Journal of Neuroscience, Vol 13, 782-792, Copyright © 1993 by Society for Neuroscience
The striatal mosaic in primates: striosomes and matrix are differentially enriched in ionotropic glutamate receptor subunits
LJ Martin, CD Blackstone, RL Huganir and DL Price
Department of Pathology, Johns Hopkins University School of Medicine, Baltimore, Maryland 21205.
The cellular and subcellular distributions of the ionotropic alpha-
amino-3-hydroxy-5-methyl-4-isoxazole propionic acid (AMPA)-preferring
glutamate receptor (GluR) in monkey striatum were demonstrated
immunocytochemically using anti-peptide antibodies to individual subunits
of the AMPA receptor. These antibodies specifically recognize GluR1, GluR4,
and an epitope common to GluR2 and GluR3 (designated as GluR2/3). On
immunoblots, the antibodies detect proteins ranging from 102 to 108 kDa in
total homogenates of monkey striatum, hippocampus, and cerebellum. By
immunoblotting, GluR1 and GluR2/3 are considerably more abundant than GluR4
in the caudate nucleus. Within the caudate nucleus, putamen, and nucleus
accumbens, numerous neuronal perikarya, dendrites, and spines show GluR1
and GluR2/3 immunoreactivities. GluR1- and GluR2/3-enriched striatal
neurons have the morphology, transmitter specificity, and distribution of
medium-sized (10-20 microns) spiny neurons; large (20-60 microns) round
neurons exhibit GluR4 immunoreactivity. GluR1 immunoreactivity, but not
GluR2/3 or GluR4 immunoreactivity, is more intense in the ventral striatum
(i.e., nucleus accumbens) than in the dorsal striatum, and GluR1 is
enriched within dendritic spines in the neuropil of the nucleus accumbens
and striosomes in the dorsal striatum. In the caudate nucleus, these
patches of dense GluR1 immunoreactivity align with regions low in calcium
binding protein immunoreactivity and high in substance P immunoreactivity.
Within striosomes, GluR1 immunoreactivity is more abundant than GluR2/3
immunoreactivity; GluR4 immunoreactivity is sparse in striosomes, but the
matrix contains large, GluR4-positive cholinergic neurons. This study
demonstrates that, within monkey striatum, subunits of ionotropic AMPA GluR
have differential distributions within striosomes and matrix. Furthermore,
the results suggest that neurons within striatal striosomes and matrix may
express different combinations of GluR subunits, thus forming receptors
with different channel properties and having consequences that may be
relevant physiologically and pathophysiologically. Neurons within these two
striatal compartments may have different roles in the synaptic plasticity
of motor systems.