Astroglia are an abundant and electrically non-excitable cell type in the brain, which can profoundly modify neuronal activity. For the latter, store-dependent calcium transients triggered by G-protein-coupled receptor are indispensable. Such calcium transients vary strongly in their spatial and temporal characteristics. They can be observed as fast, local elevations in small microdomains of the fine and fussy branches but also as large, slower waves propagating throughout a single branch, the whole astrocytic territory or even from cell to cell. While the functional relevance of these transients is well characterized, it is incompletely understood how the amplitude and waveform of these transients are controlled. The IP3 receptor type 2 is a key mediator of endoplasmic reticulum (ER)-dependent calcium elevations in astrocytes. The open probability of these receptors depends on the cytosolic calcium concentration. As the resting calcium concentration shows variations within and between astroglia, it could be responsible for site-specific scaling of calcium transients. To explore this hypothesis in acute brain slices and in vivo, we used two-photon excitation microscopy and quantified calcium concentrations and their changes by analyzing the fluorescence lifetime or intensity of suitable indicators. Independent of the type of calcium transients (spontaneous, agonist- or behavior-induced) and recording technique, we observed a positive correlation between the maximum (peak) of the transient and a negative correlation between the scale (amplitude) and the local cytosolic calcium concentration. Mechanistically, the latter relationship is linked to store-dependent calcium entry into the cytosol. Importantly, deliberately increasing or decreasing the cytosolic resting calcium concentration altered calcium transient peaks and amplitudes accordingly, which indicates that the local resting calcium concentration dynamically controls the scale of local calcium transients. In summary, our findings uncovered basic generic rules of calcium signal formation in astrocytes.