The brain extracellular matrix (ECM) is a lattice-like structure that occupies the intercellular space in the central nervous system (CNS). The ECM constituents are extremely long-lived and are widely believed to stabilize neurons and synapses in the brain. They are thought to be renewed only rarely, dependent on neuronal activity, by the activation of matrix metalloproteinases (MMPs) that cleave the existing ECM components, followed by de novo ECM protein synthesis. However, various studies have demonstrated that synapses change their structural organization on minutes to hours time scale, calling for additional mechanisms for ECM remodelling. Using advanced microscopy techniques, molecular biology tools and biochemical assays, we report here novel insights on the ECM dynamics. The proteoglycan neurocan (Ncan) frequently shifts between the neuronal surface ECM and astrocytic intracellular compartments. Ncan is secreted initially by glia cells and predominantly resides on their surfaces in young cultures. It is later transferred to neurons, and continues to shuttle between these cells throughout later developmental stages. Inhibiting this process with specific drugs or mutations results in Ncan accumulation in glia. Our findings challenge the prevailing view of ECM remodelling, highlighting a previously unknown mechanism of dynamic transcellular molecular exchanges within the CNS.