Functional correlations between neighboring neurons in the primate globus pallidus are weak or nonexistent

Abstract

The anatomical structure of the basal ganglia displays topographical organization and massive funneling of neuronal projections toward the globus pallidus as well as an axonal collateral system within this nucleus. This structure suggests the formation of correlations between the spiking activities of pallidal cells. Nevertheless, previous studies of remote neurons in the pallidum have reported uncorrelated spiking activity. These correlation results may be challenged, because remote pallidal neurons may be located in different pallidal territories. To further test the independence of pallidal activity, we studied the spiking activity of neighboring pairs recorded by the same electrodes. A narrow peak dominated the correlations of all pairs of neurons recorded on the same electrode. This type of peak is classically interpreted as a sign of strong common input. However, recent mathematical analysis shows that such peaks may derive from a technical inability to detect overlapping spikes by spike-sorting techniques. A long-term shallow trough in the correlation of neighboring neurons may also result from the same effect, which we have termed the "shadowing effect." A comparison of the expected shadowing effect with the actual correlations suggests that no real correlations exist between 93.9% of neighboring pallidal pairs. The remaining 6.1% of the pairs display symmetric long-term positive correlations centered on time 0. Thus, functional interactions between neighboring pallidal neurons do not display any significant differences from the interactions between physically remote neurons in this brain area. Moreover, the combination of anatomical data and current physiological results suggests an active decorrelating process performed in the basal ganglia.

Figure 1.

Spike sorting of spikes from two neurons recorded on a single electrode. An example of off-line analysis of two cells recorded on the same electrode (990513s2e2) is shown. In the single spike examples (bottom), the actual spike shapes are depicted by the colors of the clusters, and principal-component reconstructions are plotted in black. The unidentified signal, composed of a green spike immediately followed (and distorted) by a purple spike, is shown in blue. In addition, the spike shapes of all of the spikes within the polygons are plotted (right).

Figure 2.

Observed correlation of two pallidal neurons recorded on the same electrode. a, Short-term (±50 msec) cross-correlogram of the two neurons shown in Figure 1 (990513s2c5-6). The insets contain the autocorrelation functions of the two neurons on the same time scale. b, Long-term (±5000 msec) cross-correlogram and autocorrelation functions of the same neurons. The y-axis (conditional firing rate) scale is enlarged, because the long-term phenomenon is relatively small in magnitude.

Figure 3.

Compensation for the shadowing effect reveals no correlation between pallidal neurons. a, Estimation of the shadowing factor out of the cross-correlogram (pair 990520s1c9-10) by calculating the areas with decreased correlation around time 0. The shaded area is the shadowing factor (i.e., the area used for the estimation of the shadowing effect). b, Histogram of the shadowing factors calculated for all of the pallidal pairs. c, e, Reconstructed cross-correlograms derived from the compensated autocorrelation functions and the estimated shadowing factor (pair 990520s1c9-10) showing the short-term (±50 msec) shape (c) and long-term (±5000 msec) shape (e). d, f, The recorded cross-correlogram (dots) is shown between the confidence (p < 0.01) limits (solid lines) derived from the reconstructed cross-correlogram for the same pair. The short-term (±50 msec) and long-term (±5000 msec) shape of the correlogram and the confidence limits are shown in d and f, respectively. The vertical dotted lines in c and d are the boundaries of the shadowed areas.