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The Journal of Neuroscience, March 19, 2008, 28(12):3060-3070; doi:10.1523/JNEUROSCI.5450-07.2008

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Development/Plasticity/Repair
Synaptic Metaplasticity through NMDA Receptor Lateral Diffusion

Jiang Zhao,^1,2 * Yi Peng,^1,2 * Zhuo Xu,^1,2,3 Rong-qing Chen,^1,2,3 Qin-hua Gu,^1,2,3 Zheng Chen,¹ and Wei Lu^1,2,3

¹Department of Neurobiology, ²Key Laboratory of Neurodegenerative Disease of Jiangsu Province, and ³Key Laboratory of Human Functional Genomics of Jiangsu Province, Nanjing Medical University, Nanjing, Jiangsu Province 210029, China

Correspondence should be addressed to Dr. Wei Lu, Department of Neurobiology, Nanjing Medical University, Nanjing, Jiangsu Province 210029, China. Email: lu{at}njmu.edu.cn

Lateral diffusion of glutamate receptors was proposed as a mechanism for regulating receptor numbers at synapses and affecting synaptic functions, especially the efficiency of synaptic transmission. However, a direct link between receptor lateral diffusion and change in synaptic function has not yet been established. In the present study, we demonstrated NMDA receptor (NMDAR) lateral diffusion in CA1 neurons in hippocampal slices by detecting considerable recovery of spontaneous or evoked EPSCs from the block of (+)-MK-801 [(+)-5-methyl-10,11-dihydro-5H-dibenzo [a,d] cyclohepten-5,10-imine maleate], an irreversible NMDAR open-channel blocker. We observed changes on both the number and the composition of synaptic NMDAR on recovery. More importantly, after the recovery, long-term potentiation (LTP)-producing protocol induced only LTD (long-term depression) instead of LTP. In contrast, a complete recovery from competitive NMDAR blocker D,L-AP-5 was observed without subsequent changes on synaptic plasticity. Our data suggest a revised model of NMDAR trafficking wherein extrasynaptic NMDARs, mostly NR1/NR2B receptors, move laterally into synaptic sites, resulting in altered rule of synaptic modification. Thus, CA1 synapses exhibit a novel form of metaplasticity in which the direction of synaptic modification can be reverted through subtype-specific lateral diffusion of NMDA receptors.

Key words: NMDA receptor; lateral diffusion; LTP; LTD; MK-801; AP-5

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Received Dec. 10, 2007; revised Jan. 21, 2008; accepted Jan. 31, 2008.

Correspondence should be addressed to Dr. Wei Lu, Department of Neurobiology, Nanjing Medical University, Nanjing, Jiangsu Province 210029, China. Email: lu{at}njmu.edu.cn

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