Two input systems for body representations in the primate striatal matrix: experimental evidence in the squirrel monkey

The striatum is important in basal ganglia motor control and movement disorders. In this study we demonstrate the existence of two distinct sensorimotor cortical input systems to the striatum of the squirrel monkey. The first is a group of discrete zones in the extrastriosomal matrix of the putamen (“matrisomes”) that receive somatotopically organized projections from both the body map in ipsilateral primary motor cortex (MI) and maps in ipsilateral primary somatosensory cortex (SI). The second system is a group of matrisomes in largely different locations that receive somatotopically organized inputs from contralateral MI but not SI. Intracortical microstimulation and multiunit recording were used to guide deposits of multiple anterograde tracers in MI and SI. Striosome/matrix architecture was demonstrated by enkephalin immunohistochemistry. We found that inputs from regions of ipsilateral MI and SI that represented the same body parts sent projections to the same matrisomes of the ipsilateral putamen. Contralateral MI sent its strongest inputs to matrisomes that tended to interdigitate with those receiving inputs from ipsilateral SI and MI, except the contralateral MI face region, which sent projections that overlapped those from the ipsilateral MI face region. MI regions representing axial body parts (trunk and face) sent stronger representations to the contralateral putamen than did those representing distal parts (hand and foot). SI sent no contralateral projection. Thus, with the exception of the face representation, inputs from contralateral and ipsilateral body representations may alternate in the primate striatal matrix, an arrangement reminiscent of the alternating ocular dominance columns in visual cortex. Ipsilateral SI and MI and contralateral MI all innervated matrisomes intermingled with striosomes and with matrisomes not receiving sensorimotor cortical input. The patchiness of these maps is thus unlike the smoother somatotopic maps of sensorimotor cortex, and is also unlike the fractured somatotopy reported for the cerebellum.