Efferent connections of the internal globus pallidus in the squirrel monkey: II. Topography and synaptic organization of pallidal efferents to the pedunculopontine nucleus.

The first objective of the present study was to verify whether projections from regions of the internal pallidum (GPi) that receive inputs from different functional areas of the striatum remain segregated at the level of the pedunculopontine nucleus (PPN) in squirrel monkeys. Second, we analyzed the ultrastructural features and synaptic organization of pallidal terminals in contact with PPN neurons. This was achieved by performing iontophoretic injections of biotinylated dextran amine (BDA) in different regions of the GPi. The animals were pooled into three groups on the basis of the location of the injection sites and the resulting distribution of retrogradely labelled striatal neurons. The experimental groups were divided as follows: group 1: injections in the dorsal one-third of the GPi, retrograde labelling in the head and body of the caudate nucleus ("associative striatum"); group 2: injections in the ventrolateral two-thirds of the GPi, retrograde labelling in the postcommissural region of the putamen ("sensorimotor striatum"); and group 3: injections in the rostromedial pole of the GPi, retrograde labelling in the ventral striatum ("limbic striatum"). These injections led to the anterograde labelling of varicose fibers that arborized profusely in common regions of the PPN dorsal to the brachium conjunctivum. The fields of fibers that arose from the dorsal one-third and the rostromedial pole of the GPi were more widely spread than the afferents from the ventrolateral two-thirds of the GPi. Small numbers of retrogradely labelled cells were encountered in the PPN after each injection in the GPi. Some of them were tightly surrounded by large, BDA-containing varicosities, which implies that the connections between the GPi and the PPN are partly reciprocal. In sections processed for the simultaneous localization of beta-nicotinamide adenine dinucleotide phosphate (NADPH)-diaphorase (a marker of cholinergic cells in the PPN) and BDA, the anterogradely labelled fibers largely avoided the dense aggregate of NADPH-diaphorase-containing neurons in the PPN pars compacta (PPNc) but, rather, established contacts with unlabelled neurons in the pars dissipata (PPNd). In the electron microscope, the GPi terminals were large (1.0-5.0 microns in diameter), contained many mitochondria and pleomorphic vesicles, and formed symmetric synapses predominantly with proximal dendrites of PPN cells. In conclusion, our data suggest that the noncholinergic neurons of the PPNd are potential targets for the integration of information arising from different functional territories of the GPi in primates. The PPNd is thus in a position to act as an interface between motivational, cognitive, and motor information transmitted along the pallidotegmental projection in primates.