Neurochemical compartmentalization within the pigeon basal ganglia

• Sixteen distinct compartments were identified in the pigeon basal ganglia using multiple neurochemical markers.
• The pigeon striatum contains neurochemical regions comparable to the mammalian somatomotor, associational and limbic striatum.
• A neurochemically distinct area located in the medialmost striatum of pigeons appears to be unique to birds.
• The ventral striatum contains neurochemical regions similar to the mammalian accumbens core, shell, and rostral areas.
• Most compartments were highly conserved during tetrapod evolution, yet unique avian compartments have also evolved.

The goals of this study were to use multiple informative markers to define and characterize the neurochemically distinct compartments of the pigeon basal ganglia, especially striatum and accumbens. To this end, we used antibodies against 12 different neuropeptides, calcium-binding proteins or neurotransmitter-related enzymes that are enriched in the basal ganglia. Our results clarify boundaries between previously described basal ganglia subdivisions in birds, and reveal considerable novel heterogeneity within these previously described subdivisions. Sixteen regions were identified that each displayed a unique neurochemical organization. Four compartments were identified within the dorsal striatal region. The neurochemical characteristics support previous comparisons to part of the central extended amygdala, somatomotor striatum, and associational striatum of mammals, respectively. The medialmost part of the medial striatum, however, has several unique features, including prominent pallidal-like woolly fibers and thus may be a region unique to birds. Four neurochemically distinct regions were identified within the pigeon ventral striatum: the accumbens, paratubercular striatum, ventrocaudal striatum, and the ventral area of the lateral part of the medial striatum that is located adjacent to these regions. The pigeon accumbens is neurochemically similar to the mammalian rostral accumbens. The pigeon paratubercular and ventrocaudal striatal regions are similar to the mammalian accumbens shell. The ventral portions of the medial and lateral parts of the medial striatum, which are located adjacent to accumbens shell-like areas, have neurochemical characteristics as well as previously reported limbic connections that are comparable to the accumbens core. Comparisons to neurochemically identified compartments in reptiles, mammals, and amphibians indicate that, although most of the basic compartments of the basal ganglia were highly conserved during tetrapod evolution, uniquely avian compartments may exist as well.