The dopaminergic innervation of the pigeon telencephalon: distribution of DARPP-32 and co-occurrence with glutamate decarboxylase and tyrosine hydroxylase

Abstract

Dopaminergic axons arising from midbrain nuclei innervate the mammalian and avian telencephalon with heterogeneous regional and laminar distributions. In primate, rodent, and avian species, the neuromodulator dopamine is low or almost absent in most primary sensory areas and is most abundant in the striatal parts of the basal ganglia. Furthermore, dopaminergic fibres are present in most limbic and associative structures. Herein, the distribution of DARPP-32, a phosphoprotein related to the dopamine D1-receptor, was investigated in the pigeon telencephalon by immunocytochemical techniques. Furthermore, co-occurrence of DARPP-32-positive perikarya with tyrosine hydroxylase-positive pericellular axonal “baskets” or glutamate decarboxylase-positive neurons, as well as co-occurrence of tyrosine hydroxylase and glutamate decarboxylase were examined. Specificity of the anti-DARPP-32 monoclonal antibody in pigeon brain was determined by immunoblotting. The distribution of DARPP-32 shared important features with the distribution of D1-receptors and dopaminergic fibres in the pigeon telencephalon as described previously. In particular, DARPP-32 was highly abundant in the avian basal ganglia, where a high percentage of neurons were labelled in the “striatal” parts (paleostriatum augmentatum, lobus parolfactorius), while only neuropil staining was observed in the “pallidal” portions (paleostriatum primitivum). In contrast, DARPP-32 was almost absent or present in comparatively lower concentrations in most primary sensory areas. Secondary sensory and tertiary areas of the neostriatum contained numbers of labelled neurons comparable to that of the basal ganglia and intermediate levels of neuropil staining. Approximately up to one-third of DARPP-32-positive neurons received a basket-type innervation from tyrosine hydroxylase-positive fibres in the lateral and caudal neostriatum, but only about half as many did in the medial and frontal neostriatum, and even less so in the hyperstriatum. No case of colocalization of glutamate decarboxylase and DARPP-32 and no co-occurrence of glutamate decarboxylase-positive neurons and tyrosine hydroxylase-basket-like structures could be detected out of more than 2 000 glutamate decarboxylase-positive neurons examined, although the high DARPP-32 and high tyrosine hydroxylase staining density hampered this analysis in the basal ganglia. In conclusion, the pigeon dopaminergic system seems to be organized similar to that of mammals. Apparently, in the telencephalon, dopamine has its primary function in higher level sensory, associative and motor processes, since primary areas showed only weak or no anatomical cues of dopaminergic modulation. Dopamine might exert its effects primarily by modulating the physiological properties of non-GABAergic and therefore presumably excitatory units.