Functional circuitry of the avian basal ganglia: implications for basal ganglia organization in stem amniotes

Histochemical, pathway tracing, and neuropeptide/neurotransmitter localization studies in birds, reptiles and mammals during the 1970s and 80s clearly showed that the telencephalon in all amniotes consists of a prominent ventrally situated subpallial region termed the basal ganglia, and a large overlying region involved in higher order information processing termed the pallium or cortex. These studies also showed that the basal ganglia in all extant amniote groups possessed neurochemically and hodologically distinct striatal and pallidal territories. More recently, studies of the localization of genes controlling regional brain development have confirmed the homology of the basal ganglia among amniotes. In our ongoing studies, we have identified several aspects of the functional organization of the basal ganglia that birds also share with mammals. These include: (1) an extensive glutamatergic "cortico"-striatal input and distinctive, cell-type specific localization of glutamate receptor subtypes; (2) an extensive, presumptively glutamatergic intralaminar thalamic input to striatal neurons; (3) an extensive dopaminergic input from the midbrain targeting both substance P (SP) type and enkephalin (ENK) type striatal projection neurons, with SP-type striatal neurons seemingly richer in the D-1 type dopamine receptor; and (4) SP+ and ENK+ striatal outputs giving rise to functionally distinct so-called direct and indirect motor output pathways, with the direct pathway having a pallido-thalamo-motor cortex loop and the indirect pathway relaying back to the direct circuit via the subthalamic nucleus. These findings suggest that the major aspects of the cellular organization and functional circuitry of the basal ganglia in stem amniotes were already as observed in living amniotes, as therefore presumably was its key role in movement control. Because the organization of the basal ganglia of anamniotes is clearly less elaborate than in amniotes, and because the basal ganglia and cortex in amniotes are clearly extensively interconnected structures, it seems likely that stem amniotes were characterized by a major step forward in the grade of telencephalic organization of both the basal ganglia and the pallium.