Microstimulation of the primate neostriatum. II. Somatotopic organization of striatal microexcitable zones and their relation to neuronal response properties

Abstract

Sensorimotor response properties of neostriatal neurons were characterized in conjunction with assessments of the motor effects of intrastriatal microstimulation in unanesthetized rhesus monkeys. Neuronal activity and microexcitability were assessed at 250- to 500-micron intervals and, in some cases, at 25- to 100-micron intervals. The results are based on the functional characterization of 878 putamen and 224 caudate neurons and analysis of the effects of microstimulation at each of these recording sites. Recording/stimulation sites were located between stereotaxic planes A6 and A22 in 81 microelectrode tracks from three monkeys. A total of 443 (50.4%) putamen neurons showed discrete responses to the sensorimotor examination. Of neurons with sensorimotor responses, 232 (52.4%) showed increased rates of discharge in relation to both active and passive movements of specific body parts. An additional 193 (43.6%) cells increased their rates of discharge only during the monkey's active movements of specific body parts. The remaining 18 (4.0%) cells appeared to respond exclusively to passive somatosensory stimulation. The sensorimotor response areas of putamen neurons ranged in size from an entire limb to a single joint. Putamen neurons were somatotopically organized throughout the rostrocaudal extent of the nucleus. Neurons with sensorimotor response areas involving the leg were located in the dorsolateral putamen, those with orofacial representations were located ventromedially, and those with arm representations were located in an intermediate position. Microstimulation evoked discrete movements of individual body parts at 21.6% of the 878 putamen sites. Over 95% (181/190) of the effective sites were located within the central half of the rostrocaudal extent of the putamen, between stereotaxic planes A10 and A17. The pattern of somatotopic organization revealed by microstimulation was the same as that derived from sensorimotor response properties of putamen neurons. Moreover, a close correspondence was observed between the movements evoked from a given SMZ and the functional properties of local neurons. In contrast to the results obtained in the putamen, none of the 224 stimulation sites in the caudate nucleus was microexcitable, and only 17 (7.6%) of the caudate neurons had definable sensorimotor response properties. This is consistent with the view that the primate putamen, by virtue of its anatomic connections with the sensorimotor and premotor cortical fields, is more directly involved in motor functions, whereas the caudate nucleus, by virtue of its connections with cortical ”association“ areas, is involved in more complex behavioral functions.