This review emphasizes the importance of considering the synapse as a central driver of changes of navigation behavior in normative aging in mammals. Deeper understanding of age-related changes in synaptic plasticity and connectivity will lead to the identification of vulnerabilities in specific navigation circuits with age, as well as compensatory mechanisms that can preserve navigation function. These include age comparisons involving volumetric MRI studies, anatomical cell counts, and, where data are available, fMRI and electrophysiological measures of synaptic and network function in each of the brain structures that are thought to contribute to the complex range of behaviors associated with navigation. To better appreciate the parallel circuits and thus strategies that might be used by older individuals interchangeably during navigation, discussion in this chapter shifts away from known hierarchical levels of navigation. Methods such as virtual reality, which allow the manipulation of different sensory or motor signals available for navigation, support the idea of parallel circuits, particularly ones that are differentially affected by aging. Finally, existing computational models of navigation are examined in the context of aging for their potential contribution to understanding the observed agerelated differences in navigation circuits and behaviors. Throughout, existing gaps in our understanding of how normative aging impacts navigation are highlighted.