Efferent connections of the centromedian and parafascicular thalamic nuclei in the squirrel monkey: A light and electron microscopic study of the thalamostriatal projection in relation to striatal heterogeneity

Abstract

The organization of the thalamostriatal projections arising from the centromedian (CM) and parafascicular (Pf) thalamic nuclei in the squirrel monkey (Saimiri sciureus) was studied at both light and electron microscopic levels. Following selective injections of the anterograde axonal tracer Phaseolus vulgaris‐leucoagglutinin (PHA‐L) into the CM or Pf, patterns of terminal arborization within the striatum were compared to the biochemical heterogeneity of the striatum as revealed by immunohistochemical staining for the calcium‐binding protein calbindin D‐28k (CaBP), and histochemical staining for the enzymes acetylcholinesterase (AChE) and nicotinamide adenine dinucleotide phosphate‐diaphorase (NADPH‐diaphorase). The PHA‐L‐labeled axon terminals within the striatum were further analyzed at the ultrastructural level to characterize their pattern of synaptic organization. Dense and heterogeneous terminal fields occur in the „sensorimotor”︁ territory of the striatum after CM injections, or in the „associative”︁ striatal territory following Pf injections. In the associative territory labeled axons arborize in a diffuse manner predominantly within areas enriched with CaBP, AChE, or NADPH‐diaphorase, representing the matrix compartment, and tend to avoid areas poor in these substances, corresponding to the patch/striosome compartment. In the sensorimotor territory labeled axons form bands that occupy a subregion of the NADPH‐diaphorase‐rich zone in the putamen. The terminal pattern of the CM‐striatal projection suggests the existence of a more complex mosaic organization within the sensorimotor territory. Ultrastructural analysis of PHA‐L‐labeled elements within the striatum reveals that both CM and Pf projections form asymmetric synapses upon dendrites and spines of striatal cells. A total of 339 PHA‐L‐labeled boutons were examined after CM injections and compared to 293 boutons following Pf injections. After CM injections, 29% of PHA‐L‐labeled terminals form synapses on dendritic spines and 66% on dendritic shafts, whereas after Pf injections only 12% of synapses occur on dendritic spines compared to 81% on dendritic shafts. Labeled terminals forming axosomatic or axoaxonic synapses were not seen within the striatum following either CM or Pf injections. It is concluded that in the squirrel monkey: (1) Pf‐striatal fibers profusely arborize within the matrix compartment of the associative territory, (2) CM‐striatal fibers form bands that occupy a subregion of the NADPH‐diaphorase‐rich zone within the sensorimotor territory, and (3) that both Pf‐ and CM‐striatal projections establish asymmetric synapses with dendrites and spines of medium‐sized spiny cells. These results suggest that the complementary CM and Pf projections to the striatum are in a crucial position to exert a powerful and highly ordered excitatory influence upon the output neurons of the striatum in primates.