Visual imagery is mediated via top-down activation of visual cortex. Similar to stimulus-driven perception, the neural configurations associated with visual imagery are differentiated according to content. For example, imagining faces or places differentially activates visual areas associated with perception of actual face or place stimuli. However, while top-down activation of topographically specific visual areas during visual imagery is well established, the extent to which internally generated visual activity resembles the fine-scale population coding responsible for stimulus-driven perception remains unknown. Here, we sought to determine whether top-down mechanisms can selectively activate perceptual representations coded across spatially overlapping neural populations. We explored the precision of top-down activation of perceptual representations using neural pattern classification to identify activation patterns associated with imagery of distinct letter stimuli. Pattern analysis of the neural population observed within high-level visual cortex, including lateral occipital complex, revealed that imagery activates the same neural representations that are activated by corresponding visual stimulation. We conclude that visual imagery is mediated via top-down activation of functionally distinct, yet spatially overlapping population codes for high-level visual representations.