Feedback scales the spatial tuning of cortical responses during visual memory

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Perception, working memory, and long-term memory each evoke neural responses in visual cortex, suggesting that memory uses encoding mechanisms shared with perception. While previous research has largely focused on how perception and memory are similar, 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 of these conditions, BOLD responses were spatially tuned and were aligned with the target’s 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 systematically up the visual hierarchy from V1 to V2, V3, hV4, and beyond. In stark contrast, the widths of tuned responses were broad across the visual hierarchy during working memory and long-term memory, matched to the widths in perception in later visual field maps but much broader in V1. This pattern is consistent with the idea that mnemonic responses in V1 stem from top-down sources. Moreover, these tuned responses when biased (clockwise or counterclockwise of target) predicted matched biases in memory, suggesting that the readout of maintained and reinstated mnemonic responses influences memory guided behavior. We conclude that feedback constrains spatial tuning during memory, where earlier visual maps inherit broader tuning from later maps thereby impacting the precision of memory.

Significance Statement

We demonstrate that visual information that is seen, maintained in working memory, and retrieved from long-term memory evokes responses that differ in spatial extent within visual cortex. These differences depend on the origins of the visual inputs. Feedforward visual inputs during perception evoke tuned responses in early visual areas that increase in size up the visual hierarchy. Feedback inputs associated with memory originate from later visual areas with larger receptive fields resulting in uniformly wide spatial tuning even in primary visual cortex. 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.

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