticosterone on Opiate Addiction

Ya Yang,^1,2 * Xigeng Zheng,^3 * Yongfu Wang,⁴ Jun Cao,^1,2 Zhifang Dong,^1,2 Jingxia Cai,⁴ Nan Sui,³ and Lin Xu^1,2

¹Laboratory of Learning and Memory, Kunming Institute of Zoology, The Chinese Academy of Sciences, Kunming 650223, People's Republic of China, ²Graduate School of the Chinese Academy of Sciences, Beijing 100039, People's Republic of China, ³The Key Laboratory of Mental Health, Institute of Psychology, The Chinese Academy of Sciences, Beijing 100101, People's Republic of China, and ⁴Laboratory of Behavior and Brain, Kunming Institute of Zoology, The Chinese Academy of Sciences, Kunming 650223, People's Republic of China

The hippocampus, being sensitive to stress and glucocorticoids, plays significant roles in certain types of learning and memory. Therefore, the hippocampus is probably involved in the increasing drug use, drug seeking, and relapse caused by stress. We have studied the effect of stress with morphine on synaptic plasticity in the CA1 region of the hippocampus in vivo and on a delayed-escape paradigm of the Morris water maze. Our results reveal that acute stress enables long-term depression (LTD) induction by low-frequency stimulation (LFS) but acute morphine causes synaptic potentiation. Remarkably, exposure to an acute stressor reverses the effect of morphine from synaptic potentiation (20%) to synaptic depression (40%), precluding further LTD induction by LFS. The synaptic depression caused by stress with morphine is blocked either by the glucocorticoid receptor antagonist RU38486 or by the NMDA-receptor antagonist D-APV. Chronic morphine attenuates the ability of acute morphine to cause synaptic potentiation, and stress to enable LTD induction, but not the ability of stress in tandem with morphine to cause synaptic depression. Furthermore, corticosterone with morphine during the initial phase of drug use promotes later delayed-escape behavior, as indicated by the morphine-reinforced longer latencies to escape, leading to persistent morphine-seeking after withdrawal. These results suggest that hippocampal synaptic plasticity may play a significant role in the effects of stress or glucocorticoids on opiate addiction.

Key words: hippocampus; long-term depression; associative learning; stress; morphine-seeking; opiate addiction

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Received Oct 3, 2003; revised January 20, 2004; accepted January 20, 2004.

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