Aging and Alzheimer's disease (AD) are accompanied by impairments of autonomous navigation and spatial orientation that commonly demand the abandonment of driving and independent living. We have studied the neuronal mechanisms of navigation using single neurons in monkey cerebral cortex, finding a specific population of cells that processes the visual motion patterns of optic flow that provide important cues about self-movement. We have found that AD patients show pronounced deficits in the perceptual processing of optic flow, with different patterns of less severe impairment in mild cognitive impairment and cognitive aging. These perceptual deficits occur in subjects who show difficulties in real-world navigation that can be linked to visual associative processing impairments. Human neurophysiological recordings reveal a robust link between navigational capacity and cortical information processing in aging and AD. We conclude that visual information processing is progressively impaired in aging and AD. We speculate that these behavioral impairments reflect the progress of mechanistically linked cortical pathophysiologies that are manifestations of the fateful transition from cognitive aging to AD.