Cortical Representations of Visual Stimuli Shift Locations with Changes in Memory States

Episodic memory retrieval is thought to rely on reactivation of the same content-sensitive neural activity patterns initially expressed during memory encoding.(1-6) Yet there are emerging examples of content representations expressed in different brain regions during encoding versus retrieval.(7-14) Although these differences have been observed by comparing encoding and retrieval tasks that differ in terms of perceptual experience and cognitive demands, there are many real-world contexts-e.g., meeting a new colleague who reminds you of an old acquaintance- where the memory system might be intrinsically biased either toward encoding (the new colleague) or retrieval (the old acquaintance).(15,16) Here, we test whether intrinsic memory states, independent of task demands, determine the cortical location of content representations. In a human fMRI study, subjects (n = 33) viewed object images and were instructed to either encode the current object or retrieve a similar object from memory. Using pattern classifiers, we show that biases toward encoding versus retrieval were reflected in large-scale attentional networks.(17-19) Critically, memory states decoded from these networks-even when entirely independent from task instructions-predicted shifts of object representations from visual cortex (encoding) to ventral parietal cortex (retrieval). Finally, visual versus ventral parietal cortices exhibited differential connectivity with the hippocampus during memory encoding versus retrieval, consistent with the idea that the hippocampus mediates cortical shifts in content representations. Collectively, these findings demonstrate that intrinsic biases toward memory encoding versus retrieval determine the specific cortical locations that express content information.