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The Journal of Neuroscience, June 1, 2002, 22(11):4312-4320

Postsynaptic Expression of a New Calcium Pathway in Hippocampal CA3 Neurons and Its Influence on Mossy Fiber Long-Term Potentiation

Wataru Kakegawa¹, Nobuaki Yamada^{1, 2}, Masae Iino¹, Kimihiko Kameyama³, Tatsuya Umeda⁴, Keisuke Tsuzuki¹, and Seiji Ozawa^{1, 2}

¹ Department of Physiology, Gunma University School of Medicine, Maebashi, Gunma 371-8511, Japan, ² Core Research for Evolutional Science and Technology, Japan Science and Technology Corporation, Kawaguchi, Saitama 332-0012, Japan, ³ Molecular Neurophysiology Group, Neuroscience Research Institute, National Institute of Advanced Industrial Science and Technology, Tsukuba, Ibaraki 305-8566, Japan, and ⁴ Department of Anatomy and Cell Biology, School of Medicine, Tokyo Medical and Dental University, Bunkyo-ku, Tokyo 113-8519, Japan

Long-term potentiation (LTP) in the CA1 region of the hippocampus is induced by postsynaptic Ca²⁺ influx via NMDA receptors (NMDARs). However, this synaptic plasticity occurs independently of NMDARs when Ca²⁺-permeable AMPA receptors (AMPARs) are expressed at postsynaptic sites using various genetic techniques, indicating that an increase in Ca²⁺ level at critical postsynaptic sites, regardless of its entry pathway, triggers the induction of LTP at CA1 synapses. In contrast, NMDARs are sparsely distributed on mossy fiber (MF) synapses in CA3 hippocampal neurons, and most evidence favors the presynaptic mechanism for LTP induction, although some reports suggested a postsynaptic mechanism. In this study, we examined whether Ca²⁺ influx through the newly produced postsynaptic receptors during high-frequency stimulation affects the induction of MF LTP. For this purpose, we expressed Ca²⁺-permeable AMPARs in CA3 pyramidal neurons by Sindbis viral-mediated gene transfer of the unedited form of the glutamate receptor 2 (GluR2Q) subunit, as a new pathway for postsynaptic Ca²⁺ entry, in rat hippocampal organotypic cultures. Virally expressed myc-tagged GluR2Q was detected at the complex spines known as the thorny excrescences, which serve as postsynaptic targets for MF synaptic input, on the proximal apical dendrites of CA3 pyramidal cells. Furthermore, endogenous Ca²⁺-impermeable AMPARs at MF synapses were converted into Ca²⁺-permeable receptors by GluR2Q expression. However, the postsynaptic expression of Ca²⁺-permeable AMPARs had no significant influence on the two types of MF LTP induced by different stimulus protocols. These results supported the notion that MF LTP is independent of postsynaptic Ca²⁺.

Key words: mossy fiber LTP; Ca²⁺-permeable AMPA receptors; GluR2; Ca²⁺ influx; Sindbis viral vector; high-frequency stimulation; CA3; hippocampus

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Copyright © 2002 Society for Neuroscience  0270-6474/02/22114312-09$05.00/0

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