Memory responses in visual cortex track recall success after single-trial encoding

Abstract

Episodic memory retrieval is thought to rely on the reactivation of prior perceptual representations in sensory cortex, a phenomenon known as cortical reinstatement. Support for this idea in early sensory areas comes from memory studies involving repeated exposure and explicit recall instructions. In everyday life, however, people rely on details from single events without repeated practice or instruction. We used fMRI to test whether memory responses emerge in early visual cortex after a single encoding event. Twenty adults viewed objects presented once in one of four parafoveal locations, then later completed object recognition (old/new) and location recall tasks in which objects were shown foveally. Both memory tasks evoked spatially tuned, albeit substantially lower amplitude, responses compared to encoding in V1 to V3. These responses were tuned to the encoded parafoveal location, even though the recognition task did not ask the participant to remember the encoded location. These responses were more robust and precise for successfully remembered items, linking neural tuning in early visual cortex to one-shot memory performance. Our findings demonstrate that early visual cortex supports the defining property of episodic memory, the ability to retrieve sensory details from a single event. Significance StatementEpisodic memory allows us to vividly recall details from single past experiences. While it is hypothesized that this "mental time travel" relies on reactivating sensory cortex, previous studies used highly practiced associations or explicit visualization cues, which differ from how we naturally recall unique events. In this fMRI study, participants viewed a stream of unique objects at parafoveal locations. We found that later retrieval of these objects spontaneously reactivated early visual cortex in a spatially specific manner even when spatial location was not probed: The memory reactivated the same retinotopic location where the object initially appeared. Furthermore, the precision of this reactivation predicted memory success. These findings demonstrate that sensory cortex is fundamental to the rapid, one-shot learning that characterizes human episodic memory.