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The Journal of Neuroscience, June 24, 2009, 29(25):8005-8015; doi:10.1523/JNEUROSCI.4919-08.2009

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Behavioral/Systems/Cognitive
Spatial Pattern Coding of Sensory Information by Climbing Fiber-Evoked Calcium Signals in Networks of Neighboring Cerebellar Purkinje Cells

Simon R. Schultz,^1,2,3 Kazuo Kitamura,² Arthur Post-Uiterweer,¹ Julija Krupic,¹ and Michael Häusser²

¹Department of Bioengineering, Imperial College London, South Kensington, London SW7 2AZ, United Kingdom, ²Wolfson Institute for Biomedical Research and Department of Neuroscience, Physiology and Pharmacology, University College London, London WC1E 6BT, United Kingdom, and ³Gatsby Computational Neuroscience Unit, University College London, London WC1N 3AR, United Kingdom

Correspondence should be addressed to either of the following: Simon R. Schultz, Department of Bioengineering, Imperial College London, South Kensington, London SW7 2AZ, UK, Email: s.schultz{at}imperial.ac.uk; or Michael Häusser, Wolfson Institute for Biomedical Research, University College London, London WC1E 6BT, UK, Email: m.hausser{at}ucl.ac.uk

Climbing fiber input produces complex spike synchrony across populations of cerebellar Purkinje cells oriented in the parasagittal axis. Elucidating the fine spatial structure of this synchrony is crucial for understanding its role in the encoding and processing of sensory information within the olivocerebellar cortical circuit. We investigated these issues using in vivo multineuron two-photon calcium imaging in combination with information theoretic analysis. Spontaneous dendritic calcium transients linked to climbing fiber input were observed in multiple neighboring Purkinje cells. Spontaneous synchrony of calcium transients between individual Purkinje cells falls off over 200 µm mediolaterally, consistent with the presence of cerebellar microzones organized by climbing fiber input. Synchrony was increased after administration of harmaline, consistent with an olivary origin. Periodic sensory stimulation also resulted in a transient increase of synchrony after stimulus onset. To examine how synchrony affects the neural population code provided by the spatial pattern of complex spikes, we analyzed its information content. We found that spatial patterns of calcium events from small ensembles of cells provided substantially more stimulus information (59% more for seven-cell ensembles) than available by counting events across the pool without taking into account spatial origin. Information theoretic analysis indicated that, rather than contributing significantly to sensory coding via stimulus dependence, correlational effects on sensory coding are dominated by redundancy attributable to the prevalent spontaneous synchrony. The olivocerebellar circuit thus uses a labeled line code to report sensory signals, leaving open a role for synchrony in flexible selection of signals for output to deep cerebellar nuclei.

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Received Oct. 9, 2008; revised May 7, 2009; accepted May 16, 2009.

Correspondence should be addressed to either of the following: Simon R. Schultz, Department of Bioengineering, Imperial College London, South Kensington, London SW7 2AZ, UK, Email: s.schultz{at}imperial.ac.uk; or Michael Häusser, Wolfson Institute for Biomedical Research, University College London, London WC1E 6BT, UK, Email: m.hausser{at}ucl.ac.uk

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