Determinants of action potential propagation in cerebellar Purkinje cell axons

Axons have traditionally been viewed as highly faithful transmitters of action potentials. Recently, however, experimental evidence has accumulated to support the idea that under some circumstances axonal propagation may fail. Cerebellar Purkinje neurons fire high-frequency simple spikes, as well as bursts of spikes in response to climbing fiber activation ( the complex spike). Here we have visualized the axon of individual Purkinje cells to directly investigate the relationship between somatic spikes and axonal spikes using simultaneous somatic whole-cell and cell-attached axonal patch-clamp recordings at 200-800 mum from the soma. We demonstrate that sodium action potentials propagate at frequencies up to similar to260 Hz, higher than simple spike rates normally observed in vivo. Complex spikes, however, did not propagate reliably, with usually only the first and last spikes in the complex spike waveform being propagated. On average, only 1.7 +/- 0.2 spikes in the complex spike were propagated during resting firing, with propagation limited to interspike intervals above similar to4 msec. Hyperpolarization improved propagation efficacy without affecting total axonal spike number, whereas strong depolarization could abolish propagation of the complex spike. These findings indicate that the complex spike waveform is not faithfully transmitted to downstream synapses and that propagation of the climbing fiber response may be modulated by background activity.