Feedback scales the spatial tuning of cortical responses during visual memory

Abstract

Perception, working memory, and long-term memory each evoke neural responses in visual cortex. While previous neuroimaging research on the role of visual cortex in memory has largely emphasized similarities between perception and memory, we hypothesized that responses in visual cortex would differ depending on the origins of the inputs. Using fMRI, we quantified spatial tuning in visual cortex while participants (both sexes) viewed, maintained in working memory, or retrieved from long-term memory a peripheral target. In each condition, BOLD responses were spatially tuned and aligned with the targets polar angle in all measured visual field maps including V1. As expected given the increasing sizes of receptive fields, polar angle tuning during perception increased in width up the visual hierarchy from V1 to V2, V3, hV4, and beyond. In stark contrast, the tuned responses were broad across the visual hierarchy during long-term memory (replicating a prior result) and during working memory. This pattern is consistent with the idea that mnemonic responses in V1 stem from top-down sources, even when the stimulus was recently viewed and is held in working memory. Moreover, in long-term memory, trial-to-trial biases in these tuned responses (clockwise or counterclockwise of target), predicted matched biases in memory, suggesting that the reinstated cortical responses influence memory guided behavior. We conclude that feedback widens spatial tuning in visual cortex during memory, where earlier visual maps inherit broader tuning from later maps thereby impacting the precision of memory. Significance StatementWe demonstrate that remembering a visual stimulus evokes responses in visual cortex that differ in spatial extent compared to seeing the same stimulus. Perception evokes tuned responses in early visual areas that increase in size up the visual hierarchy. Prior work showed that feedback inputs associated with long-term memory originate from later visual areas with larger receptive fields resulting in uniformly wide spatial tuning even in primary visual cortex. We replicate these results and show that the same pattern holds when maintaining in working memory a recently viewed stimulus. That trial-to-trial difficulty is reflected in the accuracy and precision of these representations suggests that visual cortex is flexibly used for processing visuospatial information, regardless of where that information originates.