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The Journal of Neuroscience, July 23, 2008, 28(30):7599-7609; doi:10.1523/JNEUROSCI.0559-08.2008

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Cellular/Molecular
The Origin of the Complex Spike in Cerebellar Purkinje Cells

Jenny T. Davie, Beverley A. Clark, and Michael Häusser

Wolfson Institute for Biomedical Research and Department of Neuroscience, Physiology, and Pharmacology, University College London, London WC1E 6BT, United Kingdom

Correspondence should be addressed to Michael Häusser, Wolfson Institute for Biomedical Research, University College London, Gower Street, London WC1E 6BT, UK. Email: m.hausser{at}ucl.ac.uk

Activation of the climbing fiber input powerfully excites cerebellar Purkinje cells via hundreds of widespread dendritic synapses, triggering dendritic spikes as well as a characteristic high-frequency burst of somatic spikes known as the complex spike. To investigate the relationship between dendritic spikes and the spikelets within the somatic complex spike, and to evaluate the importance of the dendritic distribution of climbing fiber synapses, we made simultaneous somatic and dendritic patch-clamp recordings from Purkinje cells in cerebellar slices. Injection of large climbing fiber-like synaptic conductances at the soma using dynamic clamp was sufficient to reproduce the complex spike, independently of dendritic spikes, indicating that neither a dendritic synaptic distribution nor dendritic spikes are required. Furthermore, we found that dendritic spikes are not directly linked to spikelets in the complex spike, and that each dendritic spike is associated with only 0.24 ± 0.09 extra somatic spikelets. Rather, we demonstrate that dendritic spikes regulate the pause in firing that follows the complex spike. Finally, using dual somatic and axonal recording, we show that all spikelets in the complex spike are axonally generated. Thus, complex spike generation proceeds relatively independently of dendritic spikes, reflecting the dual functional role of climbing fiber input: triggering plasticity at dendritic synapses and generating a distinct output signal in the axon. The encoding of dendritic spiking by the post-complex spike pause provides a novel computational function for dendritic spikes, which could serve to link these two roles at the level of the target neurons in the deep cerebellar nuclei.

Key words: climbing fiber; Purkinje cell; cerebellum; dendritic spike; burst; axon

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Received Feb. 7, 2008; revised June 1, 2008; accepted June 2, 2008.

Correspondence should be addressed to Michael Häusser, Wolfson Institute for Biomedical Research, University College London, Gower Street, London WC1E 6BT, UK. Email: m.hausser{at}ucl.ac.uk

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