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High-fidelity transmission of sensory information by single cerebellar mossy fibre boutons

Abstract

Understanding the transmission of sensory information at individual synaptic connections requires knowledge of the properties of presynaptic terminals and their patterns of firing evoked by sensory stimuli. Such information has been difficult to obtain because of the small size and inaccessibility of nerve terminals in the central nervous system. Here we show, by making direct patch-clamp recordings in vivo from cerebellar mossy fibre boutons—the primary source of synaptic input to the cerebellar cortex1,2—that sensory stimulation can produce bursts of spikes in single boutons at very high instantaneous firing frequencies (more than 700 Hz). We show that the mossy fibre–granule cell synapse exhibits high-fidelity transmission at these frequencies, indicating that the rapid burst of excitatory postsynaptic currents underlying the sensory-evoked response of granule cells3 can be driven by such a presynaptic spike burst. We also demonstrate that a single mossy fibre can trigger action potential bursts in granule cells in vitro when driven with in vivo firing patterns. These findings suggest that the relay from mossy fibre to granule cell can act in a ‘detonator’ fashion, such that a single presynaptic afferent may be sufficient to transmit the sensory message. This endows the cerebellar mossy fibre system with remarkable sensitivity and high fidelity in the transmission of sensory information.

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Figure 1: Properties of mossy fibre boutons in vitro and in vivo.
Figure 2: Sensory-evoked spiking in mossy fibre boutons and EPSCs in granule cells in vivo.
Figure 3: Synaptic dynamics at the mossy fibre–granule cell synapse in vivo and in vitro.
Figure 4: High-fidelity synaptic transmission at the mossy fibre–granule cell synapse in vivo and in vitro.
Figure 5: Input from a single mossy fibre reliably drives granule cell firing.

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Acknowledgements

We thank J. Geiger for guidance during the slice experiments; B. Clark, J. Davie, M. Farrant and A. Roth for comments on the manuscript; K. Kitamura, S. Komai and M. Rizzi for help with preliminary experiments; and L. Ramakrishnan and H. Cuntz for help with histology. This work was supported by grants from the European Union, Wellcome Trust and Gatsby Foundation (M.H.), and by a Wellcome Prize Studentship (E.A.R.), a Human Frontier Science Program Long-Term Fellowship (T.I.), a Wellcome Trust Advanced Training Fellowship (I.D.) and a University College London Graduate School Research Scholarship (P.C.).

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Correspondence to Michael Häusser.

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Rancz, E., Ishikawa, T., Duguid, I. et al. High-fidelity transmission of sensory information by single cerebellar mossy fibre boutons. Nature 450, 1245–1248 (2007). https://doi.org/10.1038/nature05995

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