The temporal structure of spike trains in the primate basal ganglia: afferent regulation of bursting demonstrated with precentral cerebral cortical ablation

Abstract

We studied the temporal pattern of discharge of single units in the basal ganglia of awake primates sitting quietly. Bursting was studied with a procedure that identified individual bursts in a spike train, quantifying burst intensity (surprise), bursts per 1000 spikes, spikes per burst and burst length. Autocorrelation techniques were used to assess the dependencies of spike trains on the temporal order of intervals. Striatal units had a greater tendency to burst (79% of units) than pallidal units (50%). The caudate nucleus and putamen had nearly identical burst properties on all measures. In the pallidum, bursting was more prevalent in the external segment and bursts were more intense and more frequent than in the internal segment. The autocorrelation analysis revealed that the temporal structure of the spike train was more dependent on the order of intervals in the striatum than in the pallidum. Bursting units had an increased probability of discharge after each spike and the relative refractory period was shorter in bursting units than units without bursts. Very few units exhibited cyclic discharge properties. Ablations of areas 4 and 6 in the precentral cortex demonstrated that striatal bursting was under afferent control. The putamen, which receives more cortical afferents from areas 4 and 6 than the caudate nucleus, had fewer and less intense bursts after the afferents were lesioned. Burst intensity did not change in the pallidum after the lesion. The findings indicate that bursting properties contribute to discharge variability in the basal ganglia and suggest that information transfer in the striatum may utilize bursts. In contrast, rate coding may be a more important mechanism for units in the pallidum.