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The Journal of Neuroscience, August 17, 2005, 25(33):7697-7707; doi:10.1523/JNEUROSCI.2086-05.2005

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Development/Plasticity/Repair
Hippocampal Synaptic Metaplasticity Requires Inhibitory Autophosphorylation of Ca²⁺/Calmodulin-Dependent Kinase II

Lian Zhang,^1,2 Timo Kirschstein,¹ Britta Sommersberg,¹ Malte Merkens,¹ Denise Manahan-Vaughan,^3,4 Ype Elgersma,⁵ and Heinz Beck¹

¹Department of Epileptology, University of Bonn, D-53105 Bonn, Germany, ²Department of Pediatrics, Tongji Hospital, Huazhong University of Science and Technology, Wuhan 430030, China, ³Learning and Memory Research, International Graduate School of Neuroscience, Ruhr University Bochum, 44780 Bochum, Germany, ⁴Institute for Physiology, Humboldt University Medical Faculty (Charité), 10117 Berlin, Germany, and ⁵Department of Neuroscience, Erasmus Medical Center, University Rotterdam, 3000 DR Rotterdam, The Netherlands

Virtually all CNS synapses display the potential for activity-dependent long-term potentiation (LTP) and/or long-term depression (LTD). Intriguingly, the potential to exhibit LTP or LTD at many central synapses itself is powerfully modulated by previous synaptic activity. This higher-order form of plasticity has been termed metaplasticity. Here, we show that inhibitory autophosphorylation of Ca²⁺/calmodulin-dependent kinase II (CaMKII) is required for hippocampal metaplasticity at the lateral perforant path-dentate granule cell synapse. Brief 10 Hz priming, which does not affect basal synaptic transmission, caused a dramatic, pathway-specific and long-lasting (up to 18 h) reduction in subsequently evoked LTP at lateral perforant path synapses. In contrast, LTD was unaffected by priming. The induction of lateral perforant path metaplasticity required the activation of NMDA receptors during priming. In addition, metaplasticity was absent in knock-in mice expressing CaMKII that cannot undergo inhibitory phosphorylation, indicating that inhibitory autophosphorylation of CaMKII at threonines 305/306 is required for metaplasticity. Metaplasticity was not observed in the medial perforant pathway, consistent with the observation that CaMKII activity was not required for the induction of LTP at this synapse. Thus, modulation of CaMKII activity via autophosphorylation at Thr305/Thr306 is a key mechanism for metaplasticity that may be of importance in the integration of temporally separated episodes of activity.

Key words: metaplasticity; LTP; LTD; Ca²⁺/calmodulin-dependent kinase II; hippocampus; autophosphorylation

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Received Feb 14, 2005; revised July 4, 2005; accepted July 4, 2005.

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