High-frequency stimulation-induced synaptic potentiation in dorsal and ventral CA1 hippocampal synapses: the involvement of NMDA receptors, mGluR5, and (L-type) voltage-gated calcium channels

Wang, Yue, Michael J. Rowan, and Roger Anwyl. LTP induction dependent on activation of Ni2+-sensitive voltage-gated calcium channels, but not NMDA receptors, in the rat dentate gyrus in vitro. J. Neurophysiol. 78: 2574–2581, 1997. A N-methyl-d-aspartate receptor (NMDAR)-independent long-term potentiation (LTP) has been investigated in the dentate gyrus of the hippocampus in vitro in the presence of the NMDAR antagonist, d-2-amino-phosphonopentanoate (50–100 μM), at a concentration thatcompletely blocked NMDAR-mediated excitatory postsynaptic currents (EPSCs). LTP of patch-clamped EPSCs was induced by pairing low-frequency evoked EPSCs (1 Hz) with depolarizing voltage pulses designed to predominately open low-voltage–activated (LVA) Ca2+ channels. Voltage pulses alone induced only a short-term potentiation. The LTP was blocked by intracellular application of the rapid Ca2+ chelator bis-( o-aminophenoxy)- N,N,N′,N′-tetraacetic acid, demonstrating that a rise in intracellular Ca2+ is required for the NMDAR-independent LTP induction. The NMDAR-independent LTP induction also was blocked by Ni2+ at a low extracellular concentration (50 μM), which is known to strongly block LVA Ca2+ channels. However, Ni2+ did not inhibit the NMDAR-dependent LTP induced by high-frequency stimulation (HFS). The NMDAR-independent LTP induction was not blocked by high concentrations of the L-type Ca2+ channel blocker nifedipine (10 μM). The NMDAR-independent LTP was inhibited by the metabotropic glutamate receptor ligand (+)-α-methyl-4-carboxyphenylglycine. These experiments demonstrate the presence of a NMDAR-independent LTP induced by Ca2+ influx via Ni2+-sensitive, nifedipine-insensitive voltage-gated Ca2+ channels, probably LVA Ca2+ channels. Induction of the NMDAR-independent LTP was inhibited by prior induction of HFS-induced NMDAR-dependent LTP, demonstrating that although the NMDAR-dependent and NMDAR-independent LTP use a different Ca2+ channel for Ca2+ influx, they share a common intracellular pathway.

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Considerable differences between auditory medulla, auditory midbrain, and hippocampal synapses during sustained high-frequency stimulation: Exceptional vesicle replenishment restricted to sound localization circuit

Hearing Research ◽

10.1016/j.heares.2019.07.008 ◽

2019 ◽

Vol 381 ◽

pp. 107771 ◽

Cited By ~ 2

Author(s):

Sina E. Brill ◽

Katrin Janz ◽

Abhyudai Singh ◽

Eckhard Friauf

Keyword(s):

Sound Localization ◽

High Frequency ◽

High Frequency Stimulation ◽

Auditory Midbrain ◽

Hippocampal Synapses ◽

Frequency Stimulation

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L-Type Calcium Channels Are Required for One Form of Hippocampal Mossy Fiber LTP

Journal of Neurophysiology ◽

10.1152/jn.1998.79.4.2181 ◽

1998 ◽

Vol 79 (4) ◽

pp. 2181-2190 ◽

Cited By ~ 102

Author(s):

Ajay Kapur ◽

Mark F. Yeckel ◽

Richard Gray ◽

Daniel Johnston

Keyword(s):

