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⁺]_ERtakes 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⁺]_ERdepletion 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.SIGNIFICANCE STATEMENTCa²⁺is a key messenger that regulates neuronal functions in the brain. Although the endoplasmic reticulum (ER) plays indispensable roles as a source and sink of Ca²⁺, technical difficulties have impeded the analysis of Ca²⁺dynamics within the ER. In this study, we have used a genetically encoded ER Ca²⁺indicator to visualize Ca²⁺dynamics within the neuronal ER. We found that Ca²⁺-mobilizing synaptic inputs locally decreased the ER Ca²⁺concentration, followed by Ca²⁺replenishment by intraluminal Ca²⁺diffusion throughout the ER of dendrites and spines. Furthermore, Ca²⁺spike-inducing synaptic inputs cumulatively increased the Ca²⁺content of the ER. Thus, our study indicates that the ER functions both as a tunnel to redistribute stored Ca²⁺and as a leaky integrator of synaptic inputs.