Parallel fibers synchronize spontaneous activity in cerebellar Golgi cells

Cerebellar Golgi cells inhibit their afferent interneurons, the excitatory granule cells. Such a feedback inhibition causes both inhibitory and excitatory neurons in the circuit to synchronize. Our modeling work predicts that the long granule cell axons, the parallel fibers, entrain many Golgi cells and their afferent granule cells in a single synchronous rhythm. Spontaneous activity of 42 pairs of putative Golgi cells was recorded in anesthetized rats to test these predictions. In 25 of 26 pairs of Golgi cells that were positioned along the transverse axis, and presumed to receive common parallel fiber input, spontaneous activity showed a high level of coherence (mean Z score > 6). Conversely, 12 of 16 Golgi cell pairs positioned along the parasagittal axis (no common parallel fiber input) were not synchronized; 4 of 16 of them showed only low levels of synchronicity (mean Z score < 4). For transverse pairs the accuracy of the coherence, measured as the width at half-height of the central peak of the cross-correlogram, was rather low (29.8 +/- 12.5 msec) but increased with Golgi cell firing rate, as predicted by the model. These results suggest that in addition to their role as gain controllers, cerebellar Golgi cells may control the timing of granule cell spiking.