Single cell studies of the primate putamen. I. Functional organization.

In order to clarify the functional organization of the putamen and the nature of sensory inputs to this structure we studied the relation of single cell activity to active movements and somatosensory stimulation in the awake primate. Neurons (N = 707) were categorized on the basis of their relation to active movements or responses to sensory stimulation of individual body parts. 38% of neurons studied were related to the arm, 9% to the leg, 11% to the mouth or face, and 3% to axial portions of the body. The remaining neurons exhibited non-specific activation which could not be confidently localized to an individual body part (12%) or did not respond during the examination (26%). The high proportion of arm neurons was due to the focus of this study on cells related to arm movements. A large proportion (41%; N = 270) of the "arm" neurons was responsive to somatosensory stimulation. For these neurons the most effective stimulus (82%) was passive joint rotation. Six (5%) of the arm neurons responded to cutaneous stimulation. The putamen was found to be somatotopically organized. Neurons related to different body parts (leg, arm, and face) were segregated, and each body part was represented over a long anteroposterior extent of the nucleus. Clusters of 2-5 neurons with similar relations to active movements or responsive to passive movements of a single joint were often encountered over a 100-500 mu distance. Clusters of neurons with sensory driving were organized by joints. Rather than a single elbow or shoulder area, multiple clusters of neurons related to each joint were widely distributed over a long anteroposterior extent of the nucleus and were adjacent to clusters of neurons related to other joints of the arm. These clusters of neurons with similar functional properties may correspond to the subunits of the striatum which have been revealed by anatomic and morphologic studies. We propose that these clusters of neurons with similar functional properties represent the basic functional units of the striatum in a manner analogous to the functional columns of the neocortex.