Modulation of Long-term Potentiation in Rat Hippocampal Pyramidal Neurons by Zinc

Overview

Journal Pflugers Arch

Specialty Physiology

Date 1994 Jul 1

PMID 7971146

Citations 24

Authors

X Xie

T G Smart

Affiliations

Soon will be listed here.

Abstract

The phenomenon of long-term potentiation is frequently promulgated as an example of learning and memory mechanisms at the synaptic level in the mammalian central nervous system. In the CA3 region of the hippocampus there is an abundance of zinc, which is located in presynaptic mossy fibre nerve terminals. Stimulation of these fibres can cause the release of zinc, which interacts with excitatory amino acid receptors and may therefore modulate long-term potentiation. We now demonstrate in CA1 and CA3 neurons that zinc (100-300 microM) enhances non-N-methyl-D-aspartate-receptor-mediated responses whilst reducing excitatory synaptic transmission and inhibiting long-term potentiation. However, by using zinc-chelating agents, endogenously released zinc following high-frequency stimulation in the stratum lucidum does not appear to have any modulatory role in excitatory synaptic transmission and long-term potentiation. These results indicate that an increase in the level of extracellular zinc can limit excitatory synaptic transmission in the CA1 or CA3 region and further suggests that pathologies that can be related to excessive levels of endogenous zinc may have implications for synaptic plasticity in CA3 neurons.

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References

Hider R, Ejim L, Taylor P, Gale R, Huehns E, Porter J . Facilitated uptake of zinc into human erythrocytes. Relevance to the treatment of sickle-cell anaemia. Biochem Pharmacol. 1990; 39(6):1005-12. DOI: 10.1016/0006-2952(90)90278-s. View

Davies S, Lester R, Reymann K, Collingridge G . Temporally distinct pre- and post-synaptic mechanisms maintain long-term potentiation. Nature. 1989; 338(6215):500-3. DOI: 10.1038/338500a0. View

Madison D, Malenka R, Nicoll R . Mechanisms underlying long-term potentiation of synaptic transmission. Annu Rev Neurosci. 1991; 14:379-97. DOI: 10.1146/annurev.ne.14.030191.002115. View

Masu M, Tanabe Y, Tsuchida K, Shigemoto R, Nakanishi S . Sequence and expression of a metabotropic glutamate receptor. Nature. 1991; 349(6312):760-5. DOI: 10.1038/349760a0. View

Zalutsky R, Nicoll R . Comparison of two forms of long-term potentiation in single hippocampal neurons. Science. 1990; 248(4963):1619-24. DOI: 10.1126/science.2114039. View

Connor M, Chavkin C . Ionic zinc may function as an endogenous ligand for the haloperidol-sensitive sigma 2 receptor in rat brain. Mol Pharmacol. 1992; 42(3):471-9. View

Smart T, Xie X, Krishek B . Modulation of inhibitory and excitatory amino acid receptor ion channels by zinc. Prog Neurobiol. 1994; 42(3):393-441. DOI: 10.1016/0301-0082(94)90082-5. View

Westbrook G, Mayer M . Micromolar concentrations of Zn2+ antagonize NMDA and GABA responses of hippocampal neurons. Nature. 1987; 328(6131):640-3. DOI: 10.1038/328640a0. View

Howell G, Welch M, Frederickson C . Stimulation-induced uptake and release of zinc in hippocampal slices. Nature. 1984; 308(5961):736-8. DOI: 10.1038/308736a0. View

10.

Houamed K, Kuijper J, Gilbert T, Haldeman B, OHara P, Mulvihill E . Cloning, expression, and gene structure of a G protein-coupled glutamate receptor from rat brain. Science. 1991; 252(5010):1318-21. DOI: 10.1126/science.1656524. View

11.

Danscher G, Shipley M, Andersen P . Persistent function of mossy fibre synapses after metal chelation with DEDTC (Antabuse). Brain Res. 1975; 85(3):522-6. DOI: 10.1016/0006-8993(75)90825-2. View

12.

Weisskopf M, Zalutsky R, Nicoll R . The opioid peptide dynorphin mediates heterosynaptic depression of hippocampal mossy fibre synapses and modulates long-term potentiation. Nature. 1993; 362(6419):423-7. DOI: 10.1038/362423a0. View

13.

Mayer M, Vyklicky Jr L, Westbrook G . Modulation of excitatory amino acid receptors by group IIB metal cations in cultured mouse hippocampal neurones. J Physiol. 1989; 415:329-50. PMC: 1189179. DOI: 10.1113/jphysiol.1989.sp017724. View

14.

Smart T, Constanti A . Pre- and postsynaptic effects of zinc on in vitro prepyriform neurones. Neurosci Lett. 1983; 40(2):205-11. DOI: 10.1016/0304-3940(83)90303-8. View

15.

Kihara T, Baba A, Koyama Y, Ishihara T, Iwata H . Inhibition of [3H]glutamate release by Zn2+ in rat hippocampal slices. J Pharmacobiodyn. 1990; 13(5):321-6. DOI: 10.1248/bpb1978.13.321. View

16.

TOCCO G, Maren S, Shors T, Baudry M, Thompson R . Long-term potentiation is associated with increased [3H]AMPA binding in rat hippocampus. Brain Res. 1992; 573(2):228-34. DOI: 10.1016/0006-8993(92)90767-4. View

17.

Haas H, Greene R . Long-term potentiation and 4-aminopyridine. Cell Mol Neurobiol. 1985; 5(3):297-301. PMC: 11572903. DOI: 10.1007/BF00711014. View

18.

Sim J, Cherubini E . Submicromolar concentrations of zinc irreversibly reduce a calcium-dependent potassium current in rat hippocampal neurons in vitro. Neuroscience. 1990; 36(3):623-9. DOI: 10.1016/0306-4522(90)90005-o. View

19.

Stengaard-Pedersen K, Fredens K, Larsson L . Inhibition of opiate receptor binding by zinc ions: possible physiological importance in the hippocampus. Peptides. 1981; 2 Suppl 1:27-35. DOI: 10.1016/0196-9781(81)90052-8. View

20.

Bliss T, Collingridge G . A synaptic model of memory: long-term potentiation in the hippocampus. Nature. 1993; 361(6407):31-9. DOI: 10.1038/361031a0. View