Functions of ventral visual cortex after bilateral hippocampal loss

Abstract

Repeated stimuli elicit attenuated responses in visual cortex relative to novel stimuli. This adaptation phenomenon can be considered a form of rapid learning and a signature of perceptual memory. Adaptation occurs not only when a stimulus is repeated immediately, but also when there is a lag in terms of time and other intervening stimuli before the repetition. But how does the visual system keep track of which stimuli are repeated, especially after long delays and many intervening stimuli? We hypothesized that the hippocampus supports long-lag adaptation, given that it learns from single experiences, maintains information over delays, and sends feedback to visual cortex. We tested this hypothesis with fMRI in an amnesic patient, LSJ, who has encephalitic damage to the medial temporal lobe resulting in complete bilateral hippocampal loss. We measured adaptation at varying time lags between repetitions in functionally localized visual areas that were intact in LSJ. We observed that these areas track information over a few minutes even when the hippocampus is unavailable. Indeed, LSJ and controls were identical when attention was directed away from the repeating stimuli: adaptation occurred for lags up to three minutes, but not six minutes. However, when attention was directed toward stimuli, controls now showed an adaptation effect at six minutes but LSJ did not. These findings suggest that visual cortex can support one-shot perceptual memories lasting for several minutes but that the hippocampus is necessary for adaptation in visual cortex after longer delays when stimuli are task-relevant.