Calcium Channels ◽

High Frequency ◽

Pyramidal Neurons ◽

Mossy Fiber ◽

Calcium Influx ◽

Calcium Transients ◽

High Frequency Stimulation ◽

Frequency Stimulation ◽

Ca3 Pyramidal Neurons ◽

Postsynaptic Calcium

Kapur, Ajay, Mark F. Yeckel, Richard Gray, and Daniel Johnston. L-type calcium channels are required for one form of hippocampal mossy fiber LTP. J. Neurophysiol. 79: 2181–2190, 1998. The requirement of postsynaptic calcium influx via L-type channels for the induction of long-term potentiation (LTP) of mossy fiber input to CA3 pyramidal neurons was tested for two different patterns of stimulation. Two types of LTP-inducing stimuli were used based on the suggestion that one of them, brief high-frequency stimulation (B-HFS), induces LTP postsynaptically, whereas the other pattern, long high-frequency stimulation (L-HFS), induces mossy fiber LTP presynaptically. To test whether or not calcium influx into CA3 pyramidal neurons is necessary for LTP induced by either pattern of stimulation, nimodipine, a L-type calcium channel antagonist, was added during stimulation. In these experiments nimodipine blocked the induction of mossy fiber LTP when B-HFS was given [34 ± 5% (mean ± SE) increase in control versus 7 ± 4% in nimodipine, P < 0.003]; in contrast, nimodipine did not block the induction of LTP with L-HFS (107 ± 10% in control vs. 80 ± 9% in nimodipine, P > 0.05). Administration of nimodipine after the induction of LTP had no effect on the expression of LTP. In addition, B- and L-HFS delivered directly to commissural/associational fibers in stratum radiatum failed to induce a N-methyl-d-aspartate-independent form of LTP, obviating the possibility that the presumed mossy fiber LTP resulted from potentiation of other synapses. Nimodipine had no effect on calcium transients recorded from mossy fiber presynaptic terminals evoked with the B-HFS paradigm but reduced postsynaptic calcium transients. Our results support the hypothesis that induction of mossy fiber LTP by B-HFS is mediated postsynaptically and requires entry of calcium through L-type channels into CA3 neurons.

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Contracture of myocardial fibers of the frog ventricle during high-frequency stimulation after blocking of the calcium channels by manganese ions

Bulletin of Experimental Biology and Medicine ◽

10.1007/bf00801975 ◽

1978 ◽

Vol 85 (4) ◽

pp. 439-441

Author(s):

S. I. Zakharov ◽

A. I. Undrovinas ◽

L. V. Rozenshtraukh

Keyword(s):

Calcium Channels ◽

High Frequency ◽

High Frequency Stimulation ◽

Manganese Ions ◽

Frequency Stimulation ◽

Myocardial Fibers ◽

Frog Ventricle

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Voltage-Controlled Plasticity at GluR2-Deficient Synapses Onto Hippocampal Interneurons

Journal of Neurophysiology ◽

10.1152/jn.00425.2004 ◽

2004 ◽

Vol 92 (6) ◽

pp. 3575-3581 ◽

Cited By ~ 32

Author(s):

Fernanda Laezza ◽

Raymond Dingledine

Keyword(s):

Membrane Potential ◽

Nmda Receptors ◽

Ampa Receptors ◽

High Frequency ◽

Long Term Potentiation ◽

Receptor Expression ◽

Stratum Radiatum ◽

High Frequency Stimulation ◽

Frequency Stimulation

High-frequency stimulation of pyramidal cell inputs to developing (P9-12) hippocampal stratum radiatum interneurons expressing GluR2-lacking, Ca2+-permeable AMPA receptors produces long-term depression of synaptic transmission, if N-methyl-d-aspartate (NMDA) receptors are blocked. Here we show that these same synapses display a remarkably versatile signal integration if postsynaptic NMDA receptors are activated. At synapses expressing GluR2-deficient AMPA receptors, tetanic stimulation that activates NMDA receptors triggered long-term potentiation or depression (LTP or LTD) depending on membrane potential. LTP was elicited at most synapses when the interneuron was held at –30 mV during the stimulus train but was typically prevented by postsynaptic hyperpolarization to –70 mV, by strong depolarization to 0 mV, by d-2-amino-5-phosphonovaleric acid, or by postsynaptic injection of the Ca2+ chelator bis-( o-aminophenoxy)- N,N,N′,N′-tetraacetic acid. At synapses with predominantly GluR2-containing AMPA receptors, repetitive stimulation did not change synaptic strength regardless of whether NMDA receptors were activated. The interactions among GluR2 expression, NMDA receptor expression, and membrane potential thus confer on hippocampal interneurons a distinctive means for differential decoding of high-frequency inputs, resulting in enhanced or depressed transmission depending on the functional state of the interneuron.

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