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

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 Ca 2+-impermeable, outwardly rectifying type (type I) and a Ca 2+-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-5 H-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 Ca 2+ 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.