Neuron
Volume 11, Issue 6, December 1993, Pages 1083-1091
Journal home page for Neuron

Article
Different glutamate receptor channels mediate fast excitatory synaptic currents in inhibitory and excitatory cortical neurons

https://doi.org/10.1016/0896-6273(93)90221-CGet rights and content

Abstract

Spontaneous excitatory postsynaptic currents (sEPSCs) and responses to rapid application of glutamate were recorded in excitatory spiny, pyramidal neurons and compared with those recorded in inhibitory aspiny interneurons. The sEPSC decay time constant was faster in aspiny interneurons (2.5 ms) compared with pyramidal neurons (4.6 ms). The decay time constant in response to a brief application (1 ms) of glutamate (10 mM) in patches excised from pyramidal and aspiny interneurons were similar (1.9 and 2.7 ms, respectively). However, the rate of desensitization was faster in patches from interneurons compared with pyramidal neurons (3.4 and 12.0 ms, respectively). In addition, single-channel conductance was larger in aspiny interneurons (27 pS) compared with pyramidal neurons (9 pS). These results indicate that pyramidal neurons and aspiny interneurons express different non-N-methyl-d-aspartate receptors and that selective desensitization of interneuron receptors may contribute to depression of inhibition.

References (50)

  • L.A. Raymond et al.

    Phosphorylation of amino acid neurotransmitter receptors in synaptic plasticity

    Trends Neurosci.

    (1993)
  • L.O. Trussell et al.

    Glutamate receptor desensitization and its role in synaptic transmission

    Neuron

    (1989)
  • L.O. Trussell et al.

    Desensitization of AMPA receptors upon multiquantal neurotransmitter release

    Neuron

    (1993)
  • L. Vyklicky et al.

    Modulation of excitatory synaptic transmission by drugs that reduce desensitization at AMPA/kainate receptors

    Neuron

    (1991)
  • W. Wisden et al.

    Mammalian ionotropic glutamate receptors

    Curr. Opin. Neurobiol.

    (1993)
  • M. Abeles

    Corticonics

    (1991)
  • Y. Ben-Ari et al.

    Hippocampal seizures and failure of inhibition

    Can. J. Physiol. Pharmacol.

    (1979)
  • J.D. Clements et al.

    The time course of glutamate in the synaptic cleft

    Nature

    (1992)
  • D. Colquhoun et al.

    Action of brief pulses of glutamate on AMPA/kainate receptors in patches from different neurones of rat hippocampal slices

    J. Physiol.

    (1992)
  • B.W. Connors et al.

    Intrinsic firing patterns of diverse neocortical neurons

    Trends Neurosci.

    (1990)
  • C.H. Davies et al.

    Pairedpulse depression of monosynaptic GABA-mediated inhibitory postsynaptic responses in rat hippocampus

    J. Physiol.

    (1990)
  • R.A. Deisz et al.

    Frequency-dependent depression of inhibition in guinea pig neocortex in vitro by GABAB receptor feed-back on GABA release

    J. Physiol.

    (1989)
  • F.A. Edwards et al.

    A thin slice preparation for patch clamp recordings from neurones of the mammalian central nervous system

    Pflügers Arch.

    (1989)
  • T.A. Gilbertson et al.

    Permeation of calcium ions through non-NMDA glutamate channels in retinal bipolar cells

    Science

    (1991)
  • O.P. Hamill et al.

    Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches

    Pflügers Arch.

    (1981)
  • Cited by (155)

    • The mechanistic link between Arc/Arg3.1 expression and AMPA receptor endocytosis

      2018, Seminars in Cell and Developmental Biology
      Citation Excerpt :

      When the neuron is at a depolarized membrane potential (+ 40 mV), the polyamines block the AMPAR channel more strongly, preventing the passage of ions through the channel. Thus GluA2-lacking AMPARs are said to be inwardly rectifying which means that they pass less outward current than inward current ([38–42]; Fig. 2C,D). In contrast, receptors containing edited GluA2 subunits have a linear current-voltage relationship [43,44].

    • Thalamic Control of Cognition and Social Behavior Via Regulation of Gamma-Aminobutyric Acidergic Signaling and Excitation/Inhibition Balance in the Medial Prefrontal Cortex

      2018, Biological Psychiatry
      Citation Excerpt :

      We found that MD inhibition recapitulated certain core phenotypes by reducing inhibition in layer V PNs with associated decreases in α1-GABAAR-mediated sIPSCs. The selective GABAergic hypofunction observed is likely attributable to distinct properties of thalamocortical synapses to PNs versus PVIs such as AMPA receptor composition or density of presynaptic release sites (48,49). If AMPA receptors on PVIs have larger conductances compared with those on PNs, we would expect that decreasing the activity of thalamocortical inputs may have larger consequences for PVI activity.

    • Modulating synaptic NMDA receptors

      2017, Neuropharmacology
    • Nuclear respiratory factor 2 regulates the transcription of AMPA receptor subunit GluA2 (Gria2)

      2014, Biochimica et Biophysica Acta - Molecular Cell Research
      Citation Excerpt :

      This editing converts a glutamine to an arginine in GluA2's critical pore-forming region and renders GluA2-containing receptors less permeable to Ca2 + [26–28]. GluA2-containing receptors are inwardly rectifying and exhibit low single channel conductance as compared to those that do not contain GluA2 subunits [24,29–31]. The presence or absence of the GluA1, GluA3, and GluA4 subunits do not alter the properties of the AMPA receptor to the same extent as the presence or absence of GluA2.

    View all citing articles on Scopus

    Present address: Department of Anatomy and Neurobiology, University of Tennessee, Memphis, Memphis, Tennessee 38163.

    View full text