During aging, microglia produce inflammatory factors, show reduced tissue surveillance, altered interactions with synapses, and prolonged responses to CNS insults, positioning these cells to have profound impact on the function of nearby neurons. We and others recently showed that microglial attributes differ significantly across brain regions in young adult mice. However, the degree to which microglial properties vary during aging is largely unexplored. Here, we analyze and manipulate microglial aging within the basal ganglia, brain circuits that exhibit prominent regional microglial heterogeneity and where neurons are vulnerable to functional decline and neurodegenerative disease. In male and female mice, we demonstrate that ventral tegmental area (VTA) and substantia nigra pars compacta (SNc) microglia exhibit unique and premature responses to aging, compared to cortex and nucleus accumbens (NAc) microglia. This is associated with localized VTA/SNc neuroinflammation that may compromise synaptic function...