Synaptic excitation by climbing fibre collaterals in the cerebellar nuclei of juvenile and adult mice

Abstract

The inferior olive conveys instructive signals to the cerebellum that drive sensorimotor learning. Inferior olivary neurons transmit their signals via climbing fibres, which powerfully excite Purkinje cells, evoking complex spikes and depressing parallel fibre synapses. Additionally, however, these climbing fibres send collaterals to the cerebellar nuclei (CbN). In vivo and in vitro data suggest that climbing fibre collateral excitation is weak in adult mice, raising the question of whether the primary role of this pathway may be developmental. We therefore examined climbing fibre collateral input to large premotor CbN cells over development by virally expressing channelrhodopsin in the inferior olive. In acute cerebellar slices from P12–14 mice, light-evoked EPSCs were large (>1 nA at −70 mV). The amplitude of these EPSCs decreased over development, reaching a plateau of ∼350 pA at P20–P60. Trains of EPSCs (5 Hz) depressed strongly throughout development, while convergence estimates indicated that the total number of functional afferents decreases with age. EPSC waveforms consisted of multiple peaks, likely resulting from action potential bursts in single collaterals and variable times to spike threshold in converging afferents. Activating climbing fibre collaterals evoked well-timed increases in firing probability in CbN neurons, especially in younger mice. The initially strong input, followed by the decrement in synaptic strength coinciding with the pruning of climbing fibres in the cerebellar cortex, implicates the climbing fibre collateral pathway in early postnatal development. Additionally, the persistence of substantial synaptic input at least to P60 suggests that this pathway may function in cerebellar processing into adulthood.

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