Neural information transferred from the putamen to the globus pallidus during learned movement in the monkey

Abstract

1. We studied the physiology of the neuronal projection from the striatum to the external and internal segments of the globus pallidus (GPe and GPi, respectively) in macaque monkeys. The objective of the study was to answer the following specific questions. 1) Which classes of the electrophysiologically identified striate neurons project to GPe and GPi? 2) What kind of information is transferred from the striatum to GPe and GPi during learned movement? 3) What are the physiological actions of striate projection neurons on target neurons in GPe and GPi? 4) What is the spatial pattern of the striatopallidal projections? 2. Sequential arm and orofacial movements were used as behavioral tasks. Visual stimuli triggered a sequence of three flexions-extensions of the elbow joint across the target, and the click of a solenoid valve triggered repetitive licking movements. 3. Striatopallidal projection neurons were electrophysiologically identified by antidromic activation after focal stimulation of either GPe or GPi. Of two classes of striate neurons, tonically active neurons (TANs) with tonic spontaneous discharges (2-8 imp/s) and broad action potentials, and phasically active neurons (PANs) with a very low spontaneous discharge rate (< 0.5 imp/ s) and high-frequency discharges in relation to behavioral tasks, PANs were identified as the projection neurons to either GPe or GPi. In 325 TANs examined by stimulation of GPe or GPi, no neuron was activated antidromically, even in the case of TANs located in the close vicinity of PANs that were identified as striatopallidal projection neurons. 4. The physiologically identified projection neurons (52 cells) in the striatum exhibited either discharges related to movement (30 cells) or discharges related to preparation for movement (4 cells) during performance of learned motor tasks. The activities of the remaining 17 striatopallidal neurons either were not related to the behavioral tasks used or could not be characterized sufficiently in the tasks. However, all of the unidentified striatopallidal neurons were PANs, on the basis of the spontaneous discharge rate and the shape of the action potential. 5. PANs with movement-related activity and those with preparation for movement-related activity were antidromically activated from the globus pallidus (GP). Not only the PANs that show burst discharges specifically at the beginning of a sequence of movement but also PANs that show phasic discharges time-locked to each movement of a sequence were identified as putaminopallidal projection neurons. On the other hand, no neurons that showed responses to sensory stimulus were identified as putaminopallidal neurons. 6. The conduction velocities of the putaminopallidal axons were estimated at approximately 1 m/s on the basis of the latency of antidromic activation and conduction distance. The PANs with activity only at the beginning of a sequential movement were more frequently found to project to GPi than to GPe, whereas the PANs with burst activity at each movement were more frequently found to project to GPe than to GPi. Among the GPi-projecting PANs, neurons with initial activity only showed a tendency to have longer latencies of activation from GPi than neurons with activity time-locked to each movement. 7. The physiological action of the striatopallidal projection was examined by switching from recording to microstimulation after identification of striatopallidal projection neurons in the putamen while recording evoked field potentials or spike discharges of single GP neurons located where the electrical stimulation evoked antidromic activation of the striate neurons with the lowest threshold. A small majority of GP neurons that exhibited increase of discharges during motor tasks received facilitatory putaminopallidal influences, whereas the vast majority of GP neurons that exhibited decrease of discharges during motor tasks received suppressive putaminopallidal influences.