RAPID REPORT: Initiation of simple and complex spikes in cerebellar Purkinje cells

Lucy M Palmer,Michael Häusser,Beverley A Clark,Greg J Stuart,Arnd Roth,Jan Gründemann

doi:10.1113/jphysiol.2010.188300

Lucy M Palmer, Michael Häusser + Show 4 more

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https://doi.org/10.1113/jphysiol.2010.188300

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Abstract

Cerebellar Purkinje cells produce two distinct forms of action potential output: simple and complex spikes. Simple spikes occur spontaneously or are driven by parallel fibre input, while complex spikes are activated by climbing fibre input. Previous studies indicate that both simple and complex spikes originate in the axon of Purkinje cells, but the precise location where they are initiated is unclear. Here we address where in the axon of cerebellar Purkinje cells simple and complex spikes are generated. Using extracellular recording and voltage-sensitive dye imaging in rat and mouse Purkinje cells, we show that both simple and complex spikes are generated in the proximal axon, ∼15–20 μm from the soma. Once initiated, simple and complex spikes propagate both down the axon and back into the soma. The speed of backpropagation into the soma was significantly faster for complex compared to simple spikes, presumably due to charging of the somatodendritic membrane capacitance during the climbing fibre synaptic conductance. In conclusion, we show using two independent methods that the final integration site of simple and complex spikes is in the proximal axon of cerebellar Purkinje cells, at a location corresponding to the distal end of the axon initial segment.

Highlights

Purkinje cells are the principal cells and the only output neurons of the cerebellar cortex, transmitting inhibitory signals to the deep cerebellar nuclei
Since extracellular voltage signals may be influenced by currents arising at distant locations we used simulations of extracellular action potentials (eAPs) generation in two compartmental models to verify that our recordings were dominated by local current sources in the initial segment and first node and that multisite extracellular recordings can distinguish between the initiation of spikes at these two locations
We used a previously published model (Clark et al 2005), in which action potentials were initiated at the first node of Ranvier, and modified it by adjusting ion channel densities so that action potentials were instead initiated in the axon initial segment

Summary

Introduction

Purkinje cells are the principal cells and the only output neurons of the cerebellar cortex, transmitting inhibitory signals to the deep cerebellar nuclei. The action potential output of Purkinje cells has been classified into two distinct types: simple spikes, which occur spontaneously (Hausser & Clark, 1997; Raman & Bean, 1997) and can exceed 100 Hz in response to excitation from parallel fibres (Eccles et al 1967; Thach, 1967); and complex spikes, which are triggered by climbing fibre excitation and consist of a characteristic high-frequency burst (Eccles et al 1967; Thach, 1967).

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