In trained reaching rats, we recorded simple spikes of pairs of Purkinje cells that, with respect to each other, were either aligned on a beam of shared parallel fibers or instead were located off beam. Rates of simple spike firing in both on-beam and off-beam Purkinje cell pairs commonly showed great variety in depth of modulation during reaching behavior. But with respect to timing, on-beam Purkinje cell pairs had simple spikes that were tightly time-locked to each other (either delayed or simultaneous) and to movement, despite the variability in rate. By contrast, off-beam Purkinje cell pairs had simple spikes that were not time-locked to each other, neither delayed nor simultaneous. We discuss the implications of these observations for the cerebellar role in timing and coordinating movement.parallel fibers ͉ Purkinje cell ͉ simple spike ͉ awake reaching rat I n the mammalian cerebellar cortex, excitatory and inhibitory neuronal processes run in exactly perpendicular directions. This network provides a common excitatory input to neurons along the mediolateral (parallel-fiber on-beam) axis and a common inhibitory input to neurons along the anteriorposterior (parallel-fiber off-beam) axis. The anisotropic network is highly preserved across vertebrate species and has been proposed to be the basis of cerebellar control of timing and coordination of movement. In the original proposals (1, 2), on-beam Purkinje cells (Pcs) were hypothesized to be activated one by one in a strict temporal sequence by a traveling wave of parallel-fiber activity, the rate and timing of which were determined by parallel-fiber conduction velocity. To test this hypothesis, we recorded with multiple electrodes the simple spike (SS) activity of pairs of Pcs in awake trained rats as they reached for, grasped, and returned a food pellet to the mouth. We found that on-beam pairs of Pcs generated two types of temporally correlated SS activity. In one type, there was a delay of the second SS with respect to the first that was proportionate to the parallelfiber conduction velocity. However, this delayed correlation was observed rarely, was weak when present, and was poorly timelocked to movement. In the second type of on-beam SS correlation, the SSs of the Pc pairs occurred simultaneously with no delay and were precisely synchronized. This synchronous onbeam correlation was common (observed in SSs of almost all Pc pairs), was robust when present, and was precisely time-locked to movement. By contrast, the SSs of off-beam Pc pairs were not correlated with each other (neither delayed nor synchronous). We discuss the possibility that the observed Pc SS on-beam synchrony that is time-locked to movement may be the organizing principle for the cerebellar timing and coordination of movement.
ResultsWe recorded SS activity from the Pc layer of the cerebellar cortex of awake reaching rats (see Fig. 5 in Materials and Methods). SS activity in the paramedian lobe was strongly modulated during performance of reaching and grasping movements (Fig. 1). We recor...