Slow Oscillatory Discharge in the Primate Basal Ganglia

Abstract

Oscillations with periods in the multisecond range have previously been recorded in basal ganglia neurons of awake paralyzed rats, and in these animals were shown to be increased by systemic dopaminergic stimulation, but not altered by depletion of the nigrostriatal dopamine supply. To determine whether oscillations with frequencies below 0.5 Hz also exist in the primate basal ganglia, the spontaneous neuronal activity in the subthalamic nucleus (STN) and in the external and internal segments of the globus pallidus (GPe and GPi, respectively) was recorded with standard extracellular recording methods in two animals before and after treatment with the dopaminergic neurotoxin 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP). Oscillations with mean periods around 80 s were identified in 30% percent of GPe neurons, 36% of STN neurons, and 48% of GPi neurons. After recording in the normal state, the animals were rendered parkinsonian by intracarotid application of MPTP. This treatment resulted in a 30% reduction of the average discharge rate in GPe, a 47% increase of the average discharge rate in STN, and a 15% increase of the average discharge rate in GPi. However, there were no changes in the proportion of cells with slow oscillatory discharge. The oscillation frequencies were slightly increased in STN but remained unchanged in GPe and GPi. The results demonstrate that multisecond oscillations commonly occur in primate basal ganglia neurons and are unchanged by treatment with MPTP. The oscillations may have roles in fundamental functions of the basal ganglia-thalamocortical network, such as the regulation of the state of arousal.