In cerebellar Purkinje cell dendrites, heterosynaptic calcium signaling induced by
the proximal climbing fiber (CF) input controls plasticity at distal parallel fiber
(PF) synapses. The substrate and regulation of this long-range dendritic calcium signaling
are poorly understood. Using high-speed calcium imaging, we examine the role of active
dendritic conductances. Under basal conditions, CF stimulation evokes T-type calcium
signaling displaying sharp proximodistal decrement. Combined mGluR1 receptor activation
and depolarization, two activity-dependent signals, unlock P/Q calcium spikes initiation
and propagation, mediating efficient CF signaling at distal sites. These spikes are
initiated in proximal smooth dendrites, independently from somatic sodium action potentials,
and evoke high-frequency bursts of all-or-none fast-rising calcium transients in PF
spines. Gradual calcium spike burst unlocking arises from increasing inactivation
of mGluR1-modulated low-threshold A-type potassium channels located in distal dendrites.
Evidence for graded activity-dependent CF calcium signaling at PF synapses refines
current views on cerebellar supervised learning rules.
