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Our data demonstrated brain region-specific microglial heterogeneity in young and old mice. In addition, sleep deprivation (SD) disrupted microglia and behaviors in an age-specific manner. Microglial density in the brain is significantly positively correlated with SD-induced hyperactivity in young mice. Contrarily, negative correlations are shown between the microglial density and behaviors in vehicle-treated young and old mice. [Display omitted] • Brain region-specific microglial heterogeneity in young and old mice. • Sleep deprivation disrupts microglia and behaviors in an age-specific manner. • Microglial density is positively correlated with SD-induced behaviors in youngs. • Microglial density is negatively correlated with behaviors in young and old mice. Microglia, resident immune cells in the central nervous system, constantly monitor the state of the surrounding brain activity. The animal model induced by sleep deprivation (SD) is widely used to study the pathophysiological mechanisms of insomnia and bipolar disorder. However, it remains unclear whether SD affects behaviors in young and aged male mice and microglia in various brain regions. In this study, we confirmed brain region-specific changes in microglial density and morphology in the accumbens nucleus (Acb), amygdala (AMY), cerebellum (Cb), corpus callosum (cc), caudate putamen, hippocampus (HIP), hypothalamus (HYP), medial prefrontal cortex (mPFC), and thalamus (TH) of young mice. In addition, the density of microglia in old mice was higher than that in young mice. Compared with young mice, old mice showed a markedly increased microglial size, decreased total length of microglial processes, and decreased maximum length. Importantly, we found that 48-h SD decreased microglial density and morphology in old mice, whereas SD increased microglial density and morphology in most observed brain regions in young mice. SD-induced hyperactivity was observed only in young mice but not in old mice. Moreover, microglial density (HIP, AMY, mPFC, CPu) was significantly positively correlated with behaviors in SD- and vehicle-treated young mice. Contrarily, negative correlations were shown between the microglial density (cc, Cb, TH, HYP, Acb, AMY) and behaviors in vehicle-treated young and old mice. These results suggest that SD dysregulates the homeostatic state of microglia in a region- and age-dependent manner. Microglia may be involved in regulating age-related behavioral responses to SD. [ABSTRACT FROM AUTHOR]