Permeation of calcium through excitatory amino acid receptor channels in cultured rat hippocampal neurones.

Iino, Masae; Ozawa, Seiji; Tsuzuki, Keisuke

doi:10.1113/jphysiol.1990.sp018060

Cited by 460 publications

(255 citation statements)

References 26 publications

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“…AMPA receptors on at least certain interneurones have distinct functional properties vis-à-vis AMPA receptors on pyramidal cells: the unitary EPSC is of abrupt onset, large amplitude, and decays quickly (Miles, 1990), and interneurone AMPA receptor channels are relatively permeable to calcium and rectify at strongly depolarized membrane potentials (Iino, Ozawa & Tsuzuki, 1990). These properties depend on receptor subunit composition (particularly the relative absence of GluR-B in interneurones and perhaps on the relative presence of GluR_D) and are regulated by posttranslational alternative splicing and RNA editing (Bochet et al 1994;Geiger et al 1995).…”

Section: Ampa Receptors On Interneuronesmentioning

confidence: 99%

Spatiotemporal patterns of γ frequency oscillations tetanically induced in the rat hippocampal slice

Whittington

Stanford

Colling

et al. 1997

The Journal of Physiology

209

204

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We used transverse and longitudinal rat hippocampal slices to study the synchronization of γ frequency (> 20 Hz) oscillations, across distances of up to 4.5 mm. γ oscillations were evoked in the CA1 region by tetanic stimulation at one or two sites simultaneously, and were associated with population spikes. Tetanic stimuli that were strong enough to induce oscillations were associated with depolarization of both pyramidal cells and interneurones, largely produced by activation of metabotropic glutamate receptors. Computer simulations of γ oscillations were also performed in a model with pyramidal cells and interneurones, arranged in a chain of five cell groups. This model had suggested previously that interneurone networks alone could generate synchronous γ oscillations locally, but that pyramidal cell firing, by inducing spike doublets in interneurones, was necessary for the occurrence of highly correlated oscillations with small phase lag (< 2.5 ms), in a distributed network possessing long axon conduction delays. In both experiment and model, pyramidal cell spikes occurred in phase with local population spikes, as did the first spike of the interneurone doublet. The conductance of the interneurone α‐amino‐3‐hydroxy‐5‐methyl‐4‐isoxazole propionic acid (AMPA) receptor‐mediated conductance was manipulated in the model, while the relation between oscillations at opposite ends of the chain was examined. When the conductance was large enough for doublet firing to be synaptically induced in interneurones, oscillation phase lags were < 2.25 ms across the chain. As predicted, experimental blockade of AMPA receptors resulted in increased phase lags between two sites oscillating simultaneously, compared with control conditions. Both in model and in experiment, when stimuli to the two ends of the network were slightly different, cross‐network synchronization occurred with a shorter phase lag at high frequencies than at lower frequencies. These data suggest that, while interneurone networks alone can generate locally synchronized γ oscillations, firing of pyramidal cells, and the synaptically induced doublet firing in interneurones, contribute to the stability and tight synchrony of the oscillations in distributed networks.

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Section: Ampa Receptors On Interneuronesmentioning

confidence: 99%

Spatiotemporal patterns of γ frequency oscillations tetanically induced in the rat hippocampal slice

Whittington

Stanford

Colling

et al. 1997

The Journal of Physiology

209

204

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“…Therefore, the difference in degree of development of receptor desensitization between both preparations may play a key role for a difference in the rank order of the depolarizing activity, but the existence of different types of kainate receptors is also strongly suggested. Multiplicity of kainate receptors based on their permeability to Ca2+ is also proposed from electrophysiological evidence on cultured rat hippocampal neurones (Iino et al, 1990). In addition, recent studies on cDNA for glutamate receptors suggest the presence of a family of kainate receptor subunits with regional difference in the rat brain and with differential potencies of some non-NMDA agonists (Boulter et al, 1990;Keinanen et al, 1990;Sommer et al, 1990;Egebjerg et al, 1991;Hollmann et al, 1991;Werner et al, 1991).…”

Section: Cross Desensitization Between Kainate Derivativesmentioning

confidence: 99%

Novel kainate derivatives: potent depolarizing actions on spinal motoneurones and dorsal root fibres in newborn rats

