Long-term potentiation and long-term depression in hippocampal CA1 neurons of mice lacking the IP3 type 1 receptor

T. Nagase, K. I. Ito, K. Kato, K. Kaneko, K. Kohda, M. Matsumoto, A. Hoshino, T. Inoue, S. Fujii, H. Kato, K. Mikoshiba

Research output: Contribution to journalArticle

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Abstract

To investigate the role in synaptic plasticity of Ca2+ released from intracellular Ca2+ stores, mice lacking the inositol 1,4,5-trisphosphate type 1 receptor were developed and the physiological properties, long-term potentiation, and long-term depression of their hippocampal CA1 neurons were examined. There were no significant differences in basic synaptic functions, such as membrane properties and the input/output relationship, between homozygote mutant and wild-type mice. Enhanced paired-pulse facilitation at interpulse intervals of less than 60 ms and enhanced post-tetanic potentiation were observed in the mutant mice, suggesting that the presynaptic mechanism was altered by the absence of the inositol 1,4,5-trisphosphate type 1 receptor. Long-term potentiation in the field-excitatory postsynaptic potentials induced by tetanus (100 Hz, 1 s) and the excitatory postsynaptic currents induced by paired stimulation in hippocampal CA1 pyramidal neurons under whole-cell clamp conditions were significantly greater in mutant mice than in wild-type mice. Homosynaptic long-term depression of CA1 synaptic responses induced by low-frequency stimulation (1 Hz, 500 pulses) was not significantly different, but heterosynaptic depression of the non-associated pathway induced by tetanus was blocked in the mutant mice. Both long-term potentiation and long-term depression in mutant mice were completely dependent on N-methyl-D-aspartate receptor activity. To rule out the possibility of an effect compensating for the lack of the inositol 1,4,5-trisphosphate type 1 receptor occurring during development, an anti-inositol 1,4,5-trisphosphate type 1 receptor monoclonal antibody that blocks receptor function was diffused into the wild-type cell through a patch pipette, and the effect of acute block of inositol 1,4,5-trisphosphate type 1 receptor on long-term potentiation was examined. Significant enhancement of long-term potentiation was observed compared with after control immunoglobulin G injection, suggesting that developmental redundancy was not responsible for the increase in long-term potentiation amplitude observed in the mutant mouse. The properties of channels that could be involved in long-term potentiation induction were examined using whole-cell recording. N-methyl-D-aspartate currents were significantly larger in mutant mice than in wild-type mice only between holding potentials of -60 and -80 mV. We conclude that inositol 1,4,5-trisphosphate type 1 receptor activity is not essential for the induction of synaptic plasticity in hippocampal CA1 neurons, but appears to negatively regulate long-term potentiation induction by mild modulation of channel activities.

Original languageEnglish
Pages (from-to)821-830
Number of pages10
JournalNeuroscience
Volume117
Issue number4
DOIs
Publication statusPublished - 2003 Apr 10
Externally publishedYes

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Inositol 1,4,5-Trisphosphate Receptors
Long-Term Potentiation
Neurons
Neuronal Plasticity
Excitatory Postsynaptic Potentials
Tetanus
Long-Term Synaptic Depression
Pyramidal Cells
Homozygote
Patch-Clamp Techniques
N-Methylaspartate
N-Methyl-D-Aspartate Receptors
Immunoglobulin G
Monoclonal Antibodies

Keywords

  • Epilepsy
  • Hippocampus
  • Knockout mouse
  • NMDA receptor
  • Paired-pulse facilitation
  • Synaptic plasticity

ASJC Scopus subject areas

  • Neuroscience(all)

Cite this

Nagase, T., Ito, K. I., Kato, K., Kaneko, K., Kohda, K., Matsumoto, M., ... Mikoshiba, K. (2003). Long-term potentiation and long-term depression in hippocampal CA1 neurons of mice lacking the IP3 type 1 receptor. Neuroscience, 117(4), 821-830. https://doi.org/10.1016/S0306-4522(02)00803-5

Long-term potentiation and long-term depression in hippocampal CA1 neurons of mice lacking the IP3 type 1 receptor. / Nagase, T.; Ito, K. I.; Kato, K.; Kaneko, K.; Kohda, K.; Matsumoto, M.; Hoshino, A.; Inoue, T.; Fujii, S.; Kato, H.; Mikoshiba, K.

In: Neuroscience, Vol. 117, No. 4, 10.04.2003, p. 821-830.

Research output: Contribution to journalArticle

Nagase, T, Ito, KI, Kato, K, Kaneko, K, Kohda, K, Matsumoto, M, Hoshino, A, Inoue, T, Fujii, S, Kato, H & Mikoshiba, K 2003, 'Long-term potentiation and long-term depression in hippocampal CA1 neurons of mice lacking the IP3 type 1 receptor', Neuroscience, vol. 117, no. 4, pp. 821-830. https://doi.org/10.1016/S0306-4522(02)00803-5
Nagase, T. ; Ito, K. I. ; Kato, K. ; Kaneko, K. ; Kohda, K. ; Matsumoto, M. ; Hoshino, A. ; Inoue, T. ; Fujii, S. ; Kato, H. ; Mikoshiba, K. / Long-term potentiation and long-term depression in hippocampal CA1 neurons of mice lacking the IP3 type 1 receptor. In: Neuroscience. 2003 ; Vol. 117, No. 4. pp. 821-830.
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AU - Ito, K. I.

AU - Kato, K.

AU - Kaneko, K.

AU - Kohda, K.

AU - Matsumoto, M.

AU - Hoshino, A.

AU - Inoue, T.

AU - Fujii, S.

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KW - Epilepsy

KW - Hippocampus

KW - Knockout mouse

KW - NMDA receptor

KW - Paired-pulse facilitation

KW - Synaptic plasticity

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