Differential synaptic innervation of striatofugal neurones projecting to the internal or external segments of the globus pallidus by thalamic afferents in the squirrel monkey

It is well established that the centromedian nucleus (CM) is the major source of thalamic afferents to the sensorimotor territory of the striatum in monkeys. However, the projection sites of striatal neurones contacted by thalamic afferents still remain to be determined. We therefore carried out an anatomical study aimed at elucidating the hodology of striatal neurones that receive input from the CM in squirrel monkeys. Our approach was to combine the anterograde transport of Phaseolus vulgaris-leucoagglutinin (PHA-L) or biocytin from the CM with the retrograde transport of biotinylated dextran-amine (bio-dex) or PHA-L from the internal (GPi) or external (GPe) segments of the globus pallidus. Following CM injections, rich plexuses of anterogradely labelled, thin varicose fibres aggregated in the form of bands that were confined to the postcommissural region of the putamen. On the other hand, injections into the GPe or GPi led to profuse retrograde labelling of a multitude of medium-sized spiny neurones. In cases where the injections involved the caudoventral two-thirds of the GPe or GPi, the retrogradely labelled striatopallidal cells and the anterogradely labelled thalamostriatal fibres occurred in the sensorimotor territory of the putamen. After injections into either pallidal segments, clusters of retrogradely labelled cells were in register with bands of anterogradely labelled thalamic fibres. However, electron microscopic analysis of striatal regions containing both anterogradely labelled thalamic afferents and retrogradely labelled cells revealed that terminals from the CM frequently form asymmetric synapses with dendritic shafts and spines of striato-GPi cells but rarely with those of striato-GPe cells. In conclusion, our findings demonstrate that thalamic afferents from the CM innervate preferentially striatopallidal neurones projecting to the GPi in monkeys. These results indicate that the striatopallidal neurones contributing to the “direct” and “indirect” output pathways are differentially innervated by thalamic afferents in primates. © 1996 Wiley-Liss, Inc.