Differential synaptic innervation of neurons in the internal and external segments of the globus pallidus by the GABA- and glutamate-containing terminals in the squirrel monkey.

The present study aimed at comparing the pattern of synaptic innervation of neurons in the external (GPe) and internal (GPi) pallidum by gamma-aminobutyric acid (GABA)- and glutamate-immunoreactive terminals in the squirrel monkey. Four major populations of terminals were encountered in GPe and GPi. Our findings combined with those obtained in previous tract-tracing studies reveal that the synaptic innervation of perikarya in GPe is strikingly different from that in GPi. Although the GABA-positive type I boutons (from the striatum) represent 85% of the terminals in contact with somata in GPe, only 32% of the axosomatic synapses involve this type of terminal in GPi. However, the type II terminals (from GPe), which display a moderate level of GABA and glutamate immunoreactivities, account for 48% of the boutons in contact with perikarya in GPi but only 10% in GPe. In both pallidal segments, less than 10% of the axosomatic synapses involve the glutamate-immunoreactive type III terminals (from the subthalamic nucleus). Finally, the type IIa boutons (unknown source), which show levels of immunoreactivities similar to the type II terminals, account for 12% of the boutons in contact with perikarya in GPi but only 4% in GPe. In contrast to perikarya, the innervation of dendritic shafts is similar in both GPe and GPi; more than 80% of the axodendritic synapses involve the type I terminals, 10-15% involve the type III terminals, less than 5% are formed by the type II boutons, and less than 1% involve the type IIa terminals. Three other categories of boutons (types IV, V, VI) account for less than 1% of the total population of terminals in GPe and GPi. In conclusion, our findings demonstrate a differential synaptic innervation of neuronal perikarya in GPe and GPi in primates. These data suggest that the two pallidal segments are separate functional entities of which the neuronal activity is largely controlled by extrinsic inputs that are differentially distributed at the level of single cells.