Dendritic arbors of spiny neurons in the primate striatum are directionally polarized

Despite the relatively unfeatured cytoarchitecture of the striatum, this large subcortical region has been found to have a modular macroscopic substructure comprising the neurochemically distinct striosomes and matrix, and, within the matrix, patchy input and output arrangements called matrisomes. In the study reported here, we explored the possibility that the cellular architecture of the striatum is also more specialized than previously suspected. We injected medium spiny neurons in lightly fixed slices of the squirrel monkey caudate nucleus, reconstructed their dendritic arbors, and analyzed the orientations of these arbors with respect to the cardinal planes of the striatum. The data were unequivocal in suggesting that many spiny neurons, whether near striosomes or not, have dendritic arbors with preferred orientations along a diagonal axis running from rostral, dorsal, and medial to caudal, ventral, and lateral. This axis corresponds to the orientations of many striosomes and matrisomes in the squirrel monkey's caudate nucleus. We therefore suggest that the primate striatum is characterized not only by a macroscopic organization dividing it into striosomes and matrisomes, but also by a microscopic architecture observed by the dendritic arbors of many of its projection neurons. We obtained comparable supplementary observations for the ferret caudate nucleus, suggesting that such spatial alignment of spiny dendritic arbors may be a general feature of striatal organization. These polarized dendritic arrangements could provide a cellular framework for compartmental input-output processing within the striatum.