Cognitive decline after multiple brain-wide microstrokes is reported regularly in patients diagnosed with vascular dementia. However, the neuropathological mechanisms linking microstrokes to cognitive decline remain unclear, with no specific treatment options available. We present a mouse model to study hippocampal memory circuits in the healthy condition and after induction of cerebral microstrokes via microsphere injections. Mice are trained to navigate a virtual corridor while recording the same hippocampal neurons via chronic 2-photon calcium imaging before and after stroke for up to six weeks. Our approach allows tracking individual neurons in health and disease in relation to the cognitive performance in the spatial navigation task. We identify different classes of neurons based on their stability to encode for spatial information including stable and unstable place cells. While neurons in healthy networks largely maintain their function across days; this functional imprinting is disrupted in rewiring networks after stroke. Animals with full cognitive recovery exhibited a higher number of stable place cells than mice with a persistent cognitive deficit, where networks show a reduction in cross-session stability and quality of the neuronal representation of the corridor. Furthermore, we identified synchronicity of surviving neurons to be elevated in recovered mice, suggesting functional stability and neuronal synchronicity as protective mechanisms preventing cognitive decline. Our results provide insights into fundamental principles of network rewiring and reorganization as intrinsic repair mechanisms of the brain after multiple microstrokes, laying the basis for the development of novel therapeutic approaches or optimized cognitive rehabilitation strategies in vascular dementia.