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Pinpointing the neural signatures of single-exposure visual recognition memory

Significance Humans have a remarkable ability to remember images they have seen, even after seeing thousands, each only once and for a few seconds. One important step toward understanding how the primate brain supports this remarkable form of memory involves pinpointing the neural activity patterns that enable image memory behavior. This paper presents evidence this neural activity pattern is sensory referenced suppression: reductions in population response magnitude, corrected for sensory modulation. Memories of the images that we have seen are thought to be reflected in the reduction of neural responses in high-level visual areas such as inferotemporal (IT) cortex, a phenomenon known as repetition suppression (RS). We challenged this hypothesis with a task that required rhesus monkeys to report whether images were novel or repeated while ignoring variations in contrast, a stimulus attribute that is also known to modulate the overall IT response. The monkeys’ behavior was largely contrast invariant, contrary to the predictions of an RS-inspired decoder, which could not distinguish responses to images that are repeated from those that are of lower contrast. However, the monkeys’ behavioral patterns were well predicted by a linearly decodable variant in which the total spike count was corrected for contrast modulation. These results suggest that the IT neural activity pattern that best aligns with single-exposure visual recognition memory behavior is not RS but rather sensory referenced suppression: reductions in IT population response magnitude, corrected for sensory modulation.