THE PRIMATE SUBTHALAMIC NUCLEUS .1. FUNCTIONAL-PROPERTIES IN INTACT ANIMALS

1. The present study tests several key aspects of the current model of the intrinsic circuitry of the basal ganglia, in particular the degre e to which basal ganglia-thalamocortical circuits are functionally seg regated at the level of the subthalamic nucleus (STN). To this end the responses of STN cells to somatosensory examination (n = 301 cells), the polarity and latencies of neuronal responses to passive and active movements (n = 223 cells), responses to microstimulation(n = 1589 sit es), and cross-correlation functions of pairs of neighboring neurons ( n = 72 pairs) were studied in STNs of three African green monkeys. 2. The activity of 55% of cells examined in STN was briskly modulated in response to passive movements of individual contralateral body parts. Of these, 86% responded to passive joint rotation of muscle palpation , but in some cases (25% of responding cells) responses were also elic ited by light touch. In 91% of the responding cells responses were eli cited by manipulations around a single joint only. 3. The caudoventral sector in STN was largely devoid of cells with responses to somatosen sory stimulation. Within the rostrodorsal zone a lateral region contai ning neurons that responded to arm movements and a more medial region with neurons responding to leg movement were found. Cells responding t o orofacial movements were located more dorsally and rostrally. Neuron s with similar responses to active and passive movements of the limbs tended to be clustered within ''arm'' and ''leg'' zones. 4. Of identif ied arm cells in STN (n = 80), 36% responded to the application of tor que pulses to the elbow (43 responses overall). Forty-eight percent of these cells responded to both extension and flexion torques. Ninety-t hree percent of the responses were initial increases in discharge, whi ch characteristically occurred earlier and were shorter than initial d ecreases. Fifty-three percent of the responses were biphasic or multip hasic. 5. During active step tracking movements 40% of STN arm cells ( n = 53 cells) responded with significant changes in activity. Thirty-s ix percent of these cells showed responses with both extension and fle xion movements. Of the responses, 90% were increases in discharge. Onl y 14% of all responses were biphasic or multiphasic. Responses tended to occur around the time of movement onset (average latency 2 ms after movement onset). 6. Microstimulation (bipolar pulses, 40 mu A, 200-50 0 ms train duration, 400 Hz) of the core of STN itself did not appear to produce movement. However, stimulation at the lateral borders of ST N and of the adjacent white matter often led to limb or eye movement. 7. Cross-correlation analysis of simultaneously recorded pairs of neur ons revealed significant synchronized activity in only 11% of pairs. 8 . The somatotopic arrangement of neuronal responses and the paucity of neighboring cells discharging in synchrony strongly support the conce pt of functional segregation in the basal ganglia-thalamocortical path ways. The predominance of brisk increases in discharge in STN in respo nse to movements most likely results from corticosubthalamic activatio n. The current model of basal ganglia anatomy predicts that this will lead to inhibition of movements. The inhibitory role of STN in motor c ontrol is further supported by the failure of electrical stimulation o f the nucleus to induce movements. The late onset of responses of STN neurons in the step tracking task suggests that STN and the ''indirect '' pathway are not involved in the selection or initiation of movement s, but may rather have a role in the control of ongoing movements.