Ishida

Shinozaki²

1991

British J Pharmacology

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1Neuropharmacological actions of several kainate derivatives (kainoids) were examined for electrophysiological effects in the isolated spinal cord and the dorsal root fibre of the newborn rat. 2 Some kainoids caused depolarization of the motoneurone much more effectively than kainic acid or domoic acid and others were weaker. The rank order of the depolarizing activities of the kainoids tested here is as follows: 442-methoxyphenyl)-2-carboxy-3-pyrrolidineacetic acid (MFPA) > acromelic acid A > domoic acid _ 4-(2-hydroxyphenyl)-2-carboxy-3-pyrrolidineacetic acid (HFPA) _ acromelic acid B > kainic acid. 3 In the isolated dorsal root fibre, domoic acid caused the most significant depolarization. There were distinct differences with regard to the rank order of the depolarizing activity between the motoneurone and the dorsal root fibre. The rank order in the dorsal root fibre is domoic acid > acromelic acid B > 5-bromowillardiine _ MFPA > acromelic acid A > HFPA > kainic acid. 4 Significant desensitization of kainate receptors was observed in the isolated dorsal root fibre during prolonged application of L-glutamate, kainate and its derivatives. Cross desensitization was also observed among these excitatory amino acids. Receptors desensitized by kainate did not respond to MFPA, HFPA and acromelic acids, suggesting that these kainate derivatives activated common kainate receptors in the dorsal root fibre.5 In both motoneurones and dorsal root fibres, 6-cyano-7-nitroquinoxaline-2,3-dione (CNQX) effectively depressed the depolarization induced by kainoids, and neither 3-[(±)-2-carboxypiperazin-4-yl]propyl-1-phosphonic acid (CPP) nor picrotoxin blocked or affected the depolarization, but there were some differences in pharmacological potencies of glutamate antagonists between both preparations. 6 MFPA, HFPA and acromelic acids should provide valuable pharmacological tools for analysis of physiological functions of excitatory amino acids, in particular, as specific agonists for some subtypes of kainate receptors.

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“…When GluRl, GluR3, or GluRl+3 receptors are expressed in Xenopus oocytes, the channels show inward rectification and Ca2+ permeability in response to kainate stimulation Nakanishi et al, 1990;Hollmann et al, 1991). Before this finding, non-NMDA channels were believed to be impermeable to Ca2+, although a type of Ca*+-permeable kainate response was observed in vivo in rat hippocampal neurons (Iino et al, 1990;Ozawa et al, 1991). Expression of the GluR2 subunit alone produces very small currents, but coexpression with GluRl or GluR3 subunits results in responses that are larger than those produced by GluRl or GluR3 alone.…”

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confidence: 99%

Ethanol inhibits kainate responses of glutamate receptors expressed in Xenopus oocytes: role of calcium and protein kinase C

Dildy-Mayfield

Harris

1995

J. Neurosci.

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Recombinant alpha-amino-3-hydroxy-5-methyl-4-isoxazole propionic acid (AMPA)/kainate receptors expressed in oocytes are inhibited by ethanol and the sensitivity to ethanol depends on the kainate concentration and the subunit(s) expressed. For example, GluR3 kainate channels are more sensitive to inhibition by ethanol than GluR6 channels in the presence of maximally effective kainate concentrations. To determine if the ethanol inhibition was influenced by the cation permeability (Na+ vs Na+ and Ca2+) of the channels expressed, we compared ethanol inhibition of Ca(2+)-permeable glutamate receptors (GluRs) in oocytes perfused with normal- and high-Ca2+ buffers. The ethanol inhibition was much greater when Ca2+ was the only permeant cation. When Ba2+ was substituted for Ca2+, the ethanol inhibition was reduced, although it was still greater than with normal buffer. The enhanced ethanol inhibition of kainate-stimulated Ca2+ currents was reduced in oocytes injected with the Ca2+ chelator BAPTA, suggesting a role for intracellular Ca2+ in mediating enhanced ethanol sensitivity of kainate channels. The enhanced ethanol inhibition of Ca2+ currents was not due to a direct ethanol inhibition of Ca(2+)-stimulated Cl- currents in the oocyte because ethanol produced no effect on Ca(2+)-stimulated Cl- currents induced by injection of myo-inositol-1,4,5-trisphosphate. Because Ca2+ activates protein kinase C (PKC) and because we found that the PKC activator phorbol 12-myristate 13-acetate inhibits kainate responses (Dildy-Mayfield and Harris, 1994), we examined the role of PKC in mediating the enhanced ethanol inhibition of kainate responses produced by increased Ca2+. Inhibition of PKC by injection of the PKC inhibitor peptide or calphostin C prevented the enhanced ethanol inhibition of kainate-induced Ca2+ responses without altering ethanol inhibition in normal buffer. Thus, ethanol inhibition of kainate channels may involve two mechanisms, one that is independent of PKC and a second type that is due to activation of PKC under conditions of elevated Ca2+, resulting in enhanced inhibition of kainate responses.

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Permeation of calcium through excitatory amino acid receptor channels in cultured rat hippocampal neurones.

Cited by 460 publications

References 26 publications

Spatiotemporal patterns of γ frequency oscillations tetanically induced in the rat hippocampal slice

Spatiotemporal patterns of γ frequency oscillations tetanically induced in the rat hippocampal slice

Novel kainate derivatives: potent depolarizing actions on spinal motoneurones and dorsal root fibres in newborn rats

Ethanol inhibits kainate responses of glutamate receptors expressed in Xenopus oocytes: role of calcium and protein kinase C

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