Cellular Localization of AMPA Type Glutamate Receptor Subunits in the Basal Ganglia of Pigeons <i>(Columba livia)</i>

Abstract

Corticostriatal and thalamostriatal projections utilize glutamate as a neurotransmitter in mammals and birds. The influence on striatum is mediated, in part, by ionotropic AMPA-type glutamate receptors, which are heteromers composed of GluR1–4 subunits. Although the cellular localization of AMPA-type subunits has been well characterized in mammalian basal ganglia, their localization in avian basal ganglia has not. We thus carried out light microscopic single- and double-label and electron microscopic single-label immunohistochemical studies of GluR1–4 distribution and cellular localization in pigeon basal ganglia. Single-label studies showed that the striatal neuropil is rich in GluR1, GluR2, and GluR2/3 immunolabeling, suggesting the localization of GluR1, GluR2 and/or GluR3 to the dendrites and spines of striatal projection neurons. Double-label studies and perikaryal size distribution determined from single-label material indicated that about 25% of enkephalinergic and 25% of substance P-containing striatal projection neuron perikarya contained GluR1, whereas GluR2 was present in about 75% of enkephalinergic neurons and all substance-P -containing neurons. The perikaryal size distribution for GluR2 compared to GluR2/3 suggested that enkephalinergic neurons might more commonly contain GluR3 than do substance P neurons. Parvalbuminergic and calretininergic striatal interneurons were rich in GluR1 and GluR4, a few cholinergic striatal interneurons possessed GluR2, but somatostatinergic striatal interneurons were devoid of all subunits. The projection neurons of globus pallidus all possessed GluR1, GluR2, GluR2/3 and GluR4 immunolabeling. Ultrastructural analysis of striatum revealed that GluR1 was preferentially localized to dendritic spines, whereas GluR2/3 was found in spines, dendrites, and perikarya. GluR2/3-rich spines were generally larger than GluR1 spines and more frequently possessed perforated post-synaptic densities. These results show that the diverse basal ganglia neuron types each display different combinations of AMPA subunit localization that shape their responses to excitatory input. For striatal projection neurons and parvalbuminergic interneurons, the combinations resemble those for the corresponding cell types in mammals, and thus their AMPA responses to glutamate are likely to be similar.

Neurochemical compartmentalization within the pigeon basal ganglia

“…The specificity has been examined by the manufacturer and researchers (Heizmann and Celio, 1987; Sigma-Aldrich). It has been used previously in pigeons to describe the distribution of PARV neurons in the basal ganglia (Reiner and Anderson, 1993; Lavergetta et al, 2006), and the present results are consistent with their findings. Our data are qualitatively similar to the staining patterns shown in a previous study in in the pigeon using another PARV antibody (Husband and Shimizu, 2012).…”

“…6–8). The large GABAergic pallidal neurons are enriched in PARV, and so PARV+ neurons are plentiful in globus pallidus (Laverghetta et al, 2006). ChAT-immunolabeled neurons are relatively plentiful within the globus pallidus as well, although less numerous than in the INP.…”

“…Sections were then washed, mounted onto slides, osmicated and coverslipped for subsequent examination. For immunolabeling with CALB and PARV, the method described in Laverghetta et al (2006) was used. For SP, ENK and VIP, colchicine-treated material that had been prepared for use in prior studies was also available (Anderson and Reiner, 1990a, b, 1991).…”

The avian subpallium: New insights into structural and functional subdivisions occupying the lateral subpallial wall and their embryological origins

“…These neurons appear to have similar electrophysiological properties to their mammalian counterparts (Farries and Perkel, 2000; Farries et al, 2005b). In mammals, a fourth type of interneuron contains GABA and the calcium binding protein calretinin (Bennett and Bolam, 1993; Figueredo-Cárdenas et al, 1996), and this cell type is rare or absent in bird MSt (Laverghetta et al, 2005). …”

Morphometric analysis of the AMPA-type neurons in the Deiters vestibular complex of the chick brain

“…Similarly to other vertebrates, notably in the lateral portion of the vestibular nucleus of mammals (Popper et al, 1997;Chen et al, 2000), VNC neurons of mature chicks express GluR2/3 and GluR4 on soma and dendrites as well (Rabbath et al, 2002) but we do not know if its distribution can be clustered in different parts of the neuron. At specific parts of the avian basal ganglia, as the striatum, the constitution of the AMPA-type receptors is regionalized with GluR2/3 composing GluRs along the entire neuron (perikarya and cellular body), whereas, the GluR4 subunit appears to be restricting to receptors found in the soma (Laverghetta et al, 2006). Striatal neurons of mammals also present subunit regionalization (Popper et al, 1997;Deng et al, 2007) indicating functional differences concerning neuronal properties driven by GluRs constitution.…”