Elsevier

Neuroscience

Volume 108, Issue 1, 5 December 2001, Pages 129-141
Neuroscience

Functionally different AMPA-type glutamate receptors in morphologically identified neurons in rat superficial superior colliculus

https://doi.org/10.1016/S0306-4522(01)00407-9Get rights and content

Abstract

In the superficial superior colliculus, a center of sensory processing related to visual salience, glutamate is used as a major excitatory neurotransmitter. α-Amino-3-hydroxy-5-methyl-4-isoxazole propionic acid (AMPA)-type glutamate receptors include a Ca2+-impermeable, outwardly rectifying type (type I) and a Ca2+-permeable, inwardly rectifying type (type II). To study the contribution of these AMPA receptor subtypes to visual sensory processing in the superior colliculus, we investigated the expression of these two types of AMPA receptors in six morphologically identified subgroups of neurons in the superficial superior colliculus by whole-cell recording using slice preparations of young (17–23 days old) and adult (60–68 days old) rats. Both outwardly and inwardly rectifying current responses were observed to pressure applied 10 mM kainate, a non-desensitizing AMPA receptor agonist. These currents were completely abolished by the selective AMPA receptor antagonist 1-(4-aminophenyl)-3-methylcarbamyl-4-methyl-7,8-methylenedioxy-3,4-dihydro-5H-2,3-benzodiazepine (100 μM). The type II receptor antagonist spermine (1 mM) suppressed inwardly rectifying responses. The degree of inward rectification was correlated with the ratio of suppression by spermine, and inversely correlated with estimated Ca2+ permeability, indicating that the degree of rectification reflects the relative amount of co-expressed type I and type II receptors. An inwardly rectifying and spermine-sensitive AMPA component of excitatory postsynaptic currents was observed, suggesting involvement of type II receptors in synaptic transmission. Morphological analysis revealed that a substantial population of horizontal cells in both young and adult rats (n=31/53 and 15/17, respectively) and all wide field multipolar cells in adult rats (n=6) showed inwardly rectifying AMPA receptor responses.

From these results we suggest that type I and type II AMPA receptors are co-expressed with varying ratios in individual neurons in the rat superficial superior colliculus, and that type II receptors are abundantly expressed in most horizontal cells and wide field multipolar cells. Since these neurons are putatively GABAergic inhibitory neurons and have wide dendritic trees, type II receptors may contribute to the regulation of remote inhibitory interaction in the visual field map in the the superficial superior colliculus.

Section snippets

Preparations

The present experiments were approved by the Animal Research Committee in the Okazaki National Research Institutes. All efforts were made to minimize both the suffering and the number of animals used in this study. The methods employed in this study were in general similar to those described in the preceding studies (Isa et al., 1998, Saito and Isa, 1999). Frontal slices (200–500 μm thick) of the SC were prepared from young (17–23-day-old) and adult (60–68-day-old) Wistar rats (Japan SLC,

Results

Data were obtained from 284 neurons in slices from young rats and 67 neurons in slices from adult rats. Because of difficulties in obtaining healthy slices from adult rats, most experiments were performed using young rats except where otherwise specified. The recorded neurons were distributed throughout the whole depth of the sSC.

Expression of two types of AMPA receptors in the rat superficial superior colliculus

The results of the present study have shown that both neurons with linear or outwardly rectifying KA responses and those with inwardly rectifying KA responses are present in the rat sSC. The reversal potentials of the KA responses in the isotonic Na+-free, high Ca2+ solution were inversely correlated with the RI value, indicating that neurons with stronger inward rectification showed higher Ca2+ permeability. Previous studies have demonstrated that two types of functionally different AMPA

Acknowledgements

We thank Dr. Yasuhiko Saito for valuable comments on the earlier version of the manuscript. This study was supported by grants from the Ministry of Education, Science, Culture and Sports of Japan (Projects 10480232, 10164247 and 11145241), the Core Research for Evolutional Science and Technology (CREST) of the Japan Science and Technology Corporation and the Mitsubishi Foundation, Naito Memorial Foundation and Daiko Foundation.

References (50)

  • P Jonas et al.

    Molecular mechanisms controlling calcium entry through AMPA-type glutamate receptor channels

    Neuron

    (1995)
  • P Jonas et al.

    Differences in Ca2+ permeability of AMPA-type glutamate receptor channels in neocortical neurons caused by differential GluR-B subunit expression

    Neuron

    (1994)
  • M Kondo et al.

    Expression of AMPA receptors in rat superior colliculus and effect of orbital enucleation

    Brain Res.

    (2000)
  • A.R Labriola et al.

    Cellular morphology in the visual layer of the developing rat superior colliculus

    Exp. Neurol.

    (1977)
  • C Leranth et al.

    AMPA receptors in the rat and primate hippocampus: a possible absence of GluR2/3 subunits in most interneurons

    Neuroscience

    (1996)
  • S Ozawa et al.

    Two distinct types of AMPA responses in cultured rat hippocampal neurons

    Neurosci. Lett.

    (1993)
  • A.V Paternain et al.

    Selective antagonism of AMPA receptors unmasks kainate receptor-mediated responses in hippocampal neurons

    Neuron

    (1995)
  • T Sakurai et al.

    Reduction of glutamate content in rat superior colliculus after retino-tectal denervation

    Neurosci. Lett.

    (1990)
  • A Tokunaga et al.

    Dendritic patterns of neurons in the rat superior colliculus

    Exp. Neurol.

    (1976)
  • K.E Binns et al.

    Different roles for GABAA and GABAB receptors in visual processing in the rat superior colliculus

    J. Physiol.

    (1997)
  • M Brecht et al.

    Synchronization of visual responses in the superior colliculus of awake cats

    NeuroReport

    (2001)
  • M Brecht et al.

    Patterns of synchronization in the superior colliculus of anesthetized cats

    J. Neurosci.

    (1999)
  • F.A Edwards et al.

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

    Pflugers Arch.

    (1989)
  • E.C Fuchs et al.

    Genetically altered AMPA-type glutamate receptor kinetics in interneurons disrupt long-range synchrony of gamma oscillation

    Proc. Natl. Acad. Sci. USA

    (2001)
  • J.G Gu et al.

    Synaptic strengthening through activation of Ca2+-permeable AMPA receptors

    Nature

    (1996)
  • Cited by (14)

    • Visual System

      2015, The Rat Nervous System: Fourth Edition
    • Visual System

      2004, The Rat Nervous System
    • Neonatal pial surface electroporation

      2014, Journal of Visualized Experiments
    View all citing articles on Scopus
    View full text