The Stromal interaction molecule 1 (STIM1), is an ER-Ca²⁺ sensor and an essential component of ER-Ca²⁺ store operated Ca²⁺ entry (SOCE). Loss of STIM1 affects metabotropic Glutamate Receptor 1 (mGluR1) mediated synaptic transmission, neuronal Ca²⁺ homeostasis and intrinsic plasticity in Purkinje Neurons (PNs). Long-term changes of intracellular Ca²⁺ signaling in PNs lead to neurodegenerative conditions, as evident in individuals with mutations of the ER-Ca²⁺ channel, the Inositol 1,4,5-triphosphate receptor (IP₃R). Here, we asked if changes in such intrinsic neuronal properties, due to loss of STIM1, have an age-dependent impact on PNs. Consequently, we analyzed mRNA expression profiles and cerebellar morphology in PN specific STIM1 knockout mice (STIM1^PKO ) of both sexes across ages. Our study identified a requirement for STIM1 mediated Ca²⁺ signaling in maintaining the expression of genes belonging to key biological networks of synaptic function and neurite development amongst others. Gene expression changes correlated with altered patterns of dendritic morphology and greater innervation of PN dendrites by climbing fibers, in ageing STIM1^PKO mice. Together, our data identify STIM1 as an important regulator of Ca²⁺ homeostasis and neuronal excitability in turn required for maintaining the optimal transcriptional profile of PNs with age. Our findings are significant in the context of understanding how dysregulated calcium signals impact cellular mechanisms in multiple neurodegenerative disorders.Significance StatementIn Purkinje neurons (PNs) the Stromal interaction molecule 1 (STIM1) is required for mGluR1-dependent synaptic transmission, refilling of ER Ca²⁺ stores, regulation of spike frequency and cerebellar memory consolidation. Here, we provide evidence for a novel role of STIM1 in maintaining the gene expression profile and optimal synaptic connectivity of PNs. Expression of genes related to neurite development and synaptic organization networks are altered in PNs with persistent loss of STIM1. In agreement with these findings the dendritic morphology of PNs and climbing fiber innervations on PNs also undergo significant changes with age. These findings identify a new role for dysregulated intracellular calcium signaling in neurodegenerative disorders and provide novel therapeutic insights.