Short- and long-range synchronous activities in dimming detectors of the frog retina

In the visual system, nearby neurons of similar functional type have a tendency to fire synchronously. Cross-correlation analysis of spike discharges recorded from pairs of neurons has revealed that the synchronized activity is frequently associated with oscillatory firing patterns. However, the underlying neural mechanisms and functions of synchronization and oscillations are not well understood. In the present study, we simultaneously recorded spike discharges from multiple OFF-sustained type ganglion cells with no antagonistic surround (the dimming detectors) of the frog retina using a planar multi-electrode array and analyzed the temporal properties of light-evoked spike discharges. With full-field, temporally modulated diffuse illumination, cross-correlation analysis revealed the presence of the synchronous oscillatory pattern. The strength of the synchronized activity decreased slightly with increased intercellular distance. Synchronized spike discharges were detected even in cell pairs more than 2 mm apart. The frequency of oscillations peaked at approximately 30 Hz. The shuffled cross-correlogram was nearly flat, indicating that the synchronous oscillatory activities are most probably of neural origin. When GABA(A) antagonists were applied to the retina, oscillations were suppressed almost completely and the strength of the synchronized activity decreased with increased intercellular distance more sharply than control. When small spot illumination was applied to the overlapping receptive fields of an adjacent cell pair, a weak synchronized activity was evoked without accompanying oscillations. The same cell pair generated a strong synchronized activity accompanied with oscillations with full-field illumination. Our results suggest that local synchronous activities are generated via short-range neural interactions, and that the oscillatory activities are induced by long-range neural interactions and may contribute to the establishment of synchrony between widely separated neuronal populations.