The endoplasmic reticulum (ER) plays crucial roles in intracellular Ca2+ signaling, serving as both a source and sink of Ca2+, and regulating a variety of physiological and pathophysiological events in neurons in the brain. However, spatiotemporal Ca2+ dynamics within the ER in central neurons remain to be characterized. In this study, we visualized synaptic activity-dependent ER Ca2+ dynamics in mouse cerebellar Purkinje cells (PCs) using an ER-targeted genetically encoded Ca2+ indicator, G-CEPIA1er. We used brief parallel fiber stimulation to induce a local decrease in the ER luminal Ca2+ concentration ([Ca2+](ER)) in dendrites and spines. In this experimental system, the recovery of [Ca2+](ER) takes several seconds, and recovery half-time depends on the extent of ER Ca2+ depletion. By combining imaging analysis and numerical simulation, we show that the intraluminal diffusion of Ca2+, rather than Ca2+ reuptake, is the dominant mechanism for the replenishment of the local [Ca2+](ER) depletion immediately following the stimulation. In spines, the ER filled almost simultaneously with parent dendrites, suggesting that the ER within the spine neck does not represent a significant barrier to Ca2+ diffusion. Furthermore, we found that repetitive climbing fiber stimulation, which induces cytosolic Ca2+ spikes in PCs, cumulatively increased [Ca2+](ER). These results indicate that the neuronal ER functions both as an intracellular tunnel to redistribute stored Ca2+ within the neurons, and as a leaky integrator of Ca2+ spike-inducing synaptic inputs.