DOI: 10.1101/lm.34100. Synaptic Plasticity in Hippocampal CA1 Neurons of Mice Lacking Type 1 Inositol-1,4,5-Trisphosphate Receptors

Synaptic Plasticity in Hippocampal CA1 Neurons of Mice Lacking Type 1 Inositol-1,4,5-Trisphosphate Receptors

10.1101/lm.34100

Crossref journal-article

Cold Spring Harbor Laboratory

Learning & Memory (246)

Abstract

In hippocampal CA1 neurons of wild-type mice, delivery of a standard tetanus (100 pulses at 100 Hz) or a train of low-frequency stimuli (LFS; 1000 pulses at 1 Hz) to a naive input pathway induces, respectively, long-term potentiation (LTP) or long-term depression (LTD) of responses, and delivery of LFS 60 min after tetanus results in reversal of LTP (depotentiation, DP), while LFS applied 60 min before tetanus suppresses LTP induction (LTP suppression). To evaluate the role of the type 1 inositol-1,4,5-trisphosphate receptor (IP3R1) in hippocampal synaptic plasticity, we studied LTP, LTD, DP, and LTP suppression of the field excitatory postsynaptic potentials (EPSPs) in the CA1 neurons of mice lacking the IP3R1. No differences were seen between mutant and wild-type mice in terms of the mean magnitude of the LTP or LTD induced by a standard tetanus or LFS. However, the mean magnitude of the LTP induced by a short tetanus (10 pulses at 100 Hz) was significantly greater in mutant mice than in wild-type mice. In addition, DP or LTP suppression was attenuated in the mutant mice, the mean magnitude of the responses after delivery of LFS or tetanus being significantly greater than in wild-type mice. These results suggest that, in hippocampal CA1 neurons, the IP3R1 is involved in LTP, DP, and LTP suppression but is not essential for LTD. The facilitation of LTP induction and attenuation of DP and LTP suppression seen in mice lacking the IP3R1 indicates that this receptor plays an important role in blocking synaptic potentiation in hippocampal CA1 neurons.

Bibliography

Fujii, S., Matsumoto, M., Igarashi, K., Kato, H., & Mikoshiba, K. (2000). Synaptic Plasticity in Hippocampal CA1 Neurons of Mice Lacking Type 1 Inositol-1,4,5-Trisphosphate Receptors. Learning & Memory, 7(5), 312â320.

Authors 5

Satoshi Fujii (first)
Mineo Matsumoto (additional)
Kotaro Igarashi (additional)
Hiroshi Kato (additional)
Katsuhiko Mikoshiba (additional)

References 41 Referenced 101

10.1016/0092-8674(93)90613-U
10.1113/jphysiol.1988.sp017078 / J. Physiol. / The role of divalent cations in the N-methyl-D-aspartate responses of mouse central neurons in culture. by Ascher (1988)
10.1126/science.276.5321.2042
10.1007/BF02738403
10.1038/363347a0
10.1146/annurev.ne.19.030196.002253
10.1016/0166-2236(92)90049-E / Trends Neurosci. / Protein kinase C modulation of NMDA currents: An important link for LTP induction. by Ben-Ari (1992)
10.1038/361315a0
10.1038/361031a0
10.1113/jphysiol.1973.sp010274
10.1113/jphysiol.1973.sp010273
10.1016/0028-3908(93)90123-K
10.1038/368740a0
10.1016/0304-3940(94)90228-3
10.1113/jphysiol.1988.sp017080 / J. Physiol. / Synaptic activation of N-methyl-D-aspartate responses in the Schaffer collateral-commissural pathway of rat hippocampus. by Collingridge (1988)
10.1113/jphysiol.1988.sp017080 / J. Physiol. / Frequency-dependent N-methyl-D-aspartate receptor mediated synaptic transmission in rat hippocampus. (1988)
10.1073/pnas.89.10.4363
10.1016/0006-8993(91)90867-U
{'key': '2021111106031369000_7.5.312.19', 'first-page': '305', 'article-title': 'The long-term suppressive effect of prior activation of synaptic inputs by low-frequency stimulation on induction of long-term potentiation in CA1 neurons of guinea-pig hippocampal slices.', 'volume': '111', 'author': 'Fujii', 'year': '1996', 'journal-title': 'Exp. Brain Res.'} / Exp. Brain Res. / The long-term suppressive effect of prior activation of synaptic inputs by low-frequency stimulation on induction of long-term potentiation in CA1 neurons of guinea-pig hippocampal slices. by Fujii (1996)
10.1016/S0304-3940(99)00980-5
{'key': '2021111106031369000_7.5.312.21', 'first-page': '11', 'article-title': 'Widespread expression of inositol 1,4,5-trisphosphate receptor type 1 gene in the mouse central nervous system.', 'volume': '1', 'author': 'Furuichi', 'year': '1993', 'journal-title': 'Recept. Channels'} / Recept. Channels / Widespread expression of inositol 1,4,5-trisphosphate receptor type 1 gene in the mouse central nervous system. by Furuichi (1993)
10.1523/JNEUROSCI.14-08-04794.1994 / J. Neurosci. / Multiple types of ryanodine receptor/Ca2+ release channels are differentially expressed in rabbit brain. by Furuichi (1994)
10.1016/S0896-6273(00)81123-X
10.1038/381163a0
10.1523/JNEUROSCI.18-14-05366.1998 / J. Neurosci. / Type 1 Inositol 1,4,5-trisphosphate receptor is required for induction of long-term depression in cerebellar Purkinje neurons. by Inoue (1998)
10.1016/0304-3940(94)11127-5
10.1016/0006-8993(91)91519-7
10.1016/S0896-6273(00)80632-7
10.1038/35016089
10.1016/0896-6273(94)90205-4 / Neuron / Long-term synaptic depression in the mammalian brain. by Linden (1994)
10.1016/0166-2236(94)90014-0
10.1038/379168a0
10.1016/0165-6147(93)90069-V
10.1016/0896-6273(92)90248-C
10.1038/369486a0 / Nature / Involvement of a calcineurin/inhibitor-1 phosphatase cascade in hippocampal long-term depression. by Mulkey (1994)
10.1126/science.1329206
10.1101/lm.1.2.129
10.1016/S0896-6273(00)80336-0
10.1111/j.1469-7793.1998.761bg.x
10.1016/S0028-3908(97)00181-0
10.1016/0028-3908(93)90150-2

Dates

Type	When
Created	23 years, 1 month ago (July 26, 2002, 8 p.m.)
Deposited	3 years, 9 months ago (Nov. 11, 2021, 9:04 a.m.)
Indexed	2 weeks, 1 day ago (Aug. 20, 2025, 8:57 a.m.)
Issued	25 years ago (Sept. 1, 2000)
Published	25 years ago (Sept. 1, 2000)
Published Online	25 years ago (Sept. 1, 2000)
Published Print	25 years ago (Sept. 1, 2000)

Funders 0

None

BibTeX

@article{Fujii_2000, title={Synaptic Plasticity in Hippocampal CA1 Neurons of Mice Lacking Type 1 Inositol-1,4,5-Trisphosphate Receptors}, volume={7}, ISSN={1549-5485}, url={http://dx.doi.org/10.1101/lm.34100}, DOI={10.1101/lm.34100}, number={5}, journal={Learning & Memory}, publisher={Cold Spring Harbor Laboratory}, author={Fujii, Satoshi and Matsumoto, Mineo and Igarashi, Kotaro and Kato, Hiroshi and Mikoshiba, Katsuhiko}, year={2000}, month=sep, pages={312–320} }